Abstract
The presence of congeneric taxa on the same island suggests the possibility of in situ divergence, but can also result from multiple colonizations of previously 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.
Keywords: speciation, population differentiation, geographical isolation, niche evolution, island, Zosterops
1. Introduction
Closely related endemic taxa co-occurring in small isolated areas, such as remote oceanic islands or archipelagos, have long fascinated naturalists (e.g. [1,2]) and have been of central importance in helping us understand how species form [3–7]. However, the origin of this biogeographic pattern must be interpreted cautiously as it can be produced by different processes, including multiple independent colonization events from different source populations, repeated colonizations from the same ancestral source population or within-island diversification after colonization by an ancestral stock [3,8,9]. Being able to discriminate among these processes is a prerequisite for revealing the geographical and selective contexts underlying population divergence, and is ultimately critical for understanding the factors promoting or preventing evolutionary radiations [3,4,6,10–12].
Phylogenetic analyses have frequently been used to test the hypothesis of within-island diversification by assessing sister relationships between co-occurring single-island endemic populations or species [6,13,14]. When sister relationships recovered in phylogenetic trees can be shown not to be an artefact of gene flow, and if the age of the island clade (stem node) falls within the age of the island, it has typically been concluded that an evolutionary radiation has taken place on that island (e.g. [15]). This ‘monophyly’ test is needed to infer within-island diversification and to reject multiple colonizations that would otherwise result in topologies in which same-island species are not sister species [16,17].
However, decisions based solely on phylogenetic support need to be interpreted with caution, as phylogenetic topologies are sometimes unable to discriminate among alternative biogeographic hypotheses and are sensitive to incomplete sampling [18–22]. For example, monophyly can be recovered even in the case of multiple colonizations if sister lineages from the source areas went extinct or were not sampled due to insufficient geographical sampling. In addition, phylogenetic analyses have often relied upon evaluating speciation events in genera with more than one species on a particular island, assuming that all named species are composed of monophyletic groups of populations, thus over-relying on existing taxonomic statements and largely ignoring the possibility of complex demographic histories, including the history of gene flow between the diverging entities [18,23,24]. Therefore, coupling population genomics and phylogenetic inference based on genomic data from appropriate population sampling strategies seems the best option to address longstanding questions about colonization history and in situ diversification, and for understanding how biogeographic and ecological factors drive the differentiation of populations to the level of species.
Here, we study the population genetic history of a bird species complex, the Reunion grey white-eye (Zosterops borbonicus; taxonomy following Gill & Donsker [25]) to test the hypothesis of within-island diversification. White-eyes (Zosteropidae) stand out as a lineage in which diversification rates have been exceptionally high, and with nearly half of the world's forms being single-island endemics, they appear to respond rapidly to the geographical drivers of speciation [26–28]. A number of islands are occupied by more than one recognized species, but the presence of multiple species on a single island has been attributed to multiple colonizations in all cases [6,29–32]. Uniquely among white-eyes, and even among birds in general, the Reunion grey white-eye displays geographical variation in morphological and plumage colour traits within the small and remote volcanic oceanic island of Reunion (2512 km2) [33]. This pattern of variation has long been considered a case of within-species variation with little relevance to within-island population divergence and speciation (see e.g. [6]). Recent studies, however, have shown that the Reunion grey white-eye consists of four distinct adjacent and non-overlapping geographical forms that exhibit discrete differences in morphology and plumage (electronic supplementary material, text S1) and form extremely narrow hybrid zones where they meet [33–37]. Three of the geographical forms are found in the lowlands, primarily below 1400 m, with contact zones coinciding with natural physical barriers, such as large rivers or lava flows, that are not associated with changes in environmental conditions [36]. They differ strikingly in plumage colour, with a brown-headed brown form (LBHB for lowland brown-headed brown) with a light brown back and head, a grey-headed brown form (GHB) with a brown back and a grey head, and a brown-naped brown form (BNB) with a brown back and nape and a grey crown (electronic supplementary material, figure S1; figure 1a). A fourth form (HIGH), found in the highlands between 1400 and 3000 m, is slightly larger than the lowland forms (electronic supplementary material, text S1) and comprises two very distinct colour morphs, with birds showing predominantly grey or brown plumage, respectively [33,34,38,39]. This highland form occupies a distinct elevational and ecological zone [40,41], suggesting that it may have experienced very different selection pressures during its evolutionary history. This may explain at least partly why it is phenotypically and genetically different from the lowland forms [37,38,42]. Such disparity could have arisen as a result of the ecological and evolutionary expansion of a lineage to exploit new resource types, providing a possible case of adaptive divergence structured by elevation. Alternatively, differences between highland and lowland forms could reflect divergence prior to colonization by distinct lineages adapted to different environments. In spite of Reunion being very small relative to other islands where within-island diversification has been documented in bird lineages [43,44], current data suggest that in situ diversification is more likely than multiple immigration events to explain geographical variation in the Reunion grey white-eye, since highland and lowland forms appear to be monophyletic with regards to their closest relative, the Mauritius grey white-eye (Z. mauritianus) [27,38]. However, these conclusions are based solely on the analyses of mitochondrial and amplified fragment length polymorphism data and rely on partial population sampling, leaving open the possibility of more complex colonization and diversification scenarios.
Figure 1.
(a) Distribution ranges of the four geographical forms of the Reunion grey white-eye (black lines), with corresponding phenotypes (LBHB: lowland brown-headed brown form; GHB: grey-headed brown form; BNB: brown-naped brown form; HIGH: highland form). Points correspond to sampling localities, labelled by numbers (electronic supplementary material, table S1) and coloured according to forms. Localities with a black stripe are within contact zones (see Material and methods for contact zone definition), and corresponding contact zones are labelled with roman numerals (electronic supplementary material, table S1). Grey colours represent elevation classes: light grey = elevation below 1000 m; medium grey = elevation between 1000 and 2000 m; dark grey = elevation above 2000 m. (b) Principal components analysis of the 45 948 SNPs for Reunion grey white-eye only, with colours corresponding to geographical forms as in figure 1a. Lowland forms are LBHB, GHB and BNB, and the highland form (HIGH) has been split into HIGH-North, which corresponds to the Piton des Neiges mountain in the north of the HIGH form distribution, and HIGH-South, which corresponds to the Piton de la Fournaise volcano in the south of the HIGH form distribution. Individuals in contact zones are in grey, with contact zones labelled as in figure 1a. (Online version in colour.)
In this study, we used genome-wide analyses based on genotyping-by-sequencing (hereafter GBS) of 410 individuals representing all Reunion grey white-eye geographical forms and three closely related species, including the Mauritius grey white-eye. This enabled us to capture the pattern of lineage divergence and to investigate how biogeographic population history and ecological opportunities may explain relationships among these entities.
2. Material and methods
(a). Population sampling and DNA sequence data
Blood samples from a total of 410 individuals, captured in mistnets and then released, were collected between 2007 and 2017 (figure 1a; electronic supplementary material, table S1). These include all forms of the Reunion grey white-eye sampled across their entire range (347 individuals), the Mauritius grey white-eye, and two other closely related Zosterops species, the Reunion olive white-eye (Z. olivaceus) and the Orange River white-eye (Z. pallidus), used as outgroups. Details on sampling and choice of outgroups are presented in the electronic supplementary material, text S2 and table S2. Approximately 1 µg of high-quality DNA was extracted using a QIAGEN DNeasy Blood & Tissue kit following the manufacturer's instructions, with an extra pre-digestion grinding step. Genomic DNA extractions from 275 individuals (sequencing run 1) were sent to the BRC Genomic Diversity Facility at Cornell University [45] and an additional set of extracts from 137 individuals (sequencing run 2) was sent to the Elshire Group Ltd, for GBS sequencing with Pst1 restriction enzyme and single-end HiSeq 2500 sequencing or paired-end HiSeq X Ten sequencing, respectively (see electronic supplementary material, table S3 for details on the species composition of each sequencing run). Two randomly chosen individuals from the first run were re-extracted and re-sequenced with the second run to control for reproducibility between runs and facilitate data merging (electronic supplementary material, text S3).
(b). Reference-based GBS data processing
For Reunion grey white-eye GBS data, single nucleotide polymorphism (SNP) calling was performed as follows. Sequencing reads were first mapped against a high-quality genome assembly with a scaffold N50 exceeding one megabase [28] using the bwa-mem algorithm v. 0.7.15 [46] with default parameters. SNPs were then called using GATK v. 3.7 [47] using base quality score recalibration and indel realignment. Various SNP filters were subsequently applied (electronic supplementary material, text S2), keeping the number of genotypic differences between the two control individuals that were present in both datasets as low as possible (electronic supplementary material, text S3).
The coordinates of this SNP dataset were used to extract homologous positions from sequences from outgroup taxa. Data processing and filtering resulted in a concatenated matrix of 45 948 SNP loci for 316 Reunion grey white-eyes and 56 outgroup individuals. Details on the SNP dataset characteristics (mean depth, proportion of missing data) can be found in electronic supplementary material, text S2.
(c). Population structure analyses
In order to characterize the extent of genotypic partitioning and to assess the relative levels of divergence among Reunion grey white-eye geographical forms, we used our full dataset to perform a principal components analysis (PCA) with PLINK v. 1.90b5.3 [48] and plotted the results in R v. 3.5 [49] with adegenet v. 2.1.1 [50]. We then evaluated genetic diversity within- and between-forms by computing mean observed (Ho) and expected (He) heterozygosities [51] for each form (electronic supplementary material, table S4) and FST values [52] in 50 kbp windows between all pairs of forms and also between Reunion and Mauritius grey white-eyes using VCFtools v. 0.1.15 [53] applied to a reduced dataset (see section on phylogenetic analyses hereafter).
We used ADMIXTURE 1.3 [54], a model-based clustering algorithm, to infer the levels of shared ancestry between individuals and to assess the levels of hierarchical population structure that could have arisen through divergence. SNPs were converted into the requested input with PLINK (–recode12 option) and we ran 20 independent simulations for each value of K (from two to eight), considering that convergence had been reached when the log-likelihood between two iterations had dropped below 1 × 10−4 (default parameter). Results from the best simulation (best likelihood value) for each value of K were then plotted using R. As all individuals from a location shared similar patterns of admixture composition (electronic supplementary material, figure S2), mean admixture coefficients per locality were calculated in order to display spatial patterns of admixture. A cross-validation procedure was followed to determine the best value of K (electronic supplementary material, figure S3).
(d). Phylogenetic analyses
Our aim was to obtain a robust phylogenetic hypothesis for Reunion grey white-eye geographical forms. To minimize the impact that recent gene flow could have on our tree estimate [55], we built a reduced dataset in which we only kept individuals from localities that were sufficiently distant from the zones of contact between forms where gene flow and the occurrence of hybrid individuals, if any, were expected to be more likely (as revealed by PCA and admixture results; figure 1b and electronic supplementary material, figure S4). For that purpose, contact zones were defined according to results from previous cline studies [36,42]: for lowland forms, we excluded sampling localities within 3 km on either side of the contact zone between two forms; and for the highlands/lowlands contact zone, we excluded sampling localities located between 1200 and 1600 m elevation (electronic supplementary material, table S1). Thus, we kept in our reduced dataset a total of 25 out of 41 localities, including 177 individuals.
We first performed maximum likelihood phylogenetic analyses using IQ-TREE v. 1.6.7 [56] on this concatenated reduced dataset with a correction accounting for SNP data ascertainment bias (ascertainment bias correction, parameter—ASC) [57]. We used the TIM + F + ASC + R5 model of nucleotide substitution, since this model of sequence evolution was selected as the best fit for our data by ModelFinder [58]. We used Z. pallidus, Z. olivaceus and Z. mauritianus individuals as outgroups and performed ultrafast bootstrapping (1000 replicates) [59]. The resulting consensus tree was plotted in R using the package ape v. 5.3 [60]. We also ran IQ-TREE after excluding SNPs that were potentially under selection since this could affect phylogenetic reconstruction. Such SNPs were identified using BayeScan v. 2.1 [61], which uses differences in allelic frequencies between populations (here the geographical forms) to identify candidate loci under natural selection. Outliers were identified setting the prior odds for the neutral model to 1000 and using a false discovery rate of 0.00011 (electronic supplementary material, figure S5). We used the TIM + F + ASC + R5 model of nucleotide substitution since this model was again selected as the best fit for our data by ModelFinder.
To account for uncertainties that may result from incomplete lineage sorting in concatenated datasets, we also conducted a phylogenetic analysis under the multispecies coalescent model, as implemented in SVDquartets [62] (available in PAUP v. 4a166). In an attempt to meet the assumption of unlinked markers, as recommended by Chifman & Kubatko [62], SNPs in our reduced dataset were thinned based on their physical position so that two markers were not closer than 10 kbp, resulting in 22 073 SNP loci. We ran SVDquartets grouping individuals per locality and per form and sampling 5 000 000 quartets with 100 standard bootstraps.
Finally, using TreeMix v. 1.13 [63] with the same dataset and Z. mauritianus as the outgroup, we inferred the population tree of Z. borbonicus and tested for the presence of gene flow over the course of population divergence by adding up to five migration events between geographical forms. Since the proportion of variance explained for the population tree without migration event was extremely high (99.95%; see electronic supplementary material, figure S6), with very little improvement by sequentially adding migration events, we only present and discuss the population tree obtained without adding migration. While this approach is not primarily aimed at inferring phylogenetic relationships, it provides a useful framework to reconstruct historical branching events from large amounts of population genomic data [63,64].
(e). Genetic divergence and within-island geography
To assess the extent to which the different forms correspond to independently evolving lineages in the face of gene flow, we calculated estimated effective migration surfaces (EEMS) between populations, by assessing population structure from geo-referenced genetic samples and visualizing areas of lower-than-average gene flow, i.e. putative barriers to gene flow [65]. Using the full dataset, we calculated pairwise genetic dissimilarities (number of allelic differences between each pair of individuals across all loci) with the bed2diffs_v2 function, which replaces missing genotypes with the observed average genotype. We then used a population grid of 700 identical demes and ran the MCMC program for 2 million iterations, with a burn-in of 1 million and thinning 9999 iterations between two writing steps (default values). The convergence of the chain was confirmed by visual inspection of the likelihood trace.
3. Results
A genome-wide PCA analysis revealed that the different grey white-eye geographical forms represent clearly distinct genetic clusters (figure 1b). Some individuals sampled from narrow contact zones between lowland and highland forms fell between these clusters, as would be expected if their genetic characteristics were intermediate due to hybridization between forms. Strikingly, individuals also clustered by sampling locality in some cases (electronic supplementary material, figure S7), indicating a very fine geographical substructure, and this is well exemplified by the two clusters that separate individuals from northern and southern localities within the range of the highland form (figure 1b). The results of the clustering analysis using ADMIXTURE were in close agreement with the PCA results (electronic supplementary material, figure S4), with a lowland/highland separation (K = 2), an additional separation between LBHB and the two other lowland forms (K = 3), evidence for substructure within the GHB form (K = 4) following a north–south trend with the southernmost localities being distinguished from other, more northerly localities, and a separation between northern and southern localities within the range of the highland form (K = 5; electronic supplementary material, figure S8). Admixed individuals, defined as individuals with an admixture coefficient (1 − max(admixture)) greater than 0.3, were located predominantly in the contact zones, especially between lowland and highland forms (electronic supplementary material, figure S9). For K = 2, this represented 78% of all individuals found in the contact zones (n = 98). A notable exception was found in the BNB form where most sampled localities included a majority of admixed individuals, especially for K values greater than 3. Differences in the genetic composition of admixed individuals across BNB localities follow a spatial trend, with contributions from other forms being highest as sampling locations approach contact zones. This suggests directional introgression from LBHB, GHB and possibly HIGH forms into the BNB form, which appears to have been asymmetrically introgressed beyond the contact zones rather than being a genetic mixture of two or more parental lineages. Mean FST values indicate that lowland and highland forms are more differentiated than lowland forms are between themselves, which is consistent with both our PCA analysis (first axis separating lowland and highland forms) and the first hierarchical level of structure (K = 2) found by ADMIXTURE. All mean values are low and within the same order of magnitude, ranging from 0.01 to 0.05 (electronic supplementary material, figure S10), as would be expected if the different forms shared a recent and common origin.
The maximum likelihood phylogenetic tree using the neutral reduced dataset (excluding 155 outlier SNPs likely to be under selection) confirmed the monophyly of Z. borbonicus, and its sister relationship to Z. mauritianus (figure 2a). It also revealed strong phylogenetic structure between the different geographical forms, with two forms (LBHB and HIGH) being monophyletic (bootstrap = 99 and 100%, respectively) and nested within the BNB form, which is itself nested within the GHB form. This resolved and well-supported topology appears to be robust since it was also retrieved with TreeMix (figure 2b), SVDquartets analyses (electronic supplementary material, figure S11), as well as in a separate maximum likelihood analysis in which we included outlier loci (electronic supplementary material, figure S12). It is noteworthy that none of the geographical forms were recovered as polyphyletic, suggesting that they represent distinct groups, in spite of gene flow at their contact zones. The GHB form, currently restricted to the northern part of the island, contains deeply divergent lineages forming together a paraphyletic grade relative to other forms. The most parsimonious explanation for this pattern is that this form corresponds to the descendants of an ancestral founding stock from which the ancestors of the other three forms split off and further diverged. The precise branching order of these more recently evolved forms cannot be easily inferred since the paraphyly of the BNB form relative to LBHB and HIGH forms could reflect conflicting signals in this part of the tree owing to past or ongoing introgression. However, whatever the exact scenario, our results suggest that dispersal events into previously unoccupied areas occurred repeatedly, first across the lowlands, and then up a very steep elevational gradient into the highlands.
Figure 2.
(a) Maximum likelihood phylogenetic tree for Reunion grey white-eyes based on neutral SNP loci (excluding the 155 candidate loci under natural selection identified in BayeScan). Zosterops mauritianus, Z. olivaceus and Z. pallidus were used as outgroups (only Z. mauritianus shown, brown bar). Each tip of the tree corresponds to an individual, labelled by its locality number (electronic supplementary material, table S1), with colours corresponding to geographical forms as in figure 1a. Asterisks (*) indicate bootstrap values greater than or equal to 95%; otherwise, actual values are indicated if greater than or equal to 70%. (b) Historical relationships of Reunion grey white-eye forms as inferred using TreeMix assuming only the effects of drift (i.e. without migration events) and grouping individuals by form. The outgroup is Z. mauritianus (MAU). (Online version in colour.)
Results of the EEMS analysis using the entire dataset suggest that contact zones between all forms might be associated with barriers to migration, but the pattern is low to moderate except for the contact zone between the HIGH form and the lowland forms, including the BNB form with which we detected introgression, where strong migration barriers are also inferred (electronic supplementary material, figure S13).
4. Discussion
Our phylogenetic analyses show that the Reunion grey white-eye is a distinct monophyletic lineage that has diversified into four distinct independent lineages within the small island of Reunion. The clear reciprocal monophyly with respect to the Mauritius grey white-eye suggests that divergence took place according to the classic model of allopatric speciation, as is usually expected when islands occupied by diverging populations are far apart relative to an organism's capacity to disperse over water [3,29]. Reunion and Mauritius are 170 km apart; both islands emerged from the ocean floor at a depth of 4.5–5 km, and were, therefore, never connected to each other [66]. While we did not specifically estimate migration rates, our phylogenetic data and previous work [67] suggest that gene flow between Reunion and Mauritius grey white-eyes is absent or very low and, if any, has clearly not prevented population divergence (FST estimate of 0.18) (electronic supplementary material, figure S10; see also [37,38]). Our results also indicate that geographical differentiation has not been followed by secondary colonizations between islands, highlighting the role of inter-island colonization in the global diversification of white-eyes [26] and, more generally, the build-up of species diversity on oceanic archipelagos [11,68]. A previous study [27] provided an estimate of 0.4–0.5 Myr for the divergence time between Mauritius and Reunion grey white-eyes, so splitting time lies well within the time frame during which Reunion has been available for dispersal and colonization by birds (at least 2.1 Myr; [69]).
These results are consistent with the diversification of a single ancestral stock into several geographical forms of grey white-eyes on Reunion, but they are per se not sufficient to rule out alternative hypotheses (see e.g. [70]). Repeated colonizations followed by the extinction of a related species in a source area may have left the descendants as sister lineages forming a monophyletic group. Given that Mauritius and Reunion grey white-eyes have achieved reciprocal monophyly, such independent colonizations would need to have happened in rapid succession. This would thus be equivalent to several diverging populations, including the Mauritius grey white-eye lineage, arising simultaneously from a common ancestor. However, we found that one of the lowland forms (GHB) is paraphyletic relative to all other forms, with deep sequential splits between populations occupying different parts within the range of this form. In addition, our results revealed a western–eastern trend, with older GHB lineages mapping to the northwest and younger lineages mapping to the southwest of the island. While paraphyly may also denote sequential colonization from a now-extinct common ancestor from outside the island, phylogeographic concordance between lineage age and geography within GHB is more consistent with an early colonization of Reunion by GHB ancestors with subsequent eastward range expansion across the island accompanied by successive bouts of differentiation.
Results from population genomic analyses, while largely consistent with those obtained with phylogenetic analyses, further showed that the population genetic structure of the different forms is strongly correlated with their geographical ranges. We also found that contact zones between forms correspond to regions of low effective migration (sensu [65]), which is to be expected given their congruence with features that could reduce gene flow between forms, namely the ecotone between highland and lowland habitats separating locally adapted forms, and natural physical barriers between lowland forms that have diverged in secondary sexual traits, possibly through pre-mating isolation mediated by female choice [36,37,42]. This implies that each form constitutes its own entity, has evolved in geographical isolation for some period of time, and must be currently kept apart from others by some form of reproductive isolation in spite of recent or ongoing gene flow (see also [37]). Combined with phylogenetic data, this provides strong support for the hypothesis that a single ancestral stock colonized the island. Since Reunion is a volcanic complex that appears to have always been a single landmass [71], with little effect of Pleistocene sea-level fluctuations on its area (less than 20%) and spatial arrangement [72], our analyses further show that it is divergence within a single island that led to the different and distinct geographical forms of Reunion grey white-eyes we observe today.
We found the highland form to be of recent origin relative to the history of the complex, as revealed by the branching order in phylogenetic inferences. This is consistent with a recent expansion into the highlands from lowland ancestors. Those birds that colonized the highlands evolved into a larger form that is essentially restricted to dense cloud forests and subalpine scrubland [33,38,42], where environmental conditions are dramatically different from those experienced by lowland birds (electronic supplementary material, text S4). While the presence of a hybrid zone where the highland and lowland forms meet [42] already provided support for a model of allopatric divergence between these forms, recent demographic analyses have confirmed the role of geographical isolation by demonstrating that the patterns of gene flow between highland and lowland forms result from a recent secondary contact at mid-elevation after up to 100 000 years of divergence in isolation [37].
Geographical separation seems to have been key in promoting divergence between Reunion grey white-eye forms. In addition, the substantial morphological and ecological differences between the highland and lowland forms (electronic supplementary material, text S1), combined with their population history, highlight the potential significance of niche shifts in the diversification of this group, after it colonized the island. Indeed, recent results indicate that geographical separation combined with habitat change has led to extensive genomic differentiation between highland and lowland forms (see [37]), which could result in stronger reproductive isolation between highland and lowland forms than between lowland forms, but further analyses would be required to confirm this hypothesis.
It has been proposed that highly diverse lineages that are found across many islands may have expanded their geographical ranges and colonized new islands during evolutionary phases of high dispersal ability, and then differentiated and speciated during a subsequent phase of reduced dispersal ability [73,74]. This appears to apply to white-eyes (Zosterops) which have among the highest dispersal capabilities among birds, having colonized more islands globally than any other passerine group. Yet, the distance over water appears to pose an important barrier in Zosterops once they have colonized a small island, even when the distance to the next island is as reduced as a few kilometres [29]. Evolutionary shifts in dispersal ability have been suggested as a key driver of inter-island diversification in white-eyes [26]. However, such shifts in dispersal ability, if any, have had little consequence on intra-island processes in all Zosterops except the Reunion grey white-eye. In fact, across all islands currently occupied by more than one Zosterops species, separate colonizations can be easily invoked (see e.g. [29–32]). This suggests that in most species, low dispersal ability mainly corresponds to low ‘over-water’ dispersal.
Previous findings support the idea that the Reunion grey white-eye shows an extremely reduced propensity to disperse ‘over-land’ within Reunion, which likely relates to behavioural processes since the birds show no sign of wing reduction or flight ability [35]. The very fine population substructure found in this study (electronic supplementary material, figure S7) is in agreement with extremely low effective dispersal. We suggest that the evolution of low dispersal ability in the Reunion grey white-eye, combined with periods of geographical isolation, ecological opportunity and sexual selection, could have been key in explaining why this lineage has diversified within such a small island, well below the minimum spatial scale considered suitable for divergence in highly mobile organisms like birds [44]. There is currently no other convincing evidence of intra-island speciation, including incipient speciation, on islands smaller than 10 000 km2 [75], and, more generally, little evidence on islands smaller than Madagascar (600 000 km2) [6,29,76,77]. Recent studies have shown that more variation exists among the different geographical forms of the Reunion grey white-eye than would be expected under drift for both morphological and plumage colour traits [34,42]. Thus, while geographical isolation may have promoted evolutionary divergence between all forms, sexual selection also appears to have played a major role in the establishment of reproductive isolation [37]. Range expansion followed by range splitting or dispersal across the elevational gradient that led to the formation of the highland form seems to have been key in promoting ecological diversification within the lineage, with divergent selection pressures causing at least adaptive divergence and possibly also contributing to reproductive isolation [37,42,78]. Our study highlights the importance of both historical and ecological factors in explaining the geographical distribution of close allies on a small island, and reveals that the combination of strong selection and low dispersal can drive population divergence and incipient speciation even at very small geographical scales, furthering our understanding of the origin of diversity in remote oceanic islands and beyond.
Supplementary Material
Acknowledgements
We thank Thomas Duval, Jennifer Devillechabrolle, Guillaume Gélinaud, Marie Manceau, Juli Broggi, Josselin Cornuault, Yann Bourgeois, Joris Bertrand, Boris Delahaie, Dominique Strasberg, Philipp Heeb, René-Claude Billot, Ben Warren and Jean-Michel Probst for their assistance in the field in Reunion and Mauritius; Hélène Holota and Amaya Iribar-Pelozuelo for help with the laboratory work; Reunion National Park and Mauritius National Parks and Conservation Service for granting us permission to conduct fieldwork in protected areas of Reunion and Mauritius, respectively; Benoit Lequette (Reunion National Park) and Vikash Tatayah (Mauritius Wildlife Foundation) for facilitating collecting permits; the provincial authorities in the Free State (South Africa) for granting us permission to collect samples and specimens (permit 01-24158) and Dawie de Swardt (National Museum Bloemfontein) and Jérome Fuchs (MNHN, Paris) for help with organizing fieldwork on African white-eyes. We thank two anonymous reviewers and the Associate Editor for their comments.
Ethics
All manipulations on birds were conducted under a research permit issued by the Centre de Recherches sur la Biologie des Populations d'Oiseaux (CRBPO), Muséum National d'Histoire Naturelle (Paris).
Data accessibility
The full SNP dataset used in the study is available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.4f4qrfj7t [79].
Authors' contributions
B.M. and C.T. initiated and coordinated the project. M.G., B.N., B.M. and C.T. conceived the study and designed the experiments. B.M. and C.T. conducted the fieldwork, with the assistance of M.G., B.N. and T.L. M.G. performed the analyses. M.G., B.N., T.L., B.M. and C.T. interpreted the analyses and wrote the manuscript.
Competing interests
We declare we have no competing interests.
Funding
This work was supported by the Fonds Inkerman, the Agence Française pour le Développement, the National Geographic Society, the Fondation pour la Recherche sur la Biodiversité, the ‘Laboratoire d'Excellence’ TULIP (ANR-10-LABX-41), ANR grant (BirdIslandGenomic project, ANR-14-CE02-0002) to B.N., and a PhD studentship from the Ministère de l'Enseignement Supérieur et de la Recherche to M.G. Logistic support on Reunion was provided by the Marelongue field station run by the University of Reunion and the Observatoire des Sciences de l'Univers de La Réunion.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Citations
- Gabrielli M, Nabholz B, Leroy T, Milá B, Thébaud C.2020. Data from: Within-island diversification in a passerine bird. Dryad Digital Repository. ( ) [DOI] [PMC free article] [PubMed]
Supplementary Materials
Data Availability Statement
The full SNP dataset used in the study is available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.4f4qrfj7t [79].