Papers I have published with my collaborators
(104) Freitas B., P. B. D’Amelio, B. Milá, C. Thébaud, & T. Janicke. In the press. Meta-analysis of the acoustic adaptation hypothesis reveals no support for the effect of vegetation structure on acoustic signalling across terrestrial vertebrates. Biological Reviews
Acoustic communication plays a prominent role in various ecological and evolutionary processes involving social interactions. The properties of acoustic signals are thought to be influenced not only by the interaction between signaller and receiver but also by the acoustic characteristics of the environment through which the signal is transmitted. This conjecture forms the core of the so-called “acoustic adaptation hypothesis” (AAH), which posits that vegetation structure affects frequency and temporal parameters of acoustic signals emitted by a signaller as a function of their acoustic degradation properties. Specifically, animals in densely vegetated ‘closed habitats’ are expected to produce longer acoustic signals with lower repetition rates and lower frequencies (minimum, mean, maximum, and peak) compared to the ones inhabiting less vegetated ‘open habitats’. To date, this hypothesis has received mixed results, with the level of support depending on the taxonomic group and the methodology used. We conducted a systematic literature search of empirical studies testing for an effect of vegetation structure on acoustic signalling and assessed the generality of the AAH using a meta-analytic approach based on 371 effect sizes from 75 studies and 57 taxa encompassing birds, mammals and amphibians. Overall, our results do not provide consistent support for the AAH, neither in within-species comparisons (suggesting no overall phenotypically plastic response of acoustic signalling to vegetation structure) nor in among-species comparisons (suggesting no overall evolutionary response). However, when considering birds only, we found a weak support for the AAH in within-species comparisons, which was mainly driven by studies that measured frequency bandwidth, suggesting that this variable may exhibit a phenotypically plastic response to vegetation structure. For among-species comparisons in birds, we also found support for the AAH, but this effect was not significant after excluding comparative studies that did not account for phylogenetic non-independence. Collectively, our synthesis does not support a universal role of vegetation structure in the evolution of acoustic communication. We highlight the need for more empirical work on currently under-studied taxa such as amphibians, mammals, and insects. Furthermore, we propose a framework for future research on the AAH. We specifically advocate for a more detailed and quantitative characterization of habitats to identify frequencies with the highest detection probability and to determine if frequencies with greater detection distances are preferentially used. Finally, we stress that empirical tests of the AAH should focus on signals which are selected for increased transmission distance.
(103) Matthews, T, Triantis, K, Wayman, JP, Martin, TE, Hume, JP, Cardoso, P, Faurby, S, Mendenhall, C, Dufour, P, Rigal, F, Cooke, R, Whittaker, RJ, Pigot, AL, Thébaud, C, Jørgensen, MW, Benavides Rios, E, Soares, F, Ulrich, W, Kubota, Y, Sadler, J, Tobias, JA & Sayol, F 2024. The global loss of avian functional and phylogenetic diversity from anthropogenic extinctions. Science 386(6717):55-60. doi: 10.1126/science.adk7898. Epub 2024 Oct 3. PMID: 39361743.
Humans have been driving a global erosion of species richness for millennia, but the consequences of past extinctions for other dimensions of biodiversity—functional and phylogenetic diversity—are poorly understood. In this work, we show that, since the Late Pleistocene, the extinction of 610 bird species has caused a disproportionate loss of the global avian functional space along with ~3 billion years of unique evolutionary history. For island endemics, proportional losses have been even greater. Projected future extinctions of more than 1000 species over the next two centuries will incur further substantial reductions in functional and phylogenetic diversity. These results highlight the severe consequences of the ongoing biodiversity crisis and the urgent need to identify the ecological functions being lost through extinction.
(102) Poutaraud J., J. Sueur, C. Thébaud & S. Haupert. 2024. Meta-embedded clustering (MEC): A new method for improving
clustering quality in unlabeled bird sound datasets. Ecological Informatics 82: 102687
In recent years, ecoacoustics has offered an alternative to traditional biodiversity monitoring techniques with the development of passive acoustic monitoring (PAM) systems allowing, among others, to detect and identify species that are difficult to detect by human observers, automatically. PAM systems typically generate large audio datasets, but using these monitoring techniques to infer ecologically meaningful information remains challenging. In most cases, several thousand hours of recordings need to be manually labeled by experts limiting the operability of the systems. Based on recent developments of meta-learning algorithms and unsupervised learning techniques, we propose here Meta-Embedded Clustering (MEC), a new method with high potential for improving clustering quality in unlabeled bird sound datasets. MEC method is organized in two main steps, with: (a) fine-
tuning of a pretrained convolutional neural network (CNN) backbone with different meta-learning algorithms using pseudo-labeled data, and (b) clustering of manually-labeled bird sounds in the latent space based on vector embeddings extracted from the fine-tuned CNN. The MEC method significantly enhanced average clustering performance from less than 1% to more than 80%, greatly outperforming the traditional approach of relying solely on CNN features extracted from a general neotropical audio database. However, this enhanced performance came with the cost of excluding a portion of the data categorized as noise. By improving the quality of clustering in unlabeled bird sound datasets, the MEC method should facilitate the work of ecoacousticians in managing acoustic units of bird song/call clustered according to their similarities, and in identifying potential clusters of species undetected using traditional approaches.
(101) Cornuault J, M. Sanchez, T. Duval, A. Fouquet, & C. Thébaud. 2024. Deep genetic divergence underlies within-island eco-morphological variation in the endangered day gecko Phelsuma borbonica: implications for conservation. Conservation Genetics 25: 1035–1052. https://doi.org/10.1007/s10592-024-01622-w
The day gecko Phelsuma borbonica displays marked differences in coloration and occupies a variety of habitats across its very small range on the volcanic oceanic island of Reunion in the southwestern Indian Ocean. Such differences might reflect geographic and ecological divergence and thus be associated with an underlying genetic differentiation. We examined the partitioning of genetic diversity in Phelsuma borbonica across Reunion at a very small spatial scale (< 10 km) using mtDNA and nuDNA sequences, along with microsatellite genotype data. This study provides an account of the evolutionary history of Phelsuma borbonica, along with a quantification of effective population sizes, which constitute important information for the conservation of this endangered species, which may represent a previously unrecognized case of ncipient speciation. We found that populations of Phelsuma borbonica are genetically strongly differentiated, highlighting historically low levels of gene flow. Phylogenetic analyses suggest that Phelsuma borbonica reached its present range through two parallel southward expansions from an ancestral population located in the northern part of the island.
(100) Kitching R.L., C. Wenda,· J. Rochat,· C. Thébaud, · D. Strasberg, · K. Vogiatzis, ·S. Xing, & · L. A. Ashton. 2024. Diversity and turnover in moth assemblages in rainforests on a remote oceanic island. Biodiversity and Conservation 33 : 2265–2284. https://doi.org/10.1007/s10531-024-02874-1
Spatially driven turnover in species composition and relative abundance drives gamma diversity in all ecosystems. Assemblages of nocturnal Lepidoptera in rainforests are powerful tools for estimating and understanding this heterogeneity. There are three fundamental theoretical tools for explaining this place-to-place change: neutral stochasticity, niche-driven opportunity and historical contingency. We sampled moth and woody plant assemblages across the oceanic island landscape of La Réunion to tease apart how these factors shape diversity. We collected a total of ~ 13000 individuals of about 229 species and analyzed how distance and forest habitats shape moth assemblage turnover. We subdivided moth species into endemics and non-endemics. Our results show the local occurrence of the generally more diet-restricted endemic moths is more likely to be niche-driven due to host-plant preferences while occurrence of the generally more polyphagous non-endemic species is most parsimoniously explained by stochastic neutral mechanisms. Spatial patterns in the native flora may also be neutrally assembled sets across the rainforest region
(with implications for native moth species) whereas introduced species reflect human-driven historical contingency.
(99) Vacher J.-P., , P.J..R. Kok, M.T. Rodrigues, A. Lima, T. Hrbek, F.P. Werneck, S. Manzi, C. Thébaud, & A. Fouquet, 2024. Diversification of the terrestrial frog genus Anomaloglossus (Anura, Aromobatidae) in the Guiana Shield proceeded from highlands to lowlands, with successive loss and reacquisition of endotrophy, Molecular Phylogenetics and Evolution doi: 10.1016/j.ympev.2023.108008. Epub 2024 Jan 3. PMID: 38181828.
Two main landscapes emerge from the Guiana Shield: the highlands to the west called the Pantepui region and the Amazonian lowlands to the east, both harbouring numerous endemic species. With 32 currently recognized species, the genus Anomaloglossus stands out among Neotropical frogs as one that diversified only within the Guiana Shield both in the highlands and the lowlands. We present a time-calibrated phylogeny obtained by using combined mitogenomic and nuclear DNA, which suggests that the genus originates from Pantepui where extant lineages started diversifying around 21 Ma, and subsequently (ca. 17 Ma) dispersed during the Miocene Climatic Optimum to the lowlands of the eastern Guiana Shield where the ability to produce endotrophic tadpoles evolved. Further diversification within the lowlands in the A. stepheni group notably led to an evolutionary reversal toward exotrophy in one species group during the late Miocene, followed by reacquisition of endotrophy during the Pleistocene. These successive shifts of reproductive mode seem to have accompanied climatic oscillations. Long dry periods might have triggered evolution of exotrophy, whereas wetter climates favoured endotrophic forms, enabling colonization of terrestrial habitats distant from water. Acquisition, loss, and reacquisition of endotrophy makes Anomaloglossus unique among frogs and may largely explain the current species diversity. The micro evolutionary processes involved in these rapid shifts of reproductive mode remain to be revealed.
(98) Ferreira F., Kraus F., Richards S., Oliver P., Günther R., Trilaksono W., Arida E.A., Amidy A., Riyanto A., Tjaturadi B., Thébaud C., Fouquet A. 2023. Species delimitation and phylogenetic analyses of a New Guinean frog genus (Microhylidae: Hylophorbus) reveal many undescribed species and a complex diversification history driven by late Miocene events. Zoological Journal of the Linnean Society, Volume 202, Issue 2, https://doi.org/10.1093/zoolinnean/zlad168
New Guinea is the largest tropical island in the world and hosts immense endemic biodiversity. However, our understanding of how the gradual emergence of the terrestrial ecosystems of the island over the last 40 Myr has generated this biological richness is hampered by poorly documented species diversity and distributions. Here, we address both these issues through an integrative taxonomy and biogeographical approach using Hylophorbus, a New Guinea-endemic genus of frogs with 12 recognized species. We delimited candidate species by integrating mitochondrial DNA, nuclear DNA, and bioacoustics, then investigated their evolutionary history. Our results suggest that the current taxonomy of the genus misses true species diversity by ≥3.5-fold. Nevertheless, most candidate species (27) remain unconfirmed because of missing data, whereas five were identified unambiguously as undescribed (we describe three of these formally). Time-calibrated phylogenetic analyses suggest that Hylophorbus diversification began ~9 Mya in the northern or eastern portion of New Guinea. It would appear that lineages dispersed to new terrestrial habitats in the west, notably uplifted by the central range orogeny, until eventually reaching the Bird’s Head during the Mio-Pliocene (7–5 Mya). Conversely, a past barrier appears to have prevented north–south dispersal. These data suggest that new habitat availability has primarily driven the diversification of Hylophorbus.
(97) Gabrielli M., T. Leroy, J. Salmona, B. Nabholz, Borja Milá, & C. Thébaud. 2024. Demographic responses of oceanic island birds to local and regional ecological disruptions revealed by whole-genome sequencing. Molecular Ecology 33(4):e17243. doi: 10.1111/mec.17243. Epub 2023 Dec 18. PMID: 38108507.
Disentangling the effects of ecological disruptions operating at different spatial and temporal scales in shaping past species' demography is particularly important in the current context of rapid environmental changes driven by both local and regional factors. We argue that volcanic oceanic islands provide useful settings to study the influence of past ecological disruptions operating at local and regional scales on population demographic histories. We investigate potential drivers of past population dynamics for three closely related species of passerine birds from two volcanic oceanic islands, Reunion and Mauritius (Mascarene archipelago), with distinct volcanic history. Using ABC and PSMC inferences from complete genomes, we reconstructed the demographic history of the Reunion Grey White-eye (Zosterops borbonicus (Pennant, 1781)), the Reunion Olive White-eye (Z. olivaceus (Linnaeus, 1766)) and the Mauritius Grey White-eye (Z. mauritianus (Gmelin, 1789)) and searched for possible causes underlying similarities or differences between species living on the same or different islands. Both demographic inferences strongly support ancient and long-term expansions in all species. They also reveal different trajectories between species inhabiting different islands, but consistent demographic trajectories in species or populations from the same island. Species from Reunion appear to have experienced synchronous reductions in population size during the Last Glacial Maximum, a trend not seen in the Mauritian species. Overall, this study suggests that local events may have played a role in shaping population trajectories of these island species. It also highlights the potential of our conceptual framework to disentangle the effects of local and regional drivers on past species' demography and long-term population processes.
(96) Mould MC, M. Huet, L. Senegas, B. Mila, C. Thébaud, Y. Bourgeois & A. Chaine. 2023. Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird. Journal of evolutionary Biology 36, 82-94
Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.
(95) Utami CY, A Sholihah, FL Condamine, C Thébaud, N Hubert. 2022. Cryptic diversity impacts model selection and macroevolutionary inferences in diversification analyses. Proceedings of the Royal Society B 289(1987):20221335. doi: 10.1098/rspb.2022.1335. Epub 2022 Nov 16. PMID: 36382998; PMCID: PMC9667750.
Species persist in landscapes through ecological dynamics but proliferate at wider spatial scales through evolutionary mechanisms. Disentangling the contribution of each dynamic is challenging, but the increasing use of dated molecular phylogenies opened new perspectives. First, the increasing use of DNA sequences in biodiversity inventory shed light on a substantial amount of cryptic diversity in species-rich ecosystems. Second, explicit diversification models accounting for various eco-evolutionary models are nowavailable. Integrating both advances, we explored diversification trajectories among 10 lineages of freshwater fishes in Sundaland, for which time-calibrated and taxonomically rich phylogenies are available. By fitting diversification models to dated phylogenies and incorporatingDNA-based species delimitation methods, the impact of cryptic diversity on diversification model selection and related inferences is explored. Eight clades display constant speciation rate model as the most likely if cryptic diversity is accounted, but nine display a signature of diversification slowdownswhen cryptic diversity is ignored. Cryptic diversification occurs during the last 5 Myr for most groups, and palaeoecologicalmodels received little support. Most cryptic lineages display restricted range distribution, supporting geographical isolation across homogeneous landscapes as the main driver of diversification. These patterns question the persistence of cryptic diversity and its role during species proliferation.
(94) Matthews Thomas J, Joseph P Wayman, Pedro Cardoso, Ferran Sayol, Julian P Hume, Werner Ulrich, Joseph A Tobias, Filipa C Soares, Christophe Thébaud, Thomas E Martin, Kostas A Triantis. 2022. Threatened and extinct island endemic birds of the world: Distribution, threats and functional diversity. Journal of Biogeography 49, 1920-1940
The world's islands support disproportionate levels of endemic avian biodiversity despite suffering numerous extinctions. While intensive recent research has focused on island bird conservation or extinction, few global syntheses have considered these factors together from the perspective of morphological trait diversity. Here, we provide a global summary of the status and ecology of extant and extinct island birds, the threats they face and the implications of species loss for island functional diversity.. Here we provide a review of the literature on threatened and extinct island birds, with a particular focus on global studies that have incorporated functional diversity. Alongside this, we analyse IUCN Red List data in relation to distribution, threats and taxonomy. Using null models and functional hypervolumes, in combination with morphological trait data, we assess the functional diversity represented by threatened and extinct island endemic birds. We find that almost half of all island endemic birds extant in 1500 CE are currently either extinct or threatened with extinction, with the majority of threatened extant species having declining population trends. We also found evidence of 66 island endemic subspecies extinctions. The primary threats to extant island endemic birds currently are agriculture, biological resource use, and invasive species. While there is overlap between the hotspots of threatened and extinct island endemics birds, there are some notable differences, including the Philippines and Indonesia, which support a substantial number of threatened species but have no recorded post-1500 CE bird extinctions. Traits associated with threatened island endemic birds are large body mass, flightlessness, aquatic predator, omnivorous and vertivorous trophic niches, marine habitat affinity, and, paradoxically, higher dispersal ability. Critically, we find that threatened endemics (i) occupy distinct areas of beak morphospace, and (ii) represent substantial unique areas of the overall functional space of island endemics. We caution that the loss of threatened species may have severe effects on the ecological functions birds provide on islands.
(93) Emerson Brent , Paulo Borges, Pedro Cardoso, Peter Convey, Jeremy deWaard, Evan Economo, Rosemary Gillespie, Susan Kennedy, Henrik Krehenwinkel, Rudolf Meier, George Roderick, Dominique Strasberg, Christophe Thébaud, Anna Traveset, Thomas Creedy, Emmanouil Meramveliotakis, Victor Noguerales, Isaac Overcast, Hélène Morlon, Anna Papadopoulou, Alfried Vogler, Paula Arribas, Carmelo Andujar. 2022. Collective and harmonised high throughput barcoding of insular arthropod biodiversity: toward a Genomic Observatories Network for islands. Molecular Ecology 32(23):6161-6176. doi: 10.1111/mec.16683. Epub. PMID: 36156326.
Our current understanding of ecological and evolutionary processes underlying island biodiversity is heavily shaped by empirical data from plants and birds, although arthropods comprise the overwhelming majority of known animal species. This is due to inherent problems with obtaining high-quality arthropod data. Novel high throughput sequencing approaches are now emerging as powerful tools to overcome such limitations, and thus comprehensively address existing shortfalls in arthropod biodiversity data. Here we explore how, as a community, we might most effectively exploit these tools for comprehensive and comparable inventory and monitoring of insular arthropod biodiversity. We first review the strengths, limitations and potential synergies among existing approaches of high throughput barcode sequencing. We consider how this can be complemented with deep learning approaches applied to image analysis to study arthropod biodiversity. We then explore how these approaches can be implemented within the framework of an island Genomic Observatories Network (iGON) for the advancement of fundamental and applied understanding of island biodiversity. To this end, we identify seven island biology themes at the interface of ecology, evolution and conservation biology, within which collective and harmonised efforts in HTS arthropod inventory could yield significant advances in island biodiversity research.
(92) Triantis Kostas A., Francois Rigal, Robert J. Whittaker, Julian P. Hume, Catherine Sheard, Dimitrios Poursanidis, Jonathan Rolland, Spyros Sfenthourakis, Thomas J. Matthews, Christophe Thébaud, Joseph A. Tobias. Deterministic assembly and anthropogenic extinctions drive convergence of island bird communities. Global Ecology and Biogeography 31 : 1741-1755
Whether entire communities of organisms converge towards predictable structural properties in similar environmental conditions remains controversial. We tested for community convergence in birds by comparing the structure of oceanic archipelago assemblages with their respective regional species pools.
Here we compiled a comprehensive database of morphological trait and phylogenetic data for 6,579 bird species, including species known to have become extinct owing to human activities. We quantified morphological and phylogenetic dissimilarity among species between pairs of archipelagos, using a modified version of the mean nearest taxon distance. We tested for convergence by estimating whether overall mean turnover among archipelagos and pairwise turnover between archipelagos were lower than expected by chance.
For all land birds, we found that turnover in body plan, body mass and phylogeny among archipelagos was significantly lower than expected. Seventeen (of 18) archipelagos showed significant body plan and phylogenetic similarity with at least one other archipelago. Similar convergent patterns of community assembly were detected in different subsamples of the data (extant species, endemics, native non-endemics, and Passeriformes only). Convergence was more pronounced for extant species than for extant and extinct species combined.
Consistent convergence in phylogenetic and morphological structure among archipelagic communities arises through a combination of non-random colonization and in situ adaptation. In addition, by including data from extinct taxa, we show that community convergence both precedes and is accentuated by the anthropogenic extinction of endemic lineages. Our results highlight the potential role of non-random extinction in generating patterns of community convergence and show that convergence existed even before anthropogenic extinctions, owing to deterministic community assembly in similar environmental settings at the global scale.
(91) Milá B., J. Bruxaux, G. Friis, K. Sam, H. Ashari, & C. Thébaud. 2021. A new, undescribed species of Melanocharis berrypecker from western New Guinea and the evolutionary history of the family Melanocharitidae. Ibis 163: 1310-1329
Western New Guinea remains one of the last biologically underexplored regions of the world, and much remains to be learned regarding the diversity and evolutionary history of its fauna and flora. During a recent ornithological expedition to the Kumawa Mountains in West Papua, we encountered an undescribed species of Melanocharis berrypecker (Melanocharitidae) in cloud forest at an elevation of 1200 m asl. Its main characteristics are iridescent blue-black upperparts, satin-white underparts washed lemon yellow, and white outer edges to the external rectrices. Initially thought to represent a close relative of the Mid-mountain Berrypecker Melanocharis longicauda based on elevation and plumage colour traits, a complete phylogenetic analysis of the genus based on full mitogenomes and genome-wide nuclear data revealed that the new species, which we name Satin Berrypecker Melanocharis citreola sp. nov., is in fact sister to the phenotypically dissimilar Streaked Berrypecker M. striativentris. Phylogenetic relationships within the family Melanocharitidae, including all presently recognized genera (Toxorhamphus, Oedistoma, Rhamphocharis and Melanocharis), reveal that this family endemic to the island of New Guinea diversified during the main uplift of New Guinea in the Middle and Late Miocene (14-6 Mya), and represents an evolutionary radiation with high disparity in bill morphology and signalling traits across species. Rhamphocharis berrypeckers fall within the Melanocharis clade despite their larger beaks, and should be included in the latter genus. Interspecific genetic distances in Melanocharis are pronounced (average interspecific distance: 8.8% in COI, 12.4% in ND2), suggesting a long history of independent evolution of all lineages corresponding to currently recognized species, including the Satin Berrypecker, which shares a most recent common ancestor with its sister species in the early Pleistocene (~2.0 Mya).
(90) Arida E, Ashari H, Dahruddin H, Fitriana YS, Hamidy A, Irham M, Kadarusman, Riyanto A, Wiantoro S, Zein MSA, Hadiaty RK, Apandi, Krey F, Kurnianingsih, Melmambessy EHP, Mulyadi, Ohee HL, Saidin, Salamuk A, Sauri S, Suparno, Supriatna N, Suruwaky AM, Laksono WT, Warikar EL, Wikanta H, Yohanita AM, Slembrouck J, Legendre M, Gaucher P, Cochet C, Delrieu-Trottin E, Thébaud C, Mila B, Fouquet A, Borisenko A, Steinke D, Hocdé R, Semiadi G, Pouyaud L, Hubert N. 2021. Exploring the vertebrate fauna of the Bird's Head Peninsula (Indonesia, West Papua) through DNA barcodes. Mol Ecol Resour.ces 21:2369-2387.
Biodiversity knowledge is widely heterogeneous across the Earth's biomes. Some areas, due to their remoteness and difficult access, present large taxonomic knowledge gaps. Mostly located in the tropics, these areas have frequently experienced a fast development of anthropogenic activities during the last decades and are therefore of high conservation concerns. The biodiversity hotspots of Southeast Asia exemplify the stakes faced by tropical countries. While the hotspots of Sundaland (Java, Sumatra, Borneo) and Wallacea (Sulawesi, Moluccas) have long attracted the attention of biologists and conservationists alike, extensive parts of the Sahul area, in particular the island of New Guinea, have been much less explored biologically. Here, we describe the results of a DNA-based inventory of aquatic and terrestrial vertebrate communities, which was the objective of a multidisciplinary expedition to the Bird's Head Peninsula (West Papua, Indonesia) conducted between 17 October and 20 November 2014. This expedition resulted in the assembly of 1005 vertebrate DNA barcodes. Based on the use of multiple species-delimitation methods (GMYC, PTP, RESL, ABGD), 264 molecular operational taxonomic units (MOTUs) were delineated, among which 75 were unidentified and an additional 48 were considered cryptic. This study suggests that the diversity of vertebrates of the Bird's Head is severely underestimated and considerations on the evolutionary origin and taxonomic knowledge of these biotas are discussed.
(89) Aguilée R., F. Pellerin, M. Soubeyrand, J. Choin, & C. Thébaud. 2021. Biogeographic drivers of community assembly on oceanic islands: the importance gf archipelago structure and history. J. Biogeography 48(10), pp.2616-2628.
Aim: Accounting for geo-environmental dynamics is crucial to understand community assembly across islands. Whittaker et al. (J Biogeogr, 35:977–994, 2008)’s General Dynamic Model (GDM) aims towards this goal. Yet, it does not explicitly consider that most islands belong to archipelagos. We examined how island biodiversity dynamics are influenced by the interaction of eco-evolutionary processes acting at the archipelago level with each island's geo-environmental dynamics.
Location: Hypothetical archipelagos.
Taxon: Any.
Methods: We used an individual-based model, ecologically neutral within the archipelago. Several islands emerge in succession with a typical volcanic ontogeny. We considered both mainland and inter-island dispersal. Geographically isolated lineages diverged over time, possibly speciating.
Results: We found diversity to be at dynamic equilibrium. In an archipelago, islands hosted more diversity and more endemic species, at both island and archipelago levels, than an equivalently-sized single isolated island. This was due to an ‘archipelago effect’: inter-island dispersal increased within-island diversity through species occurrence on multiple islands; species may undergo anagenetic changes on the colonised islands, eventually speciating, thereby increasing archipelago diversity. Biodiversity dynamics of different islands may differ even on islands with identical geo-environmental dynamics because the archipelago effect varied over time and affected each island differently (‘history effect’). By accounting for these effects, we predicted detectable deviations from the GDM predictions, which are largest for remote archipelagos, with islands located close together and with an intermediate time of island emergence. In linear stepping-stone archipelagos, we predicted higher diversity on centrally located islands.
Main conclusions: Our results demonstrate that analyses of insular biodiversity data would greatly benefit from explicitly accounting for both archipelago and history effects. We suggest incorporating variables characterising the spatio-temporalstructure of the whole archipelago. We discuss possible difficulties in distinguishing between the archipelago effect and equilibrium diversity dynamics.
(88) Leroy T., M. Rousselle, M.-K. Tilak, A.E. Caizergues, C. Scornavacca, M. Recuerda, J. Fuchs, J.C. Illera, D.H. de Swardt, G. Blanco, C. Thébaud, B. Milá, & B. Nabholz. 2021. Island songbirds as windows into evolution in small populations. Current Biology 31(6), pp.1303-1310.
Due to their limited ranges and inherent isolation, island species have long been recognized as crucial systems for tackling a range of evolutionary questions, including in the early study of speciation.1,2 Such species have been less studied in the understanding of the evolutionary forces driving DNA sequence evolution. Island species usually have lower census population sizes (N) than continental species and, supposedly, lower effective population sizes (Ne). Given that both the rates of change caused by genetic drift and by selection are dependent upon Ne, island species are theoretically expected to exhibit (1) lower genetic diversity, (2) less effective natural selection against slightly deleterious mutations,3,4 and (3) a lower rate of adaptive evolution.5, 6, 7, 8 Here, we have used a large set of newly sequenced and published whole-genome sequences of Passerida species (14 insular and 11 continental) to test these predictions. We confirm that island species exhibit lower census size and Ne, supporting the hypothesis that the smaller area available on islands constrains the upper bound of Ne. In the insular species, we find lower nucleotide diversity in coding regions, higher ratios of non-synonymous to synonymous polymorphisms, and lower adaptive substitution rates. Our results provide robust evidence that the lower Ne experienced by island species has affected both the ability of natural selection to efficiently remove weakly deleterious mutations and also the adaptive potential of island species, therefore providing considerable empirical support for the nearly neutral theory. We discuss the implications for both evolutionary and conservation biology.
(87) Valente, L., Phillimore, A. B., Melo, M., Warren, B. H., Clegg, S. M., Havenstein, K., Tiedemann, R., Illera, J. C., Thébaud, C., Aschenbach, T. & Etienne, R. S. 2020. A simple dynamic model explains island bird diversity worldwide. Nature, 579: 92–96.
Colonization, speciation and extinction are dynamic processes that influence global patterns of species richness. Island biogeography theory predicts that the contribution of these processes to the accumulation of species diversity depends on the area and isolation of the island. Notably, there has been no robust global test of this prediction for islands where speciation cannot be ignored9, because neither the appropriate data nor the analytical tools have been available. In this paper, we addressed both deficiencies to reveal, for island birds, the empirical shape of the general relationships that determine how colonization, extinction and speciation rates co-vary with the area and isolation of islands. We compiled a global molecular phylogenetic dataset of birds on islands, based on the terrestrial avifaunas of 41 oceanic archipelagos worldwide (including 596 avian taxa), and applied a new analysis method to estimate the sensitivity of island-specific rates of colonization, speciation and extinction to island features (area and isolation). Our model predicts—with high explanatory power—several global relationships. We found a decline in colonization with isolation, a decline in extinction with area and an increase in speciation with area and isolation. Combining the theoretical foundations of island biogeography with the temporal information contained in molecular phylogenies proves a powerful approach to reveal the fundamental relationships that govern variation in biodiversity across the planet.
(86) Gabrielli M., T. Leroy, B. Nabholz, B. Milá, & C. Thébaud. 2020. Within-island diversification in a passerine bird. Proceeding of the Royal Society B 287: 20192999. http://dx.doi.org/10.1098/rspb.2019.2999
The presence of congeneric taxa on the same island suggests the possibility of in situ divergence, but can also result from multiple colonizations of pre- viously diverged lineages. Here, using genome-wide data from a large population sample, we test the hypothesis that intra-island divergence explains the occurrence of four geographical forms meeting at hybrid zones in the Reunion grey white-eye (Zosterops borbonicus), a species complex endemic to the small volcanic island of Reunion. Using population genomic and phylogenetic analyses, we reconstructed the population history of the different forms. We confirmed the monophyly of the complex and found that one of the lowland forms is paraphyletic and basal relative to others, a pattern highly consistent with in situ divergence. Our results suggest initial colonization of the island through the lowlands, followed by expansion into the highlands, which led to the evolution of a distinct geographical form, genetically and ecologically different from the lowland ones. Lowland forms seem to have experienced periods of geographical isolation, but they diverged from one another by sexual selection rather than niche change. Overall, low dispersal capabilities in this island bird combined with both geographical and ecological opportunities seem to explain how divergence occurred at such a small spatial scale.
(85) Bourgeois Y.X.C., J.A.M Bertrand, B. Delahaie, H. Holota, C. Thébaud, and B. Milá. 2020. Differential divergence in autosomes and sex chromosomes is associated with intra-island diversification at a very small spatial scale in a songbird lineage. Molecular Ecology 29(6), pp.1137-1153.
Recently diverged taxa showing marked phenotypic and ecological diversity provide optimal systems to understand the genetic processes underlying speciation. We used genome-wide markers to investigate the diversification of the Reunion grey white-eye (Zosterops borbonicus) on the small volcanic island of Reunion (Mascarene archipelago), where this species complex exhibits four geographical forms that are parapatrically distributed across the island and differ strikingly in plumage colour. One form restricted to the highlands is separated by a steep ecological gradient from three distinct lowland forms which meet at narrow hybrid zones that are not associ- ated with environmental variables. Analyses of genomic variation based on single nucleotide polymorphism data from genotyping-by-sequencing and pooled RAD-seq approaches show that signatures of selection associated with elevation can be found at multiple regions across the genome, whereas most loci associated with the low- land forms are located on the Z sex chromosome. We identified TYRP1, a Z-linked colour gene, as a likely candidate locus underlying colour variation among lowland forms. Tests of demographic models revealed that highland and lowland forms di- verged in the presence of gene flow, and divergence has progressed as gene flow was restricted by selection at loci across the genome. This system holds promise for in- vestigating how adaptation and reproductive isolation shape the genomic landscape of divergence at multiple stages of the speciation process.
(84) Vacher J.P., J. Chave, F. Ficetola, G. Sommeria-Klein, S. Tao, C. Thébaud, M. Blanc, A. Camacho, J. Cassimiro, T.J. Colston, M. Dewynter, R. Ernst, P. Gaucher, J.O. Gomes, R. Jairam, P.J.R. Kok, J.D. Lima, Q. Martinez, C. Marty, B.P. Noonan, P. Nunes, P. Ouboter, R. Recoder, M.T. Rodrigues, A. Snyder, S. Maques de Souza, & A. Fouquet. 2020. Large-scale DNA-based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography 47(8), 1781-1791.
Mapping Amazonian biodiversity accurately is a major challenge for integrated conservation strategies and to study its origins. However, species boundaries and their respective distribution are notoriously inaccurate in this region. In this paper, we generated a georeferenced database of short mtDNA sequences from Amazonian frogs, revised the species richness and the delineation of bioregions of the Eastern Guiana Shield and estimated endemism within these bioregions.
We used an extensive DNA-based sampling of anuran amphibians of Amazonia using next-generation sequencing to delineate Operational Taxonomic Units (OTU) and their distribution. We analysed this database to infer bioregions using Latent Dirichlet Allocation modelling. We then compared endemism within these bioregions based on our results and the current IUCN database, and inferred environmental variables that contributed the most to the biogeographic pattern.
The recognized anuran species richness within the focal area increased from 440 species currently listed by the IUCN Red List to as much as 876 OTUs with our dataset. We recovered eight bioregions, among which three lie within the Eastern Guiana Shield. We estimated that up to 82% of the OTUs found in this area are en- demic, a figure three times higher than the previous estimate (28%). Environmental features related to seasonal precipitations are identified as playing an important role in shaping Amazonian amphibian bioregions.
(83) Warren B.H., R.E. Ricklefs, C. Thébaud, D. Gravel, & N. Mouquet. 2019. How consideration of islands has inspired mainstream ecology: links between the theory of island biogeography and some other key theories. Reference Module in Earth Systems and Environmental Sciences, Elsevier, 10.1016/B978-0-12-409548-9.11788-9 .
The passing of the 50th anniversary of the theory of island biogeography (IBT) has helped spur a new wave of interest in the biology of islands. Despite the longstanding acclaim of MacArthur and Wilson’s (1963, 1967) theory, the breadth of its influence in mainstream ecology today is easily overlooked. Here we summarize some of the main links between IBT and subsequent developments in ecology. These include not only modifications to the core model to incorporate greater biological complexity, but also the role of IBT in inspiring two other quantitative theories that are at least as broad in relevance—metapopulation theory and ecological neutral theory. Using habitat fragmentation and life-history evolution as examples, we also argue that a significant legacy of IBT has been in shaping and unifying ecological schools of thought.
(82) Leroy T., Y. Anselmetti, M.-K. Tilak, S. Berard, L. Csukonyi, M. Gabrielli, C. Scornavacca, B. Mila, C. Thébaud, & B. Nabholz. 2019. A bird’s white-eye view on neo-sex chromosome evolution. Peer Community Journal 1, article no. e63.
Chromosomal organization is relatively stable among avian species, especially with regards to sex chromosomes. Members of the large Sylvioidea clade however have a pair of neo-sex chromosomes which is unique to this clade and originate from a parallel translocation of a region of the ancestral 4A chromosome on both W and Z chromosomes. Here, we took advantage of this unusual event to study the early stages of sex chromosome evolution. To do so, we sequenced a female (ZW) of two Sylvioidea species, a Zosterops borbonicus and a Z. pallidus. Then, we organized the Z. borbonicus scaffolds along chromosomes and annotated genes. Molecular phylogenetic dating under various methods and calibration sets confidently confirmed the recent diversification of the genus Zosterops (1-3.5 million years ago), thus representing one of the most exceptional rates of diversification among vertebrates. We then combined genomic coverage comparisons of five males and seven females, and homology with the zebra finch genome (Taeniopygia guttata) to identify sex chromosome scaffolds, as well as the candidate chromosome breakpoints for the two translocation events. We observed reduced levels of within-species diversity in both translocated regions and, as expected, even more so on the neoW chromosome. In order to compare the rates of molecular evolution in genomic regions of the autosomal-to-sex transitions, we then estimated the ratios of non-synonymous to synonymous polymorphisms (πN/πS) and substitutions (dN/dS). Based on both ratios, no or little contrast between autosomal and Z genes was observed, thus representing a very different outcome than the higher ratios observed at the neoW genes. In addition, we report significant changes in base composition content for translocated regions on the W and Z chromosomes and a large accumulation of transposable elements (TE) on the newly W region. Our results revealed contrasted signals of molecular evolution changes associated to these autosome-to- sex chromosome transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak suport for a fast-Z effect.
(81) Dale E.J., R. L. Kitching, C. Thébaud, S. C. Maunsell, L. A. Ashton. Moths in the Pyrénées: spatio-temporal patterns and indicators of elevational assemblages. Biodiversity and Conservation 28, 1593-1610
Understanding how assemblages of invertebrates change over continuous elevational gradients not only generates an understanding of current rules of community assembly but may also be useful for predicting the future distributions of species under global change. Temperature decreases predictably with increasing elevation and, accordingly, gradients in elevation permit the study of adjacent climates within small geographical areas. The present study examines if and how assemblages of moths change with increasing elevation in the eastern French Pyrenees. Elevation had a strong effect on the assemblage composition of moth species in both seasons. The species sets which contributed most to this strong pattern differed completely across seasons. Analysis of restrictions and fidelity to particular elevational ranges generated a set of indicator species which can be used to monitor future changes in distribution. Twelve species were identified as elevation-specific indicators (the 'predictor set’) from the spring samples and summer samples. We note the strong contrasts between species that produce overall statistical pattern and those that show strong fidelity to particular elevations and discuss this in terms of the biologies of the species concerned.
We discuss best practice for the identification and use of indicator species for monitoring future responses to climate change.
(80) Borges P.A.V., P. Cardoso, S. Fattorini, F. Rigal, T.J. Matthews, L. Di Biase, I.R. Amorim, M. Florencio, L. Borda- de-Água, C. Rego, F. Pereira, R. Nunes, R. Carvalho, M.T. Ferreira, H. López, A.J. Pérez Delgado, R. Otto, S. Fernández Lugo, L. de Nascimento, J. Caujapé-Castells, J. Casquet, S. Danflous, J. Fournel, A.-M. Sadeyen, R.B. Elias, J.M. Fernández-Palacios, P. Oromí, C. Thébaud, D. Strasberg, B.C. Emerson. 2018. Community structure of woody plants on islands along a bioclimatic gradient. Frontiers of Biogeography 10(3-4).10.21425/F5FBG40295
Understanding patterns of community structure and the causes for their variation can be furthered by comparative biogeographic analyses of island biotas. In this study, we used woody plant data at the local scale to investigate variations in species rarity, alpha, beta, and gamma diversity within and between three islands from the oceanic archipelagoes of Azores, Canaries and Mascarene. We used standardized protocols to sample ten 50 m × 50 m forest plots in each of the three islands with contrasting climate and regional species pools: Terceira (Azores), Tenerife (Canaries), and Reunion (Mascarene Islands). Occupancy frequency distributions and species abundance distributions were used to investigate rarity. The partitioning of beta diversity in a distance-decay framework was used to test for spatial patterns of community composition. Rarity was much more pronounced in the highly diverse islands of Tenerife and Reunion than in the regionally poorer island of Terceira. The number of species rose faster with increasing sample area in both Tenerife and Reunion. The slope of the species rank abundance curve was steeper in Terceira whereas the richer island assemblages approached a lognormal model. Compositional changes according to spatial distance were mostly due to replacement of species in Terceira and Reunion. Our results point to important differences in the community structure of Terceira, which is the less diverse and temperate region in comparison to Tenerife and Reunion which are highly diverse. High regional diversity of species in Tenerife and Reunion is a consequence of comparably long eco-evolutionary history that has promoted high levels of diversity which are not comparable to the relatively species-poor biota of the Azores, constrained by recent geological history and low environmental diversity.
(79) Warren Ben H., Oskar Hagen, Florian Gerber, Christophe Thébaud, Emmanuel Paradis, Elena Conti. 2018. Evaluating alternative explanations for an association of extinction risk and evolutionary uniqueness in multiple insular lineages. Evolution 72(10), 2005-2024.
Studies in insular environments have often documented a positive association of extinction risk and evolutionary uniqueness (i.e. how distant a species is from its closest living relative). However, the cause of this association is unclear. One explanation is that species threatened with extinction are evolutionarily unique because they are old, implying that extinction risk increases with time since speciation (age-dependent extinction). An alternative explanation is that such threatened species are last survivors of clades that have undergone an elevated extinction rate, and that their uniqueness results from the extinction of their close relatives. Distinguishing between these explanations is difficult but important, since they imply different biological processes determining extinction patterns. Here we designed a simulation approach to distinguish between these alternatives using living species, and applied it to twelve insular radiations that show a positive association between extinction risk and evolutionary uniqueness. We also tested the sensitivity of results to underlying assumptions and variable extinction rates. Despite differences among the radiations considered, age-dependent extinction was supported as best explaining the majority of the empirical cases. Biological processes driving characteristic changes in abundance with species duration (age-dependency) may merit further investigation.
(78) Kitson James J.N., Ben H. Warren, Christophe Thébaud, Dominique Strasberg, and Brent C. Emerson. Community assembly and diversification in a species-rich radiation of island weevils (Coleoptera: Cratopini). 2018. Journal of Biogeography 45, 2016-2026
Aim: To test a prediction derived from island biogeographical theory that in situ speciation should make an increasingly important contribution to community assembly as islands age. This prediction is tested on estimated biogeographical histories from Mauritius (approximately 9 Myr) and Reunion (approximately 5 Myr). We additionally investigate the evolutionary dynamics of insect flight loss, as the loss of flight in island lineages can influence patterns of diversification.
Location: Mascarene Islands; Southwest Indian Ocean.
Taxon: Weevils.
Methods: Up to five individuals of each taxonomically described species sampled within each sampling site were sequenced for the mitochondrial gene Cytochrome Oxidase II to delimit operational taxonomic units (OTUs). OTUs were further sequenced for the nuclear genes Arginine Kinase, Histone 3 and ribosomal 28s, to reconstruct the phylogenetic history of the group. Timings of colonization and in situ speciation events were estimated with BEAST2.
Results: Our results support the hypothesis that present-day species richness on the older island of Mauritius is largely the result of in situ speciation, with few colonization events, of which all but the most basal are recent. In contrast, Reunion presents a more uniform temporal spectrum of colonization times. Flight loss has evolved convergently at least five times, and speciation events associated with flight loss are significantly younger than speciation events that have not resulted in flight loss.
Main conclusions: Patterns of community assembly on the islands of Mauritius and Reunion fit a model where the addition of new species and species turnover is increasingly dominated by in situ speciation as an island community matures. Repeated flight loss indicates selection for flightlessness, with the young age of flightless lineages suggesting higher extinction rates over longer evolutionary timescales and little influence on present-day species richness.
(77) Borges Paulo A. V. , Pedro Cardoso, Holger Kreft, Robert J. Whittaker, Simone Fattorini, Brent C. Emerson, Artur Gil, Rosemary G. Gillespie, Thomas J. Matthews, Ana M. C. Santos, Manuel J. Steinbauer12 · Christophe Thébaud, Claudine Ah‐Peng, Isabel R. Amorim1,2 · Silvia Calvo Aranda, Ana Moura Arroz, José Manuel N. Azevedo, Mário Boieiro, Luís Borda‐de‐Água, José Carlos Carvalho, Rui B. Elias, José María Fernández‐Palacios, Margarita Florencio, Juana M. González‐Mancebo, Lawrence R. Heaney, Joaquín Hortal, Christoph Kueffer, Benoit Lequette, José Luis Martín‐Esquivel, Heriberto López, Lucas Lamelas‐López, José Marcelino, Rui Nunes, Pedro Oromí, Jairo Patiño, Antonio J. Pérez, Carla Rego, Sérvio P. Ribeiro, François Rigal, Pedro Rodrigues, Andrew J. Rominger, Margarida Santos‐Reis, Hanno Schaefer, Cecília Sérgio, Artur R. M. Serrano, Manuela Sim‐Sim, P. J. Stephenson, António O. Soares, Dominique Strasberg, Alain Vanderporten, Virgílio Vieira, Rosalina Gabriel. 2018. Global Island Monitoring Scheme (GIMS): a proposal for the long‐term coordinated survey and monitoring of native island forest biota. Biodiversity and Conservation 27, 2567–2586.
Islands harbour evolutionary and ecologically unique biota, which are currently disproportionately threatened by a multitude of anthropogenic factors, including habitat loss, invasive species and climate change. Native forests on oceanic islands are important refu-gia for endemic species, many of which are rare and highly threatened. Long-term monitor- ing schemes for those biota and ecosystems are urgently needed: (i) to provide quantitative baselines for detecting changes within island ecosystems, (ii) to evaluate the effectiveness of conservation and management actions, and (iii) to identify general ecological patterns andprocesses using multiple island systems as repeated ‘natural experiments’. In this contribu- tion, we call for a Global Island Monitoring Scheme (GIMS) for monitoring the remaining native island forests, using bryophytes, vascular plants, selected groups of arthropods and vertebrates as model taxa. As a basis for the GIMS, we also present new, optimized monitor- ing protocols for bryophytes and arthropods that were developed based on former standard- ized inventory protocols. Effective inventorying and monitoring of native island forests will require: (i) permanent plots covering diverse ecological gradients (e.g. elevation, age of ter- rain, anthropogenic disturbance); (ii) a multiple-taxa approach that is based on standardized and replicable protocols; (iii) a common set of indicator taxa and community properties that are indicative of native island forests’ welfare, building on, and harmonized with existing sampling and monitoring efforts; (iv) capacity building and training of local researchers, col- laboration and continuous dialogue with local stakeholders; and (v) long-term commitment by funding agencies to maintain a global network of native island forest monitoring plots.
(76) Bruxaux J, Gabrielli M, Ashari H, Prŷs-Jones R, Joseph L, Milá B, Besnard G, Thébaud C. Recovering the evolutionary history of crowned pigeons (Columbidae: Goura): Implications for the biogeography and conservation of New Guinean lowland birds. Molecular Phylogenetics and Evolution 120:248-258. doi: 10.1016/j.ympev.2017.11.022.
Assessing the relative contributions of immigration and diversification into the buildup of species diversity is key to understanding the role of historical processes in driving biogeographical and diversification patterns in species-rich regions. Here, we investigated how colonization, in situ speciation, and extinction history may have generated the present-day distribution and diversity of Goura crowned pigeons (Columbidae), a group of large forest-dwelling pigeons comprising four recognized species that are all endemic to New Guinea. We used a comprehensive geographical and taxonomic sampling based mostly on historical museum samples, and shallow shotgun sequencing, to generate complete mitogenomes, nuclear ribosomal clusters and independent nuclear conserved DNA elements. We used these datasets independently to reconstruct molecular phylogenies. Divergence time estimates were obtained using mitochondrial data only. All analyses revealed similar genetic divisions within the genus Goura and recovered as monophyletic groups the four species currently recognized, providing support for recent taxonomic changes based on differences in plumage characters. These four species are grouped into two pairs of strongly supported sister species, which were previously not recognized as close relatives: Goura sclaterii with Goura cristata, and Goura victoria with Goura scheepmakeri. While the geographical origin of the Goura lineage remains elusive, the crown age of 5.73 Ma is consistent with present-day species diversity being the result of a recent diversification within New Guinea. Although the orogeny of New Guinea's central cordillera must have played a role in driving diversification in Goura, cross-barrier dispersal seems more likely than vicariance to explain the speciation events having led to the four current species. Our results also have important conservation implications. Future assessments of the conservation status of Goura species should consider threat levels following the taxonomic revision proposed by del Hoyo and Collar (HBW and BirdLife International illustrated checklist of the birds of the world 1: non-passerines, 2014), which we show to be fully supported by genomic data. In particular, distinguishing G. sclaterii from G. scheepmakeri seems to be particularly relevant.
(75) Delahaie Boris, Josselin Cornuault, Charline Masson, Joris Bertrand, Yann Bourgeois, Borja Milá and Christophe Thébaud. Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex. Journal of evolutionary Biology 30:2132-2145
Patterns of phenotypic and genic frequencies across hybrid zones provide insight into the origin and evolution of reproductive isolation. The Reunion grey white-eye, Zosterops borbonicus, exhibits parapatrically distributed plumage colour forms across the lowlands of the small volcanic island of Reunion (Mascarene archipelago). These forms meet and hybridize in regions that are natural barriers to dispersal (rivers, lava fields). Here, we investigated the relationship among patterns of differentiation at neutral genetic (microsatellite) markers, phenotypic traits (morphology and plumage colour) and niche characteristics across three independent hybrid zones. Patterns of phenotypic divergence revealed that these hybrid zones are among the narrowest ever documented in birds. However, the levels of phenotypic divergence stand in stark contrast to the lack of clear population neutral genetic structure between forms. The position of the hybrid zones coincides with different natural physical barriers, yet is not associated with steep changes in vegetation and related climatic variables, and major habitat transitions are shifted from these locations by at least 18 km. This suggests that the hybrid zones are stabilized over natural dispersal barriers, independently of environmental boundaries, and are not associated with niche divergence. A striking feature of these hybrid zones is the very low levels of genetic differentiation in neutral markers between forms, suggesting that phenotypic divergence has a narrow genetic basis and may reflect recent divergence at a few linked genes under strong selection, with a possible role for assortative mating in keeping these forms apart.
(74) Ducatez Simon, Mathieu Giraudeau, Christophe Thébaud and Lisa Jacquin. Colour polymorphism is associated with lower extinction risk in birds. Global Change Biology 23, 3030-3039
Colour polymorphisms have played a major role in enhancing current understanding of how selection and demography can impact phenotypes. Because different morphs often display alternative strategies and exploit alternative ecological niches, colour polymorphism can be expected to promote adaptability to environmental changes. However, whether and how it could influence populations' and species' response to global changes remains debated. To address this question, we built an up-to-date and complete database on avian colour polymorphism based on the examination of available data from all 10,394 extant bird species. We distinguished between true polymorphism (where different genetically determined morphs co-occur in sympatry within the same population) and geographic variation (parapatric or allopatric colour variation), because these two patterns of variation are expected to have different consequences on populations' persistence. Using the IUCN red list, we then showed that polymorphic bird species are at lesser risk of extinction than nonpolymorphic ones, after controlling for a range of factors such as geographic range size, habitat breadth, life history, and phylogeny. This appears consistent with the idea that high genetic diversity and/or the existence of alternative strategies in polymorphic species promotes the ability to adaptively respond to changing environmental conditions. In contrast, polymorphic species were not less vulnerable than nonpolymorphic ones to specific drivers of extinction such as habitat alteration, direct exploitation, climate change, and invasive species. Thus, our results suggest that colour polymorphism acts as a buffer against environmental changes, although further studies are now needed to understand the underlying mechanisms. Developing accurate quantitative indices of sensitivity to specific threats is likely a key step towards a better understanding of species response to environmental changes.
(73) Vacher Jean-Pierre, Philippe Kok, Miguel Rodrigues, Jucivaldo Lima, Andy Lorenzini, Quentin Martinez, Manon Fallet, Elodie Courtois, Michel Blanc, Philippe Gaucher, Mael Dewynter, Rawien Jairam, Paul Ouboter, Christophe Thebaud, Antoine Fouquet. Cryptic diversity in Amazonian frogs: integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Aromobatidae) reveals a unique case of diversification within the Guiana Shield. Molecular Phylogenetics and Evolution 112, 158-173
Lack of resolution on species boundaries and distribution can hamper inferences in many fields of biology, notably biogeography and conservation biology. This is particularly true in megadiverse and under-surveyed regions such as Amazonia, where species richness remains vastly underestimated. Integrative approaches using a combination of phenotypic and molecular evidence have proved extremely successful in reducing knowledge gaps in species boundaries, especially in animal groups displaying high levels of cryptic diversity like amphibians. Here we combine molecular data (mitochondrial 16S rRNA and nuclear TYR, POMC, and RAG1) from 522 specimens of Anomaloglossus, a frog genus endemic to the Guiana Shield, including 16 of the 26 nominal species, with morphometrics, bioacoustics, tadpole development mode, and habitat use to evaluate species delineation in two lowlands species groups. Molecular data reveal the existence of 18 major mtDNA lineages among which only six correspond to described species. Combined with other lines of evidence, we confirm the existence of at least 12 Anomaloglossus species in the Guiana Shield lowlands. Anomaloglossus appears to be the only amphibian genus to have largely diversified within the eastern part of the Guiana Shield. Our results also reveal strikingly different phenotypic evolution among lineages. Within the A. degranvillei group, one subclade displays acoustic and morphological conservatism, while the second subclade displays less molecular divergence but clear phenotypic divergence. In the A. stepheni species group, a complex evolutionary diversification in tadpole development is observed, notably with two closely related lineages each displaying exotrophic and endotrophic tadpoles.
(72) Bourgeois Yann X. C., Boris Delahaie, Mathieu Gautier, Emeline Lhuillier, Pierre-Jean G. Malé, Joris A. M. Bertrand, Josselin Cornuault, Kazumasa Wakamatsu, Olivier Bouchez, Claire Mould, Jade Bruxaux, Hélène Holota, Borja Milá and
Christophe Thébaud. A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird. Royal Society Open Science 4:160805
Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a ‘brown’ ancestral population, the dominant ‘grey’ allele spread quickly once it arose froma new mutation. Since colour morphs are always found inmixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.
(71) Cicconardi Francesco, Paulo A. V. Borges, Dominique Strasberg, Pedro Oromí, Heriberto López, Antonio J. Pérez-Delgado, Juliane Casquet, Juli Caujapé-Castells, José María Fernández-Palacios, Christophe Thébaud, Brent C. Emerson. MtDNA metagenomics reveals large-scale invasion of belowground arthropod communities by introduced species. Molecular Ecology 26, 3104-3115
Using a series of standardised sampling plots within forest ecosystems in remote oceanic islands, we reveal fundamental differences between the structuring of aboveground and belowground arthropod biodiversity that are likely due to large-scale species introductions by humans. Species of beetle and spider were sampled almost exclusively from single islands, while soil dwelling Collembola exhibited more than tenfold higher species sharing among islands. Comparison of Collembola mitochondrial metagenomic data to a database of more than 80,000 Collembola barcode sequences revealed almost 30% of sampled island species are genetically identical, or near identical, to individuals sampled from often very distant geographic regions of the world. Patterns of mtDNA relatedness among Collembola implicate human-mediated species introductions, with minimum estimates for the proportion of introduced species on the sampled islands ranging from 45-88%. Our results call for more attention to soil mesofauna to understand the global extent and ecological consequences of species introductions.
(70) Emerson B.C., J. Casquet, H. Lopez, P. Cardoso, P.A.V. Borges, N. Mollaret, P. Oromi, D. Strasberg, & C. Thébaud. A combined field survey and molecular identification protocol for comparing forest arthropod biodiversity across spatial scales. Molecular Ecology Resources 17, 694-707
Obtaining fundamental biodiversity metrics such as alpha, beta and gamma diversity for arthropods is often complicated by a lack of prior taxonomic information and/or taxonomic expertise, which can result in unreliable morphologically based estimates. We provide a set of standardized ecological and molecular sampling protocols that can be employed by researchers whose taxonomic skills may be limited, and where there may be a lack of robust a priori information regarding the regional pool of species. These protocols combine mass sampling of arthropods, classification of samples into parataxonomic units (PUs) and selective sampling of individuals for mtDNA sequencing to infer biological species. We sampled ten lowland rainforest plots located on the volcanic oceanic island of Réunion (Mascarene archipelago) for spiders, a group with limited taxonomic and distributional data for this region. We classified adults and juveniles into PUs and then demonstrated the reconciliation of these units with presumed biological species using mtDNA sequence data, ecological data and distributional data. Because our species assignment protocol is not reliant upon prior taxonomic information, or taxonomic expertise, it minimizes the problem of the Linnean shortfall to yield diversity estimates that can be directly compared across independent studies. Field sampling can be extended to other arthropod groups and habitats by adapting our field sampling protocol accordingly.
(69) Hansen D.M, J.J. Austin, R.H. Baxter, E.J. de Boer, W. Falcón, S.J. Norder, K.F. Rijsdijk, C. Thébaud, N.J. Bunbury, & B.H. Warren. Origins of endemic island tortoises in the western Indian Ocean: A critique of the human-translocation hypothesis. Journal of Biogeography 44, 1430-1435
This paper is a reply to a paper that recently argued that giant tortoises could have been introduced to the Indian Ocean islands by early Austronesian sailors, possibly to establish provisioning stations for their journeys, just as European sailors did in more recent historical times. We present evidence from DNA phylogeny, Plio-Pleistocene ocean currents, giant tortoise dispersal, evolution of plant defences, radiocarbon dates and archaeology that indicates that the endemic giant tortoises on the Mascarenes and Seychelles colonized naturally and were not translocated there by humans.
(68) Fuchs J., D. Lemoine, J. L. Parra, J.-M. Pons, M. J. Raherilalao, R. Prys-Jones, C. Thébaud, B. H. Warren, and S. M. Goodman. Long-distance dispersal and inter-island colonization across the western Malagasy Region explain diversification in brush-warblers (Passeriformes: Nesillas). Biological Journal of the Linnean Society 119, 873-889
This study examines the colonization history and phylogeography of the brush-warblers (genus Nesillas), a genus of passerines endemic to islands of the western Indian Ocean (Madagascar, Comoros and Aldabra). The phylogeny of all recognized Nesillas taxa was reconstructed employing Bayesian phylogenetic methods and divergence times were estimated using a range of substitution rates and clock assumptions. Spatiotemporal patterns of population expansion were inferred using Spread, and niches of different lineages were compared using ecological niche modelling. Our results indicate that taxa endemic to the Comoros are paraphyletic and that the two endemic species on Madagascar (N. typica and N. lantzii) are not sister taxa. The brush-warblers started to diversify about 1.6 Myr, commencing with the separation of the clade formed by two species endemic to the Comoros (N. brevicaudata and N. mariae) from the rest of the genus. The lineages leading to the two Malagasy species diverged about 0.9 Myr; each with significantly different modern ecological niches and the subject of separate demographic processes. Patterns of diversification and endemism in Nesillas were shaped by multiple long distance dispersal events and inter-island colonization, a recurring pattern for different lineages on western Indian Ocean islands. The diversification dynamics observed for Nesillas are also consistent with the taxon cycle hypothesis.
(67) Bertrand J., B. Delahaie, Y. Bourgeois, T. Duval, R. Garcia-Jimenez, J. Cornuault, B. Pujol, C. Thébaud, B. Mila. The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird. Journal of evolutionary Biology 29, 824-836
Adaptation to local environmental conditions and the range dynamics of populations can influence evolutionary divergence along environmental gradients. Thus, it is important to investigate patterns of both phenotypic and genetic variations among populations to reveal the respective roles of these two types of factors in driving population differentiation. Here, we test for evidence of phenotypic and genetic structure across populations of a passerine bird (Zosterops borbonicus) distributed along a steep elevational gradient on the island of Reunion. Using 11 microsatellite loci screened in 401 individuals from 18 localities distributed along the gradient, we found that genetic differentiation occurred at two spatial levels: (i) between two main population groups corresponding to highland and lowland areas, respectively, and (ii) within each of these two groups. In contrast, several morphological traits varied gradually along the gradient. Comparison of neutral genetic differentiation (FST) and phenotypic differentiation (PST) showed that PST largely exceeds FST at several morphological traits, which is consistent with a role for local adaptation in driving morphological divergence along the gradient. Overall, our results revealed an area of secondary contact midway up the gradient between two major, cryptic, population groups likely diverged in allopatry. Remarkably, local adaptation has shaped phenotypic differentiation irrespective of population history, resulting in different patterns of variation along the elevational gradient. Our findings underscore the importance of understanding both historical and selective factors when
trying to explain variation along environmental gradients.
(66) Bourgeois Y., J. Bertrand, B. Delahaie, J. Cornuault, T. Duval, B. Mila, & C. Thébaud. Candidate gene analysis suggests untapped genetic complexity in melanin-based pigmentation in birds. Journal of Heredity 107, 327-335
Studies on melanin-based color variation in a context of natural selection have provided a wealth of information on the link between phenotypic and genetic variation. Here, we evaluated associations between melanic plumage patterns and genetic polymorphism in the Réunion grey white-eye (Zosterops borbonicus), a species in which mutations on MC1R do not seem to play any role in explaining melanic variation. This species exhibits five plumage color variants that can be grouped into three color forms which occupy discrete geographic regions in the lowlands of Réunion, and a fourth high-elevation form which comprises two color morphs (grey and brown) and represents a true color polymorphism. We conducted a comprehensive survey of sequence variation in 96 individuals at a series of seven candidate genes other than MC1R that have been previously shown to influence melanin-based color patterns in vertebrates, including genes that have rarely been studied in a wild bird species before: POMC, Agouti, TYR, TYRP1, DCT, Corin and SLC24A5. Of these seven genes, two (Corin and TYRP1) displayed an interesting shift in allele frequencies between lowland and highland forms and a departure from mutation-drift equilibrium consistent with balancing selection in the polymorphic highland form only. Sequence variation at Agouti, a gene frequently involved in melanin-based pigmentation patterning, was not associated with color forms or morphs. Thus, we suggest that functionally important changes in loci other than those classically studied are involved in the color polymorphism exhibited by the Réunion grey white-eye and possibly many other non-model species.
(65) Jaworski C., C. Thébaud, and J. Chave. Dynamics and persistence in a metacommunity centred on the plant Antirrhinum majus: theoretical predictions and an empirical test. Journal of Ecology 104, 456-468
Spatial processes have a major influence on the stability of species interaction networks and their resilience to environmental fluctuations. Here we combine field observations and a dynamic model to understand how spatial processes may affect a network composed of the flowering plant Antirrhinum majus, its cohort of pollinators, and a specialist seed-predator and its parasitoid.
The interactions taking place within this system were investigated by determining the fate of flowers and fruits on flowering and fruiting stems at sixteen study sites. We then used this information to estimate spatial and temporal variation in the pollination rate, parasitism rate, and hyperparasitism rate.
We found that the plants were pollinator-limited, with relatively variable fruit-to-flower ratios across sites. On almost all sites, plants were both parasitised and hyperparasitised, at a low to moderate rate.
Comparing our field observations with a tritrophic Nicholson-Bailey model, we found that empirical data are not always consistent with the conditions for local tritrophic persistence. This suggests that other mechanisms such as random disturbances and recolonisations (patch dynamics) or inter-site migration through metacommunity dynamics (source-sink dynamics) play a role in this system. Model simulations showed that dispersal could contribute to increasing tritrophic persistence in this system, and that source-sink structure, not just environmental stochasticity, may cause the observed pattern of spatial variation.
(64) Mills J., C. Teplitsky, and 59 other authors. Archiving primary data: solutions for long-term-studies. Trends in Ecology and Evolution 30, 581-589
The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehen- sion amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
(63) Vacher J.P., A. Fouquet, H. Holota & C. Thébaud. The complete mitochondrial genome of Anomaloglossus baeobatrachus (Amphibia: Anura: Aromobatidae). Mitochondrial DNA Part B, 1:1, 338-340
(62) Jaworski CC, Andalo C, Raynaud C, Simon V, Thébaud C, Chave J. 2015. The Influence of prior learning experience on pollinator choice: an experiment using bumblebees on two wild floral types of Antirrhinum majus. PLoS ONE 10(8):e0130225. doi:10.1371/journal.pone.0130225.
Understanding how pollinator behavior may influence pollen transmission across floral types is a major challenge, as pollinator decision depends on a complex range of environmental cues and prior experience. Here we report an experiment using the plant Antirrhinum majus and the bumblebee Bombus terrestris to investigate how prior learning experience may affect pollinator preferences between floral types when these are presented together. We trained naive bumblebees to forage freely on flowering individuals of either A. majus pseudomajus (magenta flowers) or A. majus striatum (yellow flowers) in a flight cage. We then used a Y-maze device to expose trained bumblebees to a dual choice between the floral types. We tested the influence of training on their choice, depending on the type of plant signals available (visual signals, olfactory signals, or both). Bumblebees had no innate preference for either subspecies. Bumblebees trained on the yellow-flowered subspecies later preferred the yellow type, even when only visual or only olfactory signals were available, and their preference was not reinforced when both signal types were available. In contrast, bumblebees trained on the magenta-flowered subspecies showed no further preference between floral types and took slightly more time to make their choice. Since pollinator constancy has been observed in wild populations of A. majus with mixed floral types, we suggest that such constancy likely relies on short-term memory rather than acquired preference through long-term memory induced by prior learning.
(61) Courchamp F., J. Dunne, Y. Le Maho, R. May, C. Thébaud & M. Hochberg. Back to fundamentals: a reply to Barot et al. Trends in Ecology and Evolution 30: 370-371
In this reply to Barot et al.'s comment on our paper "Fundamental Ecology is Fundamental", we argue that, of course, researchers can easily reconcile a search for basic understanding with a quest to solve societally relevant problems. However, we do not see why all ecologists should do so, nor why any given ecologist cannot conduct research projects that are basic science, others with additional applied objectives, and yet other projects which are purely applied. Systematically intermingling applied and fundamental ecology may be tempting but, we argue, will result in the gradual demise of fundamental ecology, and will negatively impact on ecology as a science. While not foregoing support for applied ecology, we think that a plea for renewed support for fundamental ecology is incompatible with the merger proposed by Barot et al. who insist that science should be co-designed with stakeholders at multiple levels. We argue that the basis of fundamental ecology is understanding. It must remain, be protected, and be promoted as an end unto itself.
(60) Besnard G., J. Bertand, B. Delahaie, Y. Bourgeois, E. Lhuillier, and C. Thébaud. Valuing museum specimens: high-throughput DNA sequencing using historical collections of New Guinea crowned pigeons (Goura). Biological Journal of the Linnean Society 117, 71-82
Museum specimens are of particular importance for investigating systematics and the biogeography as well as other aspects of the evolution of biodiversity. They are also a depository of specimens accumulated over recent historical times and often the only way to study recently extinct or rare species. Unfortunately, most museum specimens yield low-quality DNA limiting their generalized use in phylogenetic and population genetic studies. Advances in sequencing technologies now offer opportunities to analyse such material even from very small tissue. Here, we applied the Illumina technology (HiSeq) on three specimens of crowned pigeon (Goura spp.) collected in New Guinea between 1879 and 1934. A shotgun strategy allowed us to quickly and reliably assemble complete mitochondrial genomes and fragments of three single-copy gene phylogenetic markers even with low double- stranded DNA quantity (9 to 69 ng). Phylogenetic assignments of these new sequences confirmed them as Goura sequences. Therefore, our study confirms the power of using next-generation sequencing methods to investigate the evolutionary history of species for which access to fresh samples is limited but museum collections are available. These approaches are considerably increasing the value of many natural history collections for genetic investigations, particularly from biodiversity hotspots that are presently difficult to prospect.
(59) Bertrand J., Y. Bourgeois, & C. Thébaud. Population density of the Réunion Grey White-eye (Zosterops borbonicus) within the summit ecosystems of Réunion (Mascarene Islands). Ostrich 87, 85-88
Assessing population density is crucial for studying ecology and evolutionary biology of species as well as for conservation purposes. Here we used point count methods to infer population density in a single-island endemic passerine bird, the Réunion Grey White-eye (Zosterops borbonicus), that displays striking evidence of differentiation at a small spatial scale.. Population density was estimated at 5.17 birds per hectare (CL: 4.85-5.50), a value somewhat higher than previously believed. This estimation provides the first detailed estimation of bird population density in the vulnerable summit ecosystems of Réunion and will possibly allow a better understanding of the evolutionary causes of this plumage colour variation.
(58) Warren B.H., 22 other authors, & C. Thébaud. Islands as model systems in ecology and evolution: progress and prospects fifty years after MacArthur-Wilson. Ecology Letters 18: 200-217
The study of islands as model systems has played an important role in the development of evolutionary and ecological theory. The 50th anniversary of MacArthur and Wilson’s (December 1963) article, “An equilibrium theory of insular zoogeography”, was a recent milestone for this theme. Since 1963, island systems have provided new insights into the formation of ecological communities. Here, building on such developments, we highlight prospects for research on islands to improve our understanding of the ecology and evolution of communities in general. Throughout, we emphasise how attributes of islands combine to provide unusual research opportunities, the implications of which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-assessment of some fundamental issues that interested MacArthur and Wilson. These include the formation of ecological networks, species abundance distributions, and the contribution of evolution to community assembly. We also extend our prospects to other fields of ecology and evolution – understanding ecosystem functioning, speciation, and diversification – frequently employing assets of oceanic islands in inferring the geographic area within which evolution has occurred, and potential barriers to gene flow. Although island-based theory is continually being enriched, incorporating non-equilibrium dynamics is identified as a major challenge for the future.
(57) Courchamp F., J. Dunne, Y. Le Maho, R. May, C. Thébaud, & M. Hochberg. Fundamental ecology is fundamental. Trends in Ecology and Evolution 30: 9-16
The primary reasons for conducting fundamental research are satisfying curiosity, acquiring knowledge, and achieving understanding.%
Acoustic communication plays a prominent role in various ecological and evolutionary processes involving social interactions. The properties of acoustic signals are thought to be influenced not only by the interaction between signaller and receiver but also by the acoustic characteristics of the environment through which the signal is transmitted. This conjecture forms the core of the so-called “acoustic adaptation hypothesis” (AAH), which posits that vegetation structure affects frequency and temporal parameters of acoustic signals emitted by a signaller as a function of their acoustic degradation properties. Specifically, animals in densely vegetated ‘closed habitats’ are expected to produce longer acoustic signals with lower repetition rates and lower frequencies (minimum, mean, maximum, and peak) compared to the ones inhabiting less vegetated ‘open habitats’. To date, this hypothesis has received mixed results, with the level of support depending on the taxonomic group and the methodology used. We conducted a systematic literature search of empirical studies testing for an effect of vegetation structure on acoustic signalling and assessed the generality of the AAH using a meta-analytic approach based on 371 effect sizes from 75 studies and 57 taxa encompassing birds, mammals and amphibians. Overall, our results do not provide consistent support for the AAH, neither in within-species comparisons (suggesting no overall phenotypically plastic response of acoustic signalling to vegetation structure) nor in among-species comparisons (suggesting no overall evolutionary response). However, when considering birds only, we found a weak support for the AAH in within-species comparisons, which was mainly driven by studies that measured frequency bandwidth, suggesting that this variable may exhibit a phenotypically plastic response to vegetation structure. For among-species comparisons in birds, we also found support for the AAH, but this effect was not significant after excluding comparative studies that did not account for phylogenetic non-independence. Collectively, our synthesis does not support a universal role of vegetation structure in the evolution of acoustic communication. We highlight the need for more empirical work on currently under-studied taxa such as amphibians, mammals, and insects. Furthermore, we propose a framework for future research on the AAH. We specifically advocate for a more detailed and quantitative characterization of habitats to identify frequencies with the highest detection probability and to determine if frequencies with greater detection distances are preferentially used. Finally, we stress that empirical tests of the AAH should focus on signals which are selected for increased transmission distance.
(103) Matthews, T, Triantis, K, Wayman, JP, Martin, TE, Hume, JP, Cardoso, P, Faurby, S, Mendenhall, C, Dufour, P, Rigal, F, Cooke, R, Whittaker, RJ, Pigot, AL, Thébaud, C, Jørgensen, MW, Benavides Rios, E, Soares, F, Ulrich, W, Kubota, Y, Sadler, J, Tobias, JA & Sayol, F 2024. The global loss of avian functional and phylogenetic diversity from anthropogenic extinctions. Science 386(6717):55-60. doi: 10.1126/science.adk7898. Epub 2024 Oct 3. PMID: 39361743.
Humans have been driving a global erosion of species richness for millennia, but the consequences of past extinctions for other dimensions of biodiversity—functional and phylogenetic diversity—are poorly understood. In this work, we show that, since the Late Pleistocene, the extinction of 610 bird species has caused a disproportionate loss of the global avian functional space along with ~3 billion years of unique evolutionary history. For island endemics, proportional losses have been even greater. Projected future extinctions of more than 1000 species over the next two centuries will incur further substantial reductions in functional and phylogenetic diversity. These results highlight the severe consequences of the ongoing biodiversity crisis and the urgent need to identify the ecological functions being lost through extinction.
(102) Poutaraud J., J. Sueur, C. Thébaud & S. Haupert. 2024. Meta-embedded clustering (MEC): A new method for improving
clustering quality in unlabeled bird sound datasets. Ecological Informatics 82: 102687
In recent years, ecoacoustics has offered an alternative to traditional biodiversity monitoring techniques with the development of passive acoustic monitoring (PAM) systems allowing, among others, to detect and identify species that are difficult to detect by human observers, automatically. PAM systems typically generate large audio datasets, but using these monitoring techniques to infer ecologically meaningful information remains challenging. In most cases, several thousand hours of recordings need to be manually labeled by experts limiting the operability of the systems. Based on recent developments of meta-learning algorithms and unsupervised learning techniques, we propose here Meta-Embedded Clustering (MEC), a new method with high potential for improving clustering quality in unlabeled bird sound datasets. MEC method is organized in two main steps, with: (a) fine-
tuning of a pretrained convolutional neural network (CNN) backbone with different meta-learning algorithms using pseudo-labeled data, and (b) clustering of manually-labeled bird sounds in the latent space based on vector embeddings extracted from the fine-tuned CNN. The MEC method significantly enhanced average clustering performance from less than 1% to more than 80%, greatly outperforming the traditional approach of relying solely on CNN features extracted from a general neotropical audio database. However, this enhanced performance came with the cost of excluding a portion of the data categorized as noise. By improving the quality of clustering in unlabeled bird sound datasets, the MEC method should facilitate the work of ecoacousticians in managing acoustic units of bird song/call clustered according to their similarities, and in identifying potential clusters of species undetected using traditional approaches.
(101) Cornuault J, M. Sanchez, T. Duval, A. Fouquet, & C. Thébaud. 2024. Deep genetic divergence underlies within-island eco-morphological variation in the endangered day gecko Phelsuma borbonica: implications for conservation. Conservation Genetics 25: 1035–1052. https://doi.org/10.1007/s10592-024-01622-w
The day gecko Phelsuma borbonica displays marked differences in coloration and occupies a variety of habitats across its very small range on the volcanic oceanic island of Reunion in the southwestern Indian Ocean. Such differences might reflect geographic and ecological divergence and thus be associated with an underlying genetic differentiation. We examined the partitioning of genetic diversity in Phelsuma borbonica across Reunion at a very small spatial scale (< 10 km) using mtDNA and nuDNA sequences, along with microsatellite genotype data. This study provides an account of the evolutionary history of Phelsuma borbonica, along with a quantification of effective population sizes, which constitute important information for the conservation of this endangered species, which may represent a previously unrecognized case of ncipient speciation. We found that populations of Phelsuma borbonica are genetically strongly differentiated, highlighting historically low levels of gene flow. Phylogenetic analyses suggest that Phelsuma borbonica reached its present range through two parallel southward expansions from an ancestral population located in the northern part of the island.
(100) Kitching R.L., C. Wenda,· J. Rochat,· C. Thébaud, · D. Strasberg, · K. Vogiatzis, ·S. Xing, & · L. A. Ashton. 2024. Diversity and turnover in moth assemblages in rainforests on a remote oceanic island. Biodiversity and Conservation 33 : 2265–2284. https://doi.org/10.1007/s10531-024-02874-1
Spatially driven turnover in species composition and relative abundance drives gamma diversity in all ecosystems. Assemblages of nocturnal Lepidoptera in rainforests are powerful tools for estimating and understanding this heterogeneity. There are three fundamental theoretical tools for explaining this place-to-place change: neutral stochasticity, niche-driven opportunity and historical contingency. We sampled moth and woody plant assemblages across the oceanic island landscape of La Réunion to tease apart how these factors shape diversity. We collected a total of ~ 13000 individuals of about 229 species and analyzed how distance and forest habitats shape moth assemblage turnover. We subdivided moth species into endemics and non-endemics. Our results show the local occurrence of the generally more diet-restricted endemic moths is more likely to be niche-driven due to host-plant preferences while occurrence of the generally more polyphagous non-endemic species is most parsimoniously explained by stochastic neutral mechanisms. Spatial patterns in the native flora may also be neutrally assembled sets across the rainforest region
(with implications for native moth species) whereas introduced species reflect human-driven historical contingency.
(99) Vacher J.-P., , P.J..R. Kok, M.T. Rodrigues, A. Lima, T. Hrbek, F.P. Werneck, S. Manzi, C. Thébaud, & A. Fouquet, 2024. Diversification of the terrestrial frog genus Anomaloglossus (Anura, Aromobatidae) in the Guiana Shield proceeded from highlands to lowlands, with successive loss and reacquisition of endotrophy, Molecular Phylogenetics and Evolution doi: 10.1016/j.ympev.2023.108008. Epub 2024 Jan 3. PMID: 38181828.
Two main landscapes emerge from the Guiana Shield: the highlands to the west called the Pantepui region and the Amazonian lowlands to the east, both harbouring numerous endemic species. With 32 currently recognized species, the genus Anomaloglossus stands out among Neotropical frogs as one that diversified only within the Guiana Shield both in the highlands and the lowlands. We present a time-calibrated phylogeny obtained by using combined mitogenomic and nuclear DNA, which suggests that the genus originates from Pantepui where extant lineages started diversifying around 21 Ma, and subsequently (ca. 17 Ma) dispersed during the Miocene Climatic Optimum to the lowlands of the eastern Guiana Shield where the ability to produce endotrophic tadpoles evolved. Further diversification within the lowlands in the A. stepheni group notably led to an evolutionary reversal toward exotrophy in one species group during the late Miocene, followed by reacquisition of endotrophy during the Pleistocene. These successive shifts of reproductive mode seem to have accompanied climatic oscillations. Long dry periods might have triggered evolution of exotrophy, whereas wetter climates favoured endotrophic forms, enabling colonization of terrestrial habitats distant from water. Acquisition, loss, and reacquisition of endotrophy makes Anomaloglossus unique among frogs and may largely explain the current species diversity. The micro evolutionary processes involved in these rapid shifts of reproductive mode remain to be revealed.
(98) Ferreira F., Kraus F., Richards S., Oliver P., Günther R., Trilaksono W., Arida E.A., Amidy A., Riyanto A., Tjaturadi B., Thébaud C., Fouquet A. 2023. Species delimitation and phylogenetic analyses of a New Guinean frog genus (Microhylidae: Hylophorbus) reveal many undescribed species and a complex diversification history driven by late Miocene events. Zoological Journal of the Linnean Society, Volume 202, Issue 2, https://doi.org/10.1093/zoolinnean/zlad168
New Guinea is the largest tropical island in the world and hosts immense endemic biodiversity. However, our understanding of how the gradual emergence of the terrestrial ecosystems of the island over the last 40 Myr has generated this biological richness is hampered by poorly documented species diversity and distributions. Here, we address both these issues through an integrative taxonomy and biogeographical approach using Hylophorbus, a New Guinea-endemic genus of frogs with 12 recognized species. We delimited candidate species by integrating mitochondrial DNA, nuclear DNA, and bioacoustics, then investigated their evolutionary history. Our results suggest that the current taxonomy of the genus misses true species diversity by ≥3.5-fold. Nevertheless, most candidate species (27) remain unconfirmed because of missing data, whereas five were identified unambiguously as undescribed (we describe three of these formally). Time-calibrated phylogenetic analyses suggest that Hylophorbus diversification began ~9 Mya in the northern or eastern portion of New Guinea. It would appear that lineages dispersed to new terrestrial habitats in the west, notably uplifted by the central range orogeny, until eventually reaching the Bird’s Head during the Mio-Pliocene (7–5 Mya). Conversely, a past barrier appears to have prevented north–south dispersal. These data suggest that new habitat availability has primarily driven the diversification of Hylophorbus.
(97) Gabrielli M., T. Leroy, J. Salmona, B. Nabholz, Borja Milá, & C. Thébaud. 2024. Demographic responses of oceanic island birds to local and regional ecological disruptions revealed by whole-genome sequencing. Molecular Ecology 33(4):e17243. doi: 10.1111/mec.17243. Epub 2023 Dec 18. PMID: 38108507.
Disentangling the effects of ecological disruptions operating at different spatial and temporal scales in shaping past species' demography is particularly important in the current context of rapid environmental changes driven by both local and regional factors. We argue that volcanic oceanic islands provide useful settings to study the influence of past ecological disruptions operating at local and regional scales on population demographic histories. We investigate potential drivers of past population dynamics for three closely related species of passerine birds from two volcanic oceanic islands, Reunion and Mauritius (Mascarene archipelago), with distinct volcanic history. Using ABC and PSMC inferences from complete genomes, we reconstructed the demographic history of the Reunion Grey White-eye (Zosterops borbonicus (Pennant, 1781)), the Reunion Olive White-eye (Z. olivaceus (Linnaeus, 1766)) and the Mauritius Grey White-eye (Z. mauritianus (Gmelin, 1789)) and searched for possible causes underlying similarities or differences between species living on the same or different islands. Both demographic inferences strongly support ancient and long-term expansions in all species. They also reveal different trajectories between species inhabiting different islands, but consistent demographic trajectories in species or populations from the same island. Species from Reunion appear to have experienced synchronous reductions in population size during the Last Glacial Maximum, a trend not seen in the Mauritian species. Overall, this study suggests that local events may have played a role in shaping population trajectories of these island species. It also highlights the potential of our conceptual framework to disentangle the effects of local and regional drivers on past species' demography and long-term population processes.
(96) Mould MC, M. Huet, L. Senegas, B. Mila, C. Thébaud, Y. Bourgeois & A. Chaine. 2023. Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird. Journal of evolutionary Biology 36, 82-94
Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.
(95) Utami CY, A Sholihah, FL Condamine, C Thébaud, N Hubert. 2022. Cryptic diversity impacts model selection and macroevolutionary inferences in diversification analyses. Proceedings of the Royal Society B 289(1987):20221335. doi: 10.1098/rspb.2022.1335. Epub 2022 Nov 16. PMID: 36382998; PMCID: PMC9667750.
Species persist in landscapes through ecological dynamics but proliferate at wider spatial scales through evolutionary mechanisms. Disentangling the contribution of each dynamic is challenging, but the increasing use of dated molecular phylogenies opened new perspectives. First, the increasing use of DNA sequences in biodiversity inventory shed light on a substantial amount of cryptic diversity in species-rich ecosystems. Second, explicit diversification models accounting for various eco-evolutionary models are nowavailable. Integrating both advances, we explored diversification trajectories among 10 lineages of freshwater fishes in Sundaland, for which time-calibrated and taxonomically rich phylogenies are available. By fitting diversification models to dated phylogenies and incorporatingDNA-based species delimitation methods, the impact of cryptic diversity on diversification model selection and related inferences is explored. Eight clades display constant speciation rate model as the most likely if cryptic diversity is accounted, but nine display a signature of diversification slowdownswhen cryptic diversity is ignored. Cryptic diversification occurs during the last 5 Myr for most groups, and palaeoecologicalmodels received little support. Most cryptic lineages display restricted range distribution, supporting geographical isolation across homogeneous landscapes as the main driver of diversification. These patterns question the persistence of cryptic diversity and its role during species proliferation.
(94) Matthews Thomas J, Joseph P Wayman, Pedro Cardoso, Ferran Sayol, Julian P Hume, Werner Ulrich, Joseph A Tobias, Filipa C Soares, Christophe Thébaud, Thomas E Martin, Kostas A Triantis. 2022. Threatened and extinct island endemic birds of the world: Distribution, threats and functional diversity. Journal of Biogeography 49, 1920-1940
The world's islands support disproportionate levels of endemic avian biodiversity despite suffering numerous extinctions. While intensive recent research has focused on island bird conservation or extinction, few global syntheses have considered these factors together from the perspective of morphological trait diversity. Here, we provide a global summary of the status and ecology of extant and extinct island birds, the threats they face and the implications of species loss for island functional diversity.. Here we provide a review of the literature on threatened and extinct island birds, with a particular focus on global studies that have incorporated functional diversity. Alongside this, we analyse IUCN Red List data in relation to distribution, threats and taxonomy. Using null models and functional hypervolumes, in combination with morphological trait data, we assess the functional diversity represented by threatened and extinct island endemic birds. We find that almost half of all island endemic birds extant in 1500 CE are currently either extinct or threatened with extinction, with the majority of threatened extant species having declining population trends. We also found evidence of 66 island endemic subspecies extinctions. The primary threats to extant island endemic birds currently are agriculture, biological resource use, and invasive species. While there is overlap between the hotspots of threatened and extinct island endemics birds, there are some notable differences, including the Philippines and Indonesia, which support a substantial number of threatened species but have no recorded post-1500 CE bird extinctions. Traits associated with threatened island endemic birds are large body mass, flightlessness, aquatic predator, omnivorous and vertivorous trophic niches, marine habitat affinity, and, paradoxically, higher dispersal ability. Critically, we find that threatened endemics (i) occupy distinct areas of beak morphospace, and (ii) represent substantial unique areas of the overall functional space of island endemics. We caution that the loss of threatened species may have severe effects on the ecological functions birds provide on islands.
(93) Emerson Brent , Paulo Borges, Pedro Cardoso, Peter Convey, Jeremy deWaard, Evan Economo, Rosemary Gillespie, Susan Kennedy, Henrik Krehenwinkel, Rudolf Meier, George Roderick, Dominique Strasberg, Christophe Thébaud, Anna Traveset, Thomas Creedy, Emmanouil Meramveliotakis, Victor Noguerales, Isaac Overcast, Hélène Morlon, Anna Papadopoulou, Alfried Vogler, Paula Arribas, Carmelo Andujar. 2022. Collective and harmonised high throughput barcoding of insular arthropod biodiversity: toward a Genomic Observatories Network for islands. Molecular Ecology 32(23):6161-6176. doi: 10.1111/mec.16683. Epub. PMID: 36156326.
Our current understanding of ecological and evolutionary processes underlying island biodiversity is heavily shaped by empirical data from plants and birds, although arthropods comprise the overwhelming majority of known animal species. This is due to inherent problems with obtaining high-quality arthropod data. Novel high throughput sequencing approaches are now emerging as powerful tools to overcome such limitations, and thus comprehensively address existing shortfalls in arthropod biodiversity data. Here we explore how, as a community, we might most effectively exploit these tools for comprehensive and comparable inventory and monitoring of insular arthropod biodiversity. We first review the strengths, limitations and potential synergies among existing approaches of high throughput barcode sequencing. We consider how this can be complemented with deep learning approaches applied to image analysis to study arthropod biodiversity. We then explore how these approaches can be implemented within the framework of an island Genomic Observatories Network (iGON) for the advancement of fundamental and applied understanding of island biodiversity. To this end, we identify seven island biology themes at the interface of ecology, evolution and conservation biology, within which collective and harmonised efforts in HTS arthropod inventory could yield significant advances in island biodiversity research.
(92) Triantis Kostas A., Francois Rigal, Robert J. Whittaker, Julian P. Hume, Catherine Sheard, Dimitrios Poursanidis, Jonathan Rolland, Spyros Sfenthourakis, Thomas J. Matthews, Christophe Thébaud, Joseph A. Tobias. Deterministic assembly and anthropogenic extinctions drive convergence of island bird communities. Global Ecology and Biogeography 31 : 1741-1755
Whether entire communities of organisms converge towards predictable structural properties in similar environmental conditions remains controversial. We tested for community convergence in birds by comparing the structure of oceanic archipelago assemblages with their respective regional species pools.
Here we compiled a comprehensive database of morphological trait and phylogenetic data for 6,579 bird species, including species known to have become extinct owing to human activities. We quantified morphological and phylogenetic dissimilarity among species between pairs of archipelagos, using a modified version of the mean nearest taxon distance. We tested for convergence by estimating whether overall mean turnover among archipelagos and pairwise turnover between archipelagos were lower than expected by chance.
For all land birds, we found that turnover in body plan, body mass and phylogeny among archipelagos was significantly lower than expected. Seventeen (of 18) archipelagos showed significant body plan and phylogenetic similarity with at least one other archipelago. Similar convergent patterns of community assembly were detected in different subsamples of the data (extant species, endemics, native non-endemics, and Passeriformes only). Convergence was more pronounced for extant species than for extant and extinct species combined.
Consistent convergence in phylogenetic and morphological structure among archipelagic communities arises through a combination of non-random colonization and in situ adaptation. In addition, by including data from extinct taxa, we show that community convergence both precedes and is accentuated by the anthropogenic extinction of endemic lineages. Our results highlight the potential role of non-random extinction in generating patterns of community convergence and show that convergence existed even before anthropogenic extinctions, owing to deterministic community assembly in similar environmental settings at the global scale.
(91) Milá B., J. Bruxaux, G. Friis, K. Sam, H. Ashari, & C. Thébaud. 2021. A new, undescribed species of Melanocharis berrypecker from western New Guinea and the evolutionary history of the family Melanocharitidae. Ibis 163: 1310-1329
Western New Guinea remains one of the last biologically underexplored regions of the world, and much remains to be learned regarding the diversity and evolutionary history of its fauna and flora. During a recent ornithological expedition to the Kumawa Mountains in West Papua, we encountered an undescribed species of Melanocharis berrypecker (Melanocharitidae) in cloud forest at an elevation of 1200 m asl. Its main characteristics are iridescent blue-black upperparts, satin-white underparts washed lemon yellow, and white outer edges to the external rectrices. Initially thought to represent a close relative of the Mid-mountain Berrypecker Melanocharis longicauda based on elevation and plumage colour traits, a complete phylogenetic analysis of the genus based on full mitogenomes and genome-wide nuclear data revealed that the new species, which we name Satin Berrypecker Melanocharis citreola sp. nov., is in fact sister to the phenotypically dissimilar Streaked Berrypecker M. striativentris. Phylogenetic relationships within the family Melanocharitidae, including all presently recognized genera (Toxorhamphus, Oedistoma, Rhamphocharis and Melanocharis), reveal that this family endemic to the island of New Guinea diversified during the main uplift of New Guinea in the Middle and Late Miocene (14-6 Mya), and represents an evolutionary radiation with high disparity in bill morphology and signalling traits across species. Rhamphocharis berrypeckers fall within the Melanocharis clade despite their larger beaks, and should be included in the latter genus. Interspecific genetic distances in Melanocharis are pronounced (average interspecific distance: 8.8% in COI, 12.4% in ND2), suggesting a long history of independent evolution of all lineages corresponding to currently recognized species, including the Satin Berrypecker, which shares a most recent common ancestor with its sister species in the early Pleistocene (~2.0 Mya).
(90) Arida E, Ashari H, Dahruddin H, Fitriana YS, Hamidy A, Irham M, Kadarusman, Riyanto A, Wiantoro S, Zein MSA, Hadiaty RK, Apandi, Krey F, Kurnianingsih, Melmambessy EHP, Mulyadi, Ohee HL, Saidin, Salamuk A, Sauri S, Suparno, Supriatna N, Suruwaky AM, Laksono WT, Warikar EL, Wikanta H, Yohanita AM, Slembrouck J, Legendre M, Gaucher P, Cochet C, Delrieu-Trottin E, Thébaud C, Mila B, Fouquet A, Borisenko A, Steinke D, Hocdé R, Semiadi G, Pouyaud L, Hubert N. 2021. Exploring the vertebrate fauna of the Bird's Head Peninsula (Indonesia, West Papua) through DNA barcodes. Mol Ecol Resour.ces 21:2369-2387.
Biodiversity knowledge is widely heterogeneous across the Earth's biomes. Some areas, due to their remoteness and difficult access, present large taxonomic knowledge gaps. Mostly located in the tropics, these areas have frequently experienced a fast development of anthropogenic activities during the last decades and are therefore of high conservation concerns. The biodiversity hotspots of Southeast Asia exemplify the stakes faced by tropical countries. While the hotspots of Sundaland (Java, Sumatra, Borneo) and Wallacea (Sulawesi, Moluccas) have long attracted the attention of biologists and conservationists alike, extensive parts of the Sahul area, in particular the island of New Guinea, have been much less explored biologically. Here, we describe the results of a DNA-based inventory of aquatic and terrestrial vertebrate communities, which was the objective of a multidisciplinary expedition to the Bird's Head Peninsula (West Papua, Indonesia) conducted between 17 October and 20 November 2014. This expedition resulted in the assembly of 1005 vertebrate DNA barcodes. Based on the use of multiple species-delimitation methods (GMYC, PTP, RESL, ABGD), 264 molecular operational taxonomic units (MOTUs) were delineated, among which 75 were unidentified and an additional 48 were considered cryptic. This study suggests that the diversity of vertebrates of the Bird's Head is severely underestimated and considerations on the evolutionary origin and taxonomic knowledge of these biotas are discussed.
(89) Aguilée R., F. Pellerin, M. Soubeyrand, J. Choin, & C. Thébaud. 2021. Biogeographic drivers of community assembly on oceanic islands: the importance gf archipelago structure and history. J. Biogeography 48(10), pp.2616-2628.
Aim: Accounting for geo-environmental dynamics is crucial to understand community assembly across islands. Whittaker et al. (J Biogeogr, 35:977–994, 2008)’s General Dynamic Model (GDM) aims towards this goal. Yet, it does not explicitly consider that most islands belong to archipelagos. We examined how island biodiversity dynamics are influenced by the interaction of eco-evolutionary processes acting at the archipelago level with each island's geo-environmental dynamics.
Location: Hypothetical archipelagos.
Taxon: Any.
Methods: We used an individual-based model, ecologically neutral within the archipelago. Several islands emerge in succession with a typical volcanic ontogeny. We considered both mainland and inter-island dispersal. Geographically isolated lineages diverged over time, possibly speciating.
Results: We found diversity to be at dynamic equilibrium. In an archipelago, islands hosted more diversity and more endemic species, at both island and archipelago levels, than an equivalently-sized single isolated island. This was due to an ‘archipelago effect’: inter-island dispersal increased within-island diversity through species occurrence on multiple islands; species may undergo anagenetic changes on the colonised islands, eventually speciating, thereby increasing archipelago diversity. Biodiversity dynamics of different islands may differ even on islands with identical geo-environmental dynamics because the archipelago effect varied over time and affected each island differently (‘history effect’). By accounting for these effects, we predicted detectable deviations from the GDM predictions, which are largest for remote archipelagos, with islands located close together and with an intermediate time of island emergence. In linear stepping-stone archipelagos, we predicted higher diversity on centrally located islands.
Main conclusions: Our results demonstrate that analyses of insular biodiversity data would greatly benefit from explicitly accounting for both archipelago and history effects. We suggest incorporating variables characterising the spatio-temporalstructure of the whole archipelago. We discuss possible difficulties in distinguishing between the archipelago effect and equilibrium diversity dynamics.
(88) Leroy T., M. Rousselle, M.-K. Tilak, A.E. Caizergues, C. Scornavacca, M. Recuerda, J. Fuchs, J.C. Illera, D.H. de Swardt, G. Blanco, C. Thébaud, B. Milá, & B. Nabholz. 2021. Island songbirds as windows into evolution in small populations. Current Biology 31(6), pp.1303-1310.
Due to their limited ranges and inherent isolation, island species have long been recognized as crucial systems for tackling a range of evolutionary questions, including in the early study of speciation.1,2 Such species have been less studied in the understanding of the evolutionary forces driving DNA sequence evolution. Island species usually have lower census population sizes (N) than continental species and, supposedly, lower effective population sizes (Ne). Given that both the rates of change caused by genetic drift and by selection are dependent upon Ne, island species are theoretically expected to exhibit (1) lower genetic diversity, (2) less effective natural selection against slightly deleterious mutations,3,4 and (3) a lower rate of adaptive evolution.5, 6, 7, 8 Here, we have used a large set of newly sequenced and published whole-genome sequences of Passerida species (14 insular and 11 continental) to test these predictions. We confirm that island species exhibit lower census size and Ne, supporting the hypothesis that the smaller area available on islands constrains the upper bound of Ne. In the insular species, we find lower nucleotide diversity in coding regions, higher ratios of non-synonymous to synonymous polymorphisms, and lower adaptive substitution rates. Our results provide robust evidence that the lower Ne experienced by island species has affected both the ability of natural selection to efficiently remove weakly deleterious mutations and also the adaptive potential of island species, therefore providing considerable empirical support for the nearly neutral theory. We discuss the implications for both evolutionary and conservation biology.
(87) Valente, L., Phillimore, A. B., Melo, M., Warren, B. H., Clegg, S. M., Havenstein, K., Tiedemann, R., Illera, J. C., Thébaud, C., Aschenbach, T. & Etienne, R. S. 2020. A simple dynamic model explains island bird diversity worldwide. Nature, 579: 92–96.
Colonization, speciation and extinction are dynamic processes that influence global patterns of species richness. Island biogeography theory predicts that the contribution of these processes to the accumulation of species diversity depends on the area and isolation of the island. Notably, there has been no robust global test of this prediction for islands where speciation cannot be ignored9, because neither the appropriate data nor the analytical tools have been available. In this paper, we addressed both deficiencies to reveal, for island birds, the empirical shape of the general relationships that determine how colonization, extinction and speciation rates co-vary with the area and isolation of islands. We compiled a global molecular phylogenetic dataset of birds on islands, based on the terrestrial avifaunas of 41 oceanic archipelagos worldwide (including 596 avian taxa), and applied a new analysis method to estimate the sensitivity of island-specific rates of colonization, speciation and extinction to island features (area and isolation). Our model predicts—with high explanatory power—several global relationships. We found a decline in colonization with isolation, a decline in extinction with area and an increase in speciation with area and isolation. Combining the theoretical foundations of island biogeography with the temporal information contained in molecular phylogenies proves a powerful approach to reveal the fundamental relationships that govern variation in biodiversity across the planet.
(86) Gabrielli M., T. Leroy, B. Nabholz, B. Milá, & C. Thébaud. 2020. Within-island diversification in a passerine bird. Proceeding of the Royal Society B 287: 20192999. http://dx.doi.org/10.1098/rspb.2019.2999
The presence of congeneric taxa on the same island suggests the possibility of in situ divergence, but can also result from multiple colonizations of pre- viously diverged lineages. Here, using genome-wide data from a large population sample, we test the hypothesis that intra-island divergence explains the occurrence of four geographical forms meeting at hybrid zones in the Reunion grey white-eye (Zosterops borbonicus), a species complex endemic to the small volcanic island of Reunion. Using population genomic and phylogenetic analyses, we reconstructed the population history of the different forms. We confirmed the monophyly of the complex and found that one of the lowland forms is paraphyletic and basal relative to others, a pattern highly consistent with in situ divergence. Our results suggest initial colonization of the island through the lowlands, followed by expansion into the highlands, which led to the evolution of a distinct geographical form, genetically and ecologically different from the lowland ones. Lowland forms seem to have experienced periods of geographical isolation, but they diverged from one another by sexual selection rather than niche change. Overall, low dispersal capabilities in this island bird combined with both geographical and ecological opportunities seem to explain how divergence occurred at such a small spatial scale.
(85) Bourgeois Y.X.C., J.A.M Bertrand, B. Delahaie, H. Holota, C. Thébaud, and B. Milá. 2020. Differential divergence in autosomes and sex chromosomes is associated with intra-island diversification at a very small spatial scale in a songbird lineage. Molecular Ecology 29(6), pp.1137-1153.
Recently diverged taxa showing marked phenotypic and ecological diversity provide optimal systems to understand the genetic processes underlying speciation. We used genome-wide markers to investigate the diversification of the Reunion grey white-eye (Zosterops borbonicus) on the small volcanic island of Reunion (Mascarene archipelago), where this species complex exhibits four geographical forms that are parapatrically distributed across the island and differ strikingly in plumage colour. One form restricted to the highlands is separated by a steep ecological gradient from three distinct lowland forms which meet at narrow hybrid zones that are not associ- ated with environmental variables. Analyses of genomic variation based on single nucleotide polymorphism data from genotyping-by-sequencing and pooled RAD-seq approaches show that signatures of selection associated with elevation can be found at multiple regions across the genome, whereas most loci associated with the low- land forms are located on the Z sex chromosome. We identified TYRP1, a Z-linked colour gene, as a likely candidate locus underlying colour variation among lowland forms. Tests of demographic models revealed that highland and lowland forms di- verged in the presence of gene flow, and divergence has progressed as gene flow was restricted by selection at loci across the genome. This system holds promise for in- vestigating how adaptation and reproductive isolation shape the genomic landscape of divergence at multiple stages of the speciation process.
(84) Vacher J.P., J. Chave, F. Ficetola, G. Sommeria-Klein, S. Tao, C. Thébaud, M. Blanc, A. Camacho, J. Cassimiro, T.J. Colston, M. Dewynter, R. Ernst, P. Gaucher, J.O. Gomes, R. Jairam, P.J.R. Kok, J.D. Lima, Q. Martinez, C. Marty, B.P. Noonan, P. Nunes, P. Ouboter, R. Recoder, M.T. Rodrigues, A. Snyder, S. Maques de Souza, & A. Fouquet. 2020. Large-scale DNA-based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography 47(8), 1781-1791.
Mapping Amazonian biodiversity accurately is a major challenge for integrated conservation strategies and to study its origins. However, species boundaries and their respective distribution are notoriously inaccurate in this region. In this paper, we generated a georeferenced database of short mtDNA sequences from Amazonian frogs, revised the species richness and the delineation of bioregions of the Eastern Guiana Shield and estimated endemism within these bioregions.
We used an extensive DNA-based sampling of anuran amphibians of Amazonia using next-generation sequencing to delineate Operational Taxonomic Units (OTU) and their distribution. We analysed this database to infer bioregions using Latent Dirichlet Allocation modelling. We then compared endemism within these bioregions based on our results and the current IUCN database, and inferred environmental variables that contributed the most to the biogeographic pattern.
The recognized anuran species richness within the focal area increased from 440 species currently listed by the IUCN Red List to as much as 876 OTUs with our dataset. We recovered eight bioregions, among which three lie within the Eastern Guiana Shield. We estimated that up to 82% of the OTUs found in this area are en- demic, a figure three times higher than the previous estimate (28%). Environmental features related to seasonal precipitations are identified as playing an important role in shaping Amazonian amphibian bioregions.
(83) Warren B.H., R.E. Ricklefs, C. Thébaud, D. Gravel, & N. Mouquet. 2019. How consideration of islands has inspired mainstream ecology: links between the theory of island biogeography and some other key theories. Reference Module in Earth Systems and Environmental Sciences, Elsevier, 10.1016/B978-0-12-409548-9.11788-9 .
The passing of the 50th anniversary of the theory of island biogeography (IBT) has helped spur a new wave of interest in the biology of islands. Despite the longstanding acclaim of MacArthur and Wilson’s (1963, 1967) theory, the breadth of its influence in mainstream ecology today is easily overlooked. Here we summarize some of the main links between IBT and subsequent developments in ecology. These include not only modifications to the core model to incorporate greater biological complexity, but also the role of IBT in inspiring two other quantitative theories that are at least as broad in relevance—metapopulation theory and ecological neutral theory. Using habitat fragmentation and life-history evolution as examples, we also argue that a significant legacy of IBT has been in shaping and unifying ecological schools of thought.
(82) Leroy T., Y. Anselmetti, M.-K. Tilak, S. Berard, L. Csukonyi, M. Gabrielli, C. Scornavacca, B. Mila, C. Thébaud, & B. Nabholz. 2019. A bird’s white-eye view on neo-sex chromosome evolution. Peer Community Journal 1, article no. e63.
Chromosomal organization is relatively stable among avian species, especially with regards to sex chromosomes. Members of the large Sylvioidea clade however have a pair of neo-sex chromosomes which is unique to this clade and originate from a parallel translocation of a region of the ancestral 4A chromosome on both W and Z chromosomes. Here, we took advantage of this unusual event to study the early stages of sex chromosome evolution. To do so, we sequenced a female (ZW) of two Sylvioidea species, a Zosterops borbonicus and a Z. pallidus. Then, we organized the Z. borbonicus scaffolds along chromosomes and annotated genes. Molecular phylogenetic dating under various methods and calibration sets confidently confirmed the recent diversification of the genus Zosterops (1-3.5 million years ago), thus representing one of the most exceptional rates of diversification among vertebrates. We then combined genomic coverage comparisons of five males and seven females, and homology with the zebra finch genome (Taeniopygia guttata) to identify sex chromosome scaffolds, as well as the candidate chromosome breakpoints for the two translocation events. We observed reduced levels of within-species diversity in both translocated regions and, as expected, even more so on the neoW chromosome. In order to compare the rates of molecular evolution in genomic regions of the autosomal-to-sex transitions, we then estimated the ratios of non-synonymous to synonymous polymorphisms (πN/πS) and substitutions (dN/dS). Based on both ratios, no or little contrast between autosomal and Z genes was observed, thus representing a very different outcome than the higher ratios observed at the neoW genes. In addition, we report significant changes in base composition content for translocated regions on the W and Z chromosomes and a large accumulation of transposable elements (TE) on the newly W region. Our results revealed contrasted signals of molecular evolution changes associated to these autosome-to- sex chromosome transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak suport for a fast-Z effect.
(81) Dale E.J., R. L. Kitching, C. Thébaud, S. C. Maunsell, L. A. Ashton. Moths in the Pyrénées: spatio-temporal patterns and indicators of elevational assemblages. Biodiversity and Conservation 28, 1593-1610
Understanding how assemblages of invertebrates change over continuous elevational gradients not only generates an understanding of current rules of community assembly but may also be useful for predicting the future distributions of species under global change. Temperature decreases predictably with increasing elevation and, accordingly, gradients in elevation permit the study of adjacent climates within small geographical areas. The present study examines if and how assemblages of moths change with increasing elevation in the eastern French Pyrenees. Elevation had a strong effect on the assemblage composition of moth species in both seasons. The species sets which contributed most to this strong pattern differed completely across seasons. Analysis of restrictions and fidelity to particular elevational ranges generated a set of indicator species which can be used to monitor future changes in distribution. Twelve species were identified as elevation-specific indicators (the 'predictor set’) from the spring samples and summer samples. We note the strong contrasts between species that produce overall statistical pattern and those that show strong fidelity to particular elevations and discuss this in terms of the biologies of the species concerned.
We discuss best practice for the identification and use of indicator species for monitoring future responses to climate change.
(80) Borges P.A.V., P. Cardoso, S. Fattorini, F. Rigal, T.J. Matthews, L. Di Biase, I.R. Amorim, M. Florencio, L. Borda- de-Água, C. Rego, F. Pereira, R. Nunes, R. Carvalho, M.T. Ferreira, H. López, A.J. Pérez Delgado, R. Otto, S. Fernández Lugo, L. de Nascimento, J. Caujapé-Castells, J. Casquet, S. Danflous, J. Fournel, A.-M. Sadeyen, R.B. Elias, J.M. Fernández-Palacios, P. Oromí, C. Thébaud, D. Strasberg, B.C. Emerson. 2018. Community structure of woody plants on islands along a bioclimatic gradient. Frontiers of Biogeography 10(3-4).10.21425/F5FBG40295
Understanding patterns of community structure and the causes for their variation can be furthered by comparative biogeographic analyses of island biotas. In this study, we used woody plant data at the local scale to investigate variations in species rarity, alpha, beta, and gamma diversity within and between three islands from the oceanic archipelagoes of Azores, Canaries and Mascarene. We used standardized protocols to sample ten 50 m × 50 m forest plots in each of the three islands with contrasting climate and regional species pools: Terceira (Azores), Tenerife (Canaries), and Reunion (Mascarene Islands). Occupancy frequency distributions and species abundance distributions were used to investigate rarity. The partitioning of beta diversity in a distance-decay framework was used to test for spatial patterns of community composition. Rarity was much more pronounced in the highly diverse islands of Tenerife and Reunion than in the regionally poorer island of Terceira. The number of species rose faster with increasing sample area in both Tenerife and Reunion. The slope of the species rank abundance curve was steeper in Terceira whereas the richer island assemblages approached a lognormal model. Compositional changes according to spatial distance were mostly due to replacement of species in Terceira and Reunion. Our results point to important differences in the community structure of Terceira, which is the less diverse and temperate region in comparison to Tenerife and Reunion which are highly diverse. High regional diversity of species in Tenerife and Reunion is a consequence of comparably long eco-evolutionary history that has promoted high levels of diversity which are not comparable to the relatively species-poor biota of the Azores, constrained by recent geological history and low environmental diversity.
(79) Warren Ben H., Oskar Hagen, Florian Gerber, Christophe Thébaud, Emmanuel Paradis, Elena Conti. 2018. Evaluating alternative explanations for an association of extinction risk and evolutionary uniqueness in multiple insular lineages. Evolution 72(10), 2005-2024.
Studies in insular environments have often documented a positive association of extinction risk and evolutionary uniqueness (i.e. how distant a species is from its closest living relative). However, the cause of this association is unclear. One explanation is that species threatened with extinction are evolutionarily unique because they are old, implying that extinction risk increases with time since speciation (age-dependent extinction). An alternative explanation is that such threatened species are last survivors of clades that have undergone an elevated extinction rate, and that their uniqueness results from the extinction of their close relatives. Distinguishing between these explanations is difficult but important, since they imply different biological processes determining extinction patterns. Here we designed a simulation approach to distinguish between these alternatives using living species, and applied it to twelve insular radiations that show a positive association between extinction risk and evolutionary uniqueness. We also tested the sensitivity of results to underlying assumptions and variable extinction rates. Despite differences among the radiations considered, age-dependent extinction was supported as best explaining the majority of the empirical cases. Biological processes driving characteristic changes in abundance with species duration (age-dependency) may merit further investigation.
(78) Kitson James J.N., Ben H. Warren, Christophe Thébaud, Dominique Strasberg, and Brent C. Emerson. Community assembly and diversification in a species-rich radiation of island weevils (Coleoptera: Cratopini). 2018. Journal of Biogeography 45, 2016-2026
Aim: To test a prediction derived from island biogeographical theory that in situ speciation should make an increasingly important contribution to community assembly as islands age. This prediction is tested on estimated biogeographical histories from Mauritius (approximately 9 Myr) and Reunion (approximately 5 Myr). We additionally investigate the evolutionary dynamics of insect flight loss, as the loss of flight in island lineages can influence patterns of diversification.
Location: Mascarene Islands; Southwest Indian Ocean.
Taxon: Weevils.
Methods: Up to five individuals of each taxonomically described species sampled within each sampling site were sequenced for the mitochondrial gene Cytochrome Oxidase II to delimit operational taxonomic units (OTUs). OTUs were further sequenced for the nuclear genes Arginine Kinase, Histone 3 and ribosomal 28s, to reconstruct the phylogenetic history of the group. Timings of colonization and in situ speciation events were estimated with BEAST2.
Results: Our results support the hypothesis that present-day species richness on the older island of Mauritius is largely the result of in situ speciation, with few colonization events, of which all but the most basal are recent. In contrast, Reunion presents a more uniform temporal spectrum of colonization times. Flight loss has evolved convergently at least five times, and speciation events associated with flight loss are significantly younger than speciation events that have not resulted in flight loss.
Main conclusions: Patterns of community assembly on the islands of Mauritius and Reunion fit a model where the addition of new species and species turnover is increasingly dominated by in situ speciation as an island community matures. Repeated flight loss indicates selection for flightlessness, with the young age of flightless lineages suggesting higher extinction rates over longer evolutionary timescales and little influence on present-day species richness.
(77) Borges Paulo A. V. , Pedro Cardoso, Holger Kreft, Robert J. Whittaker, Simone Fattorini, Brent C. Emerson, Artur Gil, Rosemary G. Gillespie, Thomas J. Matthews, Ana M. C. Santos, Manuel J. Steinbauer12 · Christophe Thébaud, Claudine Ah‐Peng, Isabel R. Amorim1,2 · Silvia Calvo Aranda, Ana Moura Arroz, José Manuel N. Azevedo, Mário Boieiro, Luís Borda‐de‐Água, José Carlos Carvalho, Rui B. Elias, José María Fernández‐Palacios, Margarita Florencio, Juana M. González‐Mancebo, Lawrence R. Heaney, Joaquín Hortal, Christoph Kueffer, Benoit Lequette, José Luis Martín‐Esquivel, Heriberto López, Lucas Lamelas‐López, José Marcelino, Rui Nunes, Pedro Oromí, Jairo Patiño, Antonio J. Pérez, Carla Rego, Sérvio P. Ribeiro, François Rigal, Pedro Rodrigues, Andrew J. Rominger, Margarida Santos‐Reis, Hanno Schaefer, Cecília Sérgio, Artur R. M. Serrano, Manuela Sim‐Sim, P. J. Stephenson, António O. Soares, Dominique Strasberg, Alain Vanderporten, Virgílio Vieira, Rosalina Gabriel. 2018. Global Island Monitoring Scheme (GIMS): a proposal for the long‐term coordinated survey and monitoring of native island forest biota. Biodiversity and Conservation 27, 2567–2586.
Islands harbour evolutionary and ecologically unique biota, which are currently disproportionately threatened by a multitude of anthropogenic factors, including habitat loss, invasive species and climate change. Native forests on oceanic islands are important refu-gia for endemic species, many of which are rare and highly threatened. Long-term monitor- ing schemes for those biota and ecosystems are urgently needed: (i) to provide quantitative baselines for detecting changes within island ecosystems, (ii) to evaluate the effectiveness of conservation and management actions, and (iii) to identify general ecological patterns andprocesses using multiple island systems as repeated ‘natural experiments’. In this contribu- tion, we call for a Global Island Monitoring Scheme (GIMS) for monitoring the remaining native island forests, using bryophytes, vascular plants, selected groups of arthropods and vertebrates as model taxa. As a basis for the GIMS, we also present new, optimized monitor- ing protocols for bryophytes and arthropods that were developed based on former standard- ized inventory protocols. Effective inventorying and monitoring of native island forests will require: (i) permanent plots covering diverse ecological gradients (e.g. elevation, age of ter- rain, anthropogenic disturbance); (ii) a multiple-taxa approach that is based on standardized and replicable protocols; (iii) a common set of indicator taxa and community properties that are indicative of native island forests’ welfare, building on, and harmonized with existing sampling and monitoring efforts; (iv) capacity building and training of local researchers, col- laboration and continuous dialogue with local stakeholders; and (v) long-term commitment by funding agencies to maintain a global network of native island forest monitoring plots.
(76) Bruxaux J, Gabrielli M, Ashari H, Prŷs-Jones R, Joseph L, Milá B, Besnard G, Thébaud C. Recovering the evolutionary history of crowned pigeons (Columbidae: Goura): Implications for the biogeography and conservation of New Guinean lowland birds. Molecular Phylogenetics and Evolution 120:248-258. doi: 10.1016/j.ympev.2017.11.022.
Assessing the relative contributions of immigration and diversification into the buildup of species diversity is key to understanding the role of historical processes in driving biogeographical and diversification patterns in species-rich regions. Here, we investigated how colonization, in situ speciation, and extinction history may have generated the present-day distribution and diversity of Goura crowned pigeons (Columbidae), a group of large forest-dwelling pigeons comprising four recognized species that are all endemic to New Guinea. We used a comprehensive geographical and taxonomic sampling based mostly on historical museum samples, and shallow shotgun sequencing, to generate complete mitogenomes, nuclear ribosomal clusters and independent nuclear conserved DNA elements. We used these datasets independently to reconstruct molecular phylogenies. Divergence time estimates were obtained using mitochondrial data only. All analyses revealed similar genetic divisions within the genus Goura and recovered as monophyletic groups the four species currently recognized, providing support for recent taxonomic changes based on differences in plumage characters. These four species are grouped into two pairs of strongly supported sister species, which were previously not recognized as close relatives: Goura sclaterii with Goura cristata, and Goura victoria with Goura scheepmakeri. While the geographical origin of the Goura lineage remains elusive, the crown age of 5.73 Ma is consistent with present-day species diversity being the result of a recent diversification within New Guinea. Although the orogeny of New Guinea's central cordillera must have played a role in driving diversification in Goura, cross-barrier dispersal seems more likely than vicariance to explain the speciation events having led to the four current species. Our results also have important conservation implications. Future assessments of the conservation status of Goura species should consider threat levels following the taxonomic revision proposed by del Hoyo and Collar (HBW and BirdLife International illustrated checklist of the birds of the world 1: non-passerines, 2014), which we show to be fully supported by genomic data. In particular, distinguishing G. sclaterii from G. scheepmakeri seems to be particularly relevant.
(75) Delahaie Boris, Josselin Cornuault, Charline Masson, Joris Bertrand, Yann Bourgeois, Borja Milá and Christophe Thébaud. Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex. Journal of evolutionary Biology 30:2132-2145
Patterns of phenotypic and genic frequencies across hybrid zones provide insight into the origin and evolution of reproductive isolation. The Reunion grey white-eye, Zosterops borbonicus, exhibits parapatrically distributed plumage colour forms across the lowlands of the small volcanic island of Reunion (Mascarene archipelago). These forms meet and hybridize in regions that are natural barriers to dispersal (rivers, lava fields). Here, we investigated the relationship among patterns of differentiation at neutral genetic (microsatellite) markers, phenotypic traits (morphology and plumage colour) and niche characteristics across three independent hybrid zones. Patterns of phenotypic divergence revealed that these hybrid zones are among the narrowest ever documented in birds. However, the levels of phenotypic divergence stand in stark contrast to the lack of clear population neutral genetic structure between forms. The position of the hybrid zones coincides with different natural physical barriers, yet is not associated with steep changes in vegetation and related climatic variables, and major habitat transitions are shifted from these locations by at least 18 km. This suggests that the hybrid zones are stabilized over natural dispersal barriers, independently of environmental boundaries, and are not associated with niche divergence. A striking feature of these hybrid zones is the very low levels of genetic differentiation in neutral markers between forms, suggesting that phenotypic divergence has a narrow genetic basis and may reflect recent divergence at a few linked genes under strong selection, with a possible role for assortative mating in keeping these forms apart.
(74) Ducatez Simon, Mathieu Giraudeau, Christophe Thébaud and Lisa Jacquin. Colour polymorphism is associated with lower extinction risk in birds. Global Change Biology 23, 3030-3039
Colour polymorphisms have played a major role in enhancing current understanding of how selection and demography can impact phenotypes. Because different morphs often display alternative strategies and exploit alternative ecological niches, colour polymorphism can be expected to promote adaptability to environmental changes. However, whether and how it could influence populations' and species' response to global changes remains debated. To address this question, we built an up-to-date and complete database on avian colour polymorphism based on the examination of available data from all 10,394 extant bird species. We distinguished between true polymorphism (where different genetically determined morphs co-occur in sympatry within the same population) and geographic variation (parapatric or allopatric colour variation), because these two patterns of variation are expected to have different consequences on populations' persistence. Using the IUCN red list, we then showed that polymorphic bird species are at lesser risk of extinction than nonpolymorphic ones, after controlling for a range of factors such as geographic range size, habitat breadth, life history, and phylogeny. This appears consistent with the idea that high genetic diversity and/or the existence of alternative strategies in polymorphic species promotes the ability to adaptively respond to changing environmental conditions. In contrast, polymorphic species were not less vulnerable than nonpolymorphic ones to specific drivers of extinction such as habitat alteration, direct exploitation, climate change, and invasive species. Thus, our results suggest that colour polymorphism acts as a buffer against environmental changes, although further studies are now needed to understand the underlying mechanisms. Developing accurate quantitative indices of sensitivity to specific threats is likely a key step towards a better understanding of species response to environmental changes.
(73) Vacher Jean-Pierre, Philippe Kok, Miguel Rodrigues, Jucivaldo Lima, Andy Lorenzini, Quentin Martinez, Manon Fallet, Elodie Courtois, Michel Blanc, Philippe Gaucher, Mael Dewynter, Rawien Jairam, Paul Ouboter, Christophe Thebaud, Antoine Fouquet. Cryptic diversity in Amazonian frogs: integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Aromobatidae) reveals a unique case of diversification within the Guiana Shield. Molecular Phylogenetics and Evolution 112, 158-173
Lack of resolution on species boundaries and distribution can hamper inferences in many fields of biology, notably biogeography and conservation biology. This is particularly true in megadiverse and under-surveyed regions such as Amazonia, where species richness remains vastly underestimated. Integrative approaches using a combination of phenotypic and molecular evidence have proved extremely successful in reducing knowledge gaps in species boundaries, especially in animal groups displaying high levels of cryptic diversity like amphibians. Here we combine molecular data (mitochondrial 16S rRNA and nuclear TYR, POMC, and RAG1) from 522 specimens of Anomaloglossus, a frog genus endemic to the Guiana Shield, including 16 of the 26 nominal species, with morphometrics, bioacoustics, tadpole development mode, and habitat use to evaluate species delineation in two lowlands species groups. Molecular data reveal the existence of 18 major mtDNA lineages among which only six correspond to described species. Combined with other lines of evidence, we confirm the existence of at least 12 Anomaloglossus species in the Guiana Shield lowlands. Anomaloglossus appears to be the only amphibian genus to have largely diversified within the eastern part of the Guiana Shield. Our results also reveal strikingly different phenotypic evolution among lineages. Within the A. degranvillei group, one subclade displays acoustic and morphological conservatism, while the second subclade displays less molecular divergence but clear phenotypic divergence. In the A. stepheni species group, a complex evolutionary diversification in tadpole development is observed, notably with two closely related lineages each displaying exotrophic and endotrophic tadpoles.
(72) Bourgeois Yann X. C., Boris Delahaie, Mathieu Gautier, Emeline Lhuillier, Pierre-Jean G. Malé, Joris A. M. Bertrand, Josselin Cornuault, Kazumasa Wakamatsu, Olivier Bouchez, Claire Mould, Jade Bruxaux, Hélène Holota, Borja Milá and
Christophe Thébaud. A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird. Royal Society Open Science 4:160805
Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a ‘brown’ ancestral population, the dominant ‘grey’ allele spread quickly once it arose froma new mutation. Since colour morphs are always found inmixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.
(71) Cicconardi Francesco, Paulo A. V. Borges, Dominique Strasberg, Pedro Oromí, Heriberto López, Antonio J. Pérez-Delgado, Juliane Casquet, Juli Caujapé-Castells, José María Fernández-Palacios, Christophe Thébaud, Brent C. Emerson. MtDNA metagenomics reveals large-scale invasion of belowground arthropod communities by introduced species. Molecular Ecology 26, 3104-3115
Using a series of standardised sampling plots within forest ecosystems in remote oceanic islands, we reveal fundamental differences between the structuring of aboveground and belowground arthropod biodiversity that are likely due to large-scale species introductions by humans. Species of beetle and spider were sampled almost exclusively from single islands, while soil dwelling Collembola exhibited more than tenfold higher species sharing among islands. Comparison of Collembola mitochondrial metagenomic data to a database of more than 80,000 Collembola barcode sequences revealed almost 30% of sampled island species are genetically identical, or near identical, to individuals sampled from often very distant geographic regions of the world. Patterns of mtDNA relatedness among Collembola implicate human-mediated species introductions, with minimum estimates for the proportion of introduced species on the sampled islands ranging from 45-88%. Our results call for more attention to soil mesofauna to understand the global extent and ecological consequences of species introductions.
(70) Emerson B.C., J. Casquet, H. Lopez, P. Cardoso, P.A.V. Borges, N. Mollaret, P. Oromi, D. Strasberg, & C. Thébaud. A combined field survey and molecular identification protocol for comparing forest arthropod biodiversity across spatial scales. Molecular Ecology Resources 17, 694-707
Obtaining fundamental biodiversity metrics such as alpha, beta and gamma diversity for arthropods is often complicated by a lack of prior taxonomic information and/or taxonomic expertise, which can result in unreliable morphologically based estimates. We provide a set of standardized ecological and molecular sampling protocols that can be employed by researchers whose taxonomic skills may be limited, and where there may be a lack of robust a priori information regarding the regional pool of species. These protocols combine mass sampling of arthropods, classification of samples into parataxonomic units (PUs) and selective sampling of individuals for mtDNA sequencing to infer biological species. We sampled ten lowland rainforest plots located on the volcanic oceanic island of Réunion (Mascarene archipelago) for spiders, a group with limited taxonomic and distributional data for this region. We classified adults and juveniles into PUs and then demonstrated the reconciliation of these units with presumed biological species using mtDNA sequence data, ecological data and distributional data. Because our species assignment protocol is not reliant upon prior taxonomic information, or taxonomic expertise, it minimizes the problem of the Linnean shortfall to yield diversity estimates that can be directly compared across independent studies. Field sampling can be extended to other arthropod groups and habitats by adapting our field sampling protocol accordingly.
(69) Hansen D.M, J.J. Austin, R.H. Baxter, E.J. de Boer, W. Falcón, S.J. Norder, K.F. Rijsdijk, C. Thébaud, N.J. Bunbury, & B.H. Warren. Origins of endemic island tortoises in the western Indian Ocean: A critique of the human-translocation hypothesis. Journal of Biogeography 44, 1430-1435
This paper is a reply to a paper that recently argued that giant tortoises could have been introduced to the Indian Ocean islands by early Austronesian sailors, possibly to establish provisioning stations for their journeys, just as European sailors did in more recent historical times. We present evidence from DNA phylogeny, Plio-Pleistocene ocean currents, giant tortoise dispersal, evolution of plant defences, radiocarbon dates and archaeology that indicates that the endemic giant tortoises on the Mascarenes and Seychelles colonized naturally and were not translocated there by humans.
(68) Fuchs J., D. Lemoine, J. L. Parra, J.-M. Pons, M. J. Raherilalao, R. Prys-Jones, C. Thébaud, B. H. Warren, and S. M. Goodman. Long-distance dispersal and inter-island colonization across the western Malagasy Region explain diversification in brush-warblers (Passeriformes: Nesillas). Biological Journal of the Linnean Society 119, 873-889
This study examines the colonization history and phylogeography of the brush-warblers (genus Nesillas), a genus of passerines endemic to islands of the western Indian Ocean (Madagascar, Comoros and Aldabra). The phylogeny of all recognized Nesillas taxa was reconstructed employing Bayesian phylogenetic methods and divergence times were estimated using a range of substitution rates and clock assumptions. Spatiotemporal patterns of population expansion were inferred using Spread, and niches of different lineages were compared using ecological niche modelling. Our results indicate that taxa endemic to the Comoros are paraphyletic and that the two endemic species on Madagascar (N. typica and N. lantzii) are not sister taxa. The brush-warblers started to diversify about 1.6 Myr, commencing with the separation of the clade formed by two species endemic to the Comoros (N. brevicaudata and N. mariae) from the rest of the genus. The lineages leading to the two Malagasy species diverged about 0.9 Myr; each with significantly different modern ecological niches and the subject of separate demographic processes. Patterns of diversification and endemism in Nesillas were shaped by multiple long distance dispersal events and inter-island colonization, a recurring pattern for different lineages on western Indian Ocean islands. The diversification dynamics observed for Nesillas are also consistent with the taxon cycle hypothesis.
(67) Bertrand J., B. Delahaie, Y. Bourgeois, T. Duval, R. Garcia-Jimenez, J. Cornuault, B. Pujol, C. Thébaud, B. Mila. The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird. Journal of evolutionary Biology 29, 824-836
Adaptation to local environmental conditions and the range dynamics of populations can influence evolutionary divergence along environmental gradients. Thus, it is important to investigate patterns of both phenotypic and genetic variations among populations to reveal the respective roles of these two types of factors in driving population differentiation. Here, we test for evidence of phenotypic and genetic structure across populations of a passerine bird (Zosterops borbonicus) distributed along a steep elevational gradient on the island of Reunion. Using 11 microsatellite loci screened in 401 individuals from 18 localities distributed along the gradient, we found that genetic differentiation occurred at two spatial levels: (i) between two main population groups corresponding to highland and lowland areas, respectively, and (ii) within each of these two groups. In contrast, several morphological traits varied gradually along the gradient. Comparison of neutral genetic differentiation (FST) and phenotypic differentiation (PST) showed that PST largely exceeds FST at several morphological traits, which is consistent with a role for local adaptation in driving morphological divergence along the gradient. Overall, our results revealed an area of secondary contact midway up the gradient between two major, cryptic, population groups likely diverged in allopatry. Remarkably, local adaptation has shaped phenotypic differentiation irrespective of population history, resulting in different patterns of variation along the elevational gradient. Our findings underscore the importance of understanding both historical and selective factors when
trying to explain variation along environmental gradients.
(66) Bourgeois Y., J. Bertrand, B. Delahaie, J. Cornuault, T. Duval, B. Mila, & C. Thébaud. Candidate gene analysis suggests untapped genetic complexity in melanin-based pigmentation in birds. Journal of Heredity 107, 327-335
Studies on melanin-based color variation in a context of natural selection have provided a wealth of information on the link between phenotypic and genetic variation. Here, we evaluated associations between melanic plumage patterns and genetic polymorphism in the Réunion grey white-eye (Zosterops borbonicus), a species in which mutations on MC1R do not seem to play any role in explaining melanic variation. This species exhibits five plumage color variants that can be grouped into three color forms which occupy discrete geographic regions in the lowlands of Réunion, and a fourth high-elevation form which comprises two color morphs (grey and brown) and represents a true color polymorphism. We conducted a comprehensive survey of sequence variation in 96 individuals at a series of seven candidate genes other than MC1R that have been previously shown to influence melanin-based color patterns in vertebrates, including genes that have rarely been studied in a wild bird species before: POMC, Agouti, TYR, TYRP1, DCT, Corin and SLC24A5. Of these seven genes, two (Corin and TYRP1) displayed an interesting shift in allele frequencies between lowland and highland forms and a departure from mutation-drift equilibrium consistent with balancing selection in the polymorphic highland form only. Sequence variation at Agouti, a gene frequently involved in melanin-based pigmentation patterning, was not associated with color forms or morphs. Thus, we suggest that functionally important changes in loci other than those classically studied are involved in the color polymorphism exhibited by the Réunion grey white-eye and possibly many other non-model species.
(65) Jaworski C., C. Thébaud, and J. Chave. Dynamics and persistence in a metacommunity centred on the plant Antirrhinum majus: theoretical predictions and an empirical test. Journal of Ecology 104, 456-468
Spatial processes have a major influence on the stability of species interaction networks and their resilience to environmental fluctuations. Here we combine field observations and a dynamic model to understand how spatial processes may affect a network composed of the flowering plant Antirrhinum majus, its cohort of pollinators, and a specialist seed-predator and its parasitoid.
The interactions taking place within this system were investigated by determining the fate of flowers and fruits on flowering and fruiting stems at sixteen study sites. We then used this information to estimate spatial and temporal variation in the pollination rate, parasitism rate, and hyperparasitism rate.
We found that the plants were pollinator-limited, with relatively variable fruit-to-flower ratios across sites. On almost all sites, plants were both parasitised and hyperparasitised, at a low to moderate rate.
Comparing our field observations with a tritrophic Nicholson-Bailey model, we found that empirical data are not always consistent with the conditions for local tritrophic persistence. This suggests that other mechanisms such as random disturbances and recolonisations (patch dynamics) or inter-site migration through metacommunity dynamics (source-sink dynamics) play a role in this system. Model simulations showed that dispersal could contribute to increasing tritrophic persistence in this system, and that source-sink structure, not just environmental stochasticity, may cause the observed pattern of spatial variation.
(64) Mills J., C. Teplitsky, and 59 other authors. Archiving primary data: solutions for long-term-studies. Trends in Ecology and Evolution 30, 581-589
The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehen- sion amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
(63) Vacher J.P., A. Fouquet, H. Holota & C. Thébaud. The complete mitochondrial genome of Anomaloglossus baeobatrachus (Amphibia: Anura: Aromobatidae). Mitochondrial DNA Part B, 1:1, 338-340
(62) Jaworski CC, Andalo C, Raynaud C, Simon V, Thébaud C, Chave J. 2015. The Influence of prior learning experience on pollinator choice: an experiment using bumblebees on two wild floral types of Antirrhinum majus. PLoS ONE 10(8):e0130225. doi:10.1371/journal.pone.0130225.
Understanding how pollinator behavior may influence pollen transmission across floral types is a major challenge, as pollinator decision depends on a complex range of environmental cues and prior experience. Here we report an experiment using the plant Antirrhinum majus and the bumblebee Bombus terrestris to investigate how prior learning experience may affect pollinator preferences between floral types when these are presented together. We trained naive bumblebees to forage freely on flowering individuals of either A. majus pseudomajus (magenta flowers) or A. majus striatum (yellow flowers) in a flight cage. We then used a Y-maze device to expose trained bumblebees to a dual choice between the floral types. We tested the influence of training on their choice, depending on the type of plant signals available (visual signals, olfactory signals, or both). Bumblebees had no innate preference for either subspecies. Bumblebees trained on the yellow-flowered subspecies later preferred the yellow type, even when only visual or only olfactory signals were available, and their preference was not reinforced when both signal types were available. In contrast, bumblebees trained on the magenta-flowered subspecies showed no further preference between floral types and took slightly more time to make their choice. Since pollinator constancy has been observed in wild populations of A. majus with mixed floral types, we suggest that such constancy likely relies on short-term memory rather than acquired preference through long-term memory induced by prior learning.
(61) Courchamp F., J. Dunne, Y. Le Maho, R. May, C. Thébaud & M. Hochberg. Back to fundamentals: a reply to Barot et al. Trends in Ecology and Evolution 30: 370-371
In this reply to Barot et al.'s comment on our paper "Fundamental Ecology is Fundamental", we argue that, of course, researchers can easily reconcile a search for basic understanding with a quest to solve societally relevant problems. However, we do not see why all ecologists should do so, nor why any given ecologist cannot conduct research projects that are basic science, others with additional applied objectives, and yet other projects which are purely applied. Systematically intermingling applied and fundamental ecology may be tempting but, we argue, will result in the gradual demise of fundamental ecology, and will negatively impact on ecology as a science. While not foregoing support for applied ecology, we think that a plea for renewed support for fundamental ecology is incompatible with the merger proposed by Barot et al. who insist that science should be co-designed with stakeholders at multiple levels. We argue that the basis of fundamental ecology is understanding. It must remain, be protected, and be promoted as an end unto itself.
(60) Besnard G., J. Bertand, B. Delahaie, Y. Bourgeois, E. Lhuillier, and C. Thébaud. Valuing museum specimens: high-throughput DNA sequencing using historical collections of New Guinea crowned pigeons (Goura). Biological Journal of the Linnean Society 117, 71-82
Museum specimens are of particular importance for investigating systematics and the biogeography as well as other aspects of the evolution of biodiversity. They are also a depository of specimens accumulated over recent historical times and often the only way to study recently extinct or rare species. Unfortunately, most museum specimens yield low-quality DNA limiting their generalized use in phylogenetic and population genetic studies. Advances in sequencing technologies now offer opportunities to analyse such material even from very small tissue. Here, we applied the Illumina technology (HiSeq) on three specimens of crowned pigeon (Goura spp.) collected in New Guinea between 1879 and 1934. A shotgun strategy allowed us to quickly and reliably assemble complete mitochondrial genomes and fragments of three single-copy gene phylogenetic markers even with low double- stranded DNA quantity (9 to 69 ng). Phylogenetic assignments of these new sequences confirmed them as Goura sequences. Therefore, our study confirms the power of using next-generation sequencing methods to investigate the evolutionary history of species for which access to fresh samples is limited but museum collections are available. These approaches are considerably increasing the value of many natural history collections for genetic investigations, particularly from biodiversity hotspots that are presently difficult to prospect.
(59) Bertrand J., Y. Bourgeois, & C. Thébaud. Population density of the Réunion Grey White-eye (Zosterops borbonicus) within the summit ecosystems of Réunion (Mascarene Islands). Ostrich 87, 85-88
Assessing population density is crucial for studying ecology and evolutionary biology of species as well as for conservation purposes. Here we used point count methods to infer population density in a single-island endemic passerine bird, the Réunion Grey White-eye (Zosterops borbonicus), that displays striking evidence of differentiation at a small spatial scale.. Population density was estimated at 5.17 birds per hectare (CL: 4.85-5.50), a value somewhat higher than previously believed. This estimation provides the first detailed estimation of bird population density in the vulnerable summit ecosystems of Réunion and will possibly allow a better understanding of the evolutionary causes of this plumage colour variation.
(58) Warren B.H., 22 other authors, & C. Thébaud. Islands as model systems in ecology and evolution: progress and prospects fifty years after MacArthur-Wilson. Ecology Letters 18: 200-217
The study of islands as model systems has played an important role in the development of evolutionary and ecological theory. The 50th anniversary of MacArthur and Wilson’s (December 1963) article, “An equilibrium theory of insular zoogeography”, was a recent milestone for this theme. Since 1963, island systems have provided new insights into the formation of ecological communities. Here, building on such developments, we highlight prospects for research on islands to improve our understanding of the ecology and evolution of communities in general. Throughout, we emphasise how attributes of islands combine to provide unusual research opportunities, the implications of which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-assessment of some fundamental issues that interested MacArthur and Wilson. These include the formation of ecological networks, species abundance distributions, and the contribution of evolution to community assembly. We also extend our prospects to other fields of ecology and evolution – understanding ecosystem functioning, speciation, and diversification – frequently employing assets of oceanic islands in inferring the geographic area within which evolution has occurred, and potential barriers to gene flow. Although island-based theory is continually being enriched, incorporating non-equilibrium dynamics is identified as a major challenge for the future.
(57) Courchamp F., J. Dunne, Y. Le Maho, R. May, C. Thébaud, & M. Hochberg. Fundamental ecology is fundamental. Trends in Ecology and Evolution 30: 9-16
The primary reasons for conducting fundamental research are satisfying curiosity, acquiring knowledge, and achieving understanding.%