Face Of Gene Flow Research Articles

Divergent Selection in Low Recombination Regions Shapes the Genomic Islands in Two Incipient Shorebird Species.

Speciation in the face of gene flow is usually associated with a heterogeneous genomic landscape of divergence in nascent species pairs. However, multiple factors, such as divergent selection and local recombination rate variation, can influence the formation of these genomic islands. Examination of the genomic landscapes of species pairs that are still in the early stages of speciation provides an insight into this conundrum. In this study, population genomic analyses were undertaken using a wide range of sampling and whole-genome resequencing data from 96 unrelated individuals of Kentish plover (Charadrius alexandrinus) and white-faced plover (Charadrius dealbatus). We suggest that the two species exhibit varying levels of population admixture along the Chinese coast and on the Taiwan Island. Genome-wide analyses for introgression indicate that ancient introgression had occurred in Taiwan population, and gene flow is still ongoing in mainland coastal populations. Furthermore, we identified a few genomic regions with significant levels of interspecific differentiation and local recombination suppression, which contain several genes potentially associated with disease resistance, coloration, and regulation of plumage molting and thus may be relevant to the phenotypic and ecological divergence of the two nascent species. Overall, our findings suggest that divergent selection in low recombination regions may be a main force in shaping the genomic islands in two incipient shorebird species.

Gene Flow and Isolation in the Arid Nearctic Revealed by Genomic Analyses of Desert Spiny Lizards.

The opposing forces of gene flow and isolation are two major processes shaping genetic diversity. Understanding how these vary across space and time is necessary to identify the environmental features that promote diversification. The detection of considerable geographic structure in taxa from the arid Nearctic has prompted research into the drivers of isolation in the region. Several geographic features have been proposed as barriers to gene flow, including the Colorado River, Western Continental Divide (WCD), and a hypothetical Mid-Peninsular Seaway in Baja California. However, recent studies suggest that the role of barriers in genetic differentiation may have been overestimated when compared to other mechanisms of divergence. In this study, we infer historical and spatial patterns of connectivity and isolation in Desert Spiny Lizards (Sceloporus magister) and Baja Spiny Lizards (Sceloporus zosteromus), which together form a species complex composed of parapatric lineages with wide distributions in arid western North America. Our analyses incorporate mitochondrial sequences, genomic-scale data, and past and present climatic data to evaluate the nature and strength of barriers to gene flow in the region. Our approach relies on estimates of migration under the multispecies coalescent to understand the history of lineage divergence in the face of gene flow. Results show that the S. magister complex is geographically structured, but we also detect instances of gene flow. The WCD is a strong barrier to gene flow, while the Colorado River is more permeable. Analyses yield conflicting results for the catalyst of differentiation of peninsular lineages in S. zosteromus. Our study shows how large-scale genomic data for thoroughly sampled species can shed new light on biogeography. Furthermore, our approach highlights the need for the combined analysis of multiple sources of evidence to adequately characterize the drivers of divergence.

Habitat-associated genomic variation in a wall lizard from an oceanic island.

The lizard Teira dugesii exhibits morphological divergence between beach and inland habitats in the face of gene flow, within the volcanic island of Madeira, Portugal. Here, we analysed genomic data obtained by genotyping-by-sequencing, which provided 16378 SNPs from 94 individuals sampled from 15 sites across Madeira. Ancient within-island divergence in allopatry appears to have mediated divergence in similar species within other Atlantic islands but this hypothesis was not supported for T. dugesii. Across all samples, a total of 168 SNPs were classified as statistical outliers using pcadapt and OutFLANK. Redundancy analysis revealed that 17 of these outliers were associated with beach/inland habitats. The SNPs were located within 16 sequence tags and 15 of these were homologous with sequences in a 31Mb region on chromosome three of a reference wall lizard genome (the remaining tag could not be associated with any chromosome). We further-investigated outliers through contingency analyses of allele frequencies at each of four pairs of adjacent beach-inland sites. The majority of the outliers detected by the redundancy analysis were confirmed at two pairs of these matched sites. These analyses also suggested some parallel divergence at different localities. Six other outliers were associated with site elevation, four of which were located on chromosome five of the reference genome. Our study lends supports to a previous hypothesis that divergent selection between grey shingle beaches and inland regions overcomes gene flow and leads to the observed morphological divergence between populations in these adjacent habitats.

Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale

BackgroundThe factors that maintain phenotypic and genetic variation within a population have received long-term attention in evolutionary biology. Here the genetic basis and evolution of the geographically widespread variation in twig trichome color (from red to white) in a shrub Melastoma normale was investigated using Pool-seq and evolutionary analyses.ResultsThe results show that the twig trichome coloration is under selection in different light environments and that a 6-kb region containing an R2R3 MYB transcription factor gene is the major region of divergence between the extreme red and white morphs. This gene has two highly divergent groups of alleles, one of which likely originated from introgression from another species in this genus and has risen to high frequency (> 0.6) within each of the three populations under investigation. In contrast, polymorphisms in other regions of the genome show no sign of differentiation between the two morphs, suggesting that genomic patterns of diversity have been shaped by homogenizing gene flow. Population genetics analysis reveals signals of balancing selection acting on this gene, and it is suggested that spatially varying selection is the most likely mechanism of balancing selection in this case.ConclusionsThis study demonstrate that polymorphisms on a single transcription factor gene largely confer the twig trichome color variation in M. normale, while also explaining how adaptive divergence can occur and be maintained in the face of gene flow.

Digest: Complex dynamics of speciation and implications for macroevolutionary models.

What kinds of reproductive barriers are important for maintaining species integrity, and how are species boundaries preserved in the face of gene flow? Ivey et al. (2023) find little evidence for reproductive barriers and uncover a history of introgression between two incipient species of monkeyflower. These findings contribute to a growing body of work that calls for a reconsideration of how speciation dynamics are modeled at the macroevolutionary level.

Genomic divergence between two sister Medicago species triggered by the Quaternary climatic oscillations in the Qinghai-Tibet Plateau and northern China.

Speciation is a central topic in evolutionary biology. However, it remains poorly understood of how genomic divergence originated and accumulatedin the face of gene flow during ecological adaptation. Closely related species that have adapted to distinct environments but inhabit some overlapping ranges provide an ideal system to evaluate this issue.Here, we combine population genomics and species distribution models (SDMs) to examine genomic divergences between two sister species, Medicago ruthenicaand M. archiducis-nicolai, that occur in northern China and the northeast Qinghai-Tibet Plateau (QTP), respectively, with overlapping distribution in the border of the two regions.Medicago ruthenicaand M. archiducis-nicolai are well-delimited based on population genomic data, although hybrids exist in sympatric sampling locations. Coalescent simulations and SDMs suggest that the two species diverged from each other in the Quaternary but have been in continuous contact with gene flow occurring between the two species ever since. We also discovered positive selection signatures associated with genes both outside and within genomic islands in both species that are likely involved in adaptations to arid and high-altitude environments. Our findings provide insights into how natural selection and climatic changes in the Quaternary initiated and maintained interspecific divergence of the two sister species.

Hybridization in the Fringed Orchids: An Analysis of Species Boundaries in the Face of Gene Flow

Natural hybridization between closely related species in sympatry is an evolutionary process that is common in orchids. Once seen as a threat to parent species, interspecific genetic change is increasingly viewed as a source of novel variation in some ecological contexts. Terrestrial fringed orchids in the genus Platanthera contain several clades with high genetic compatibility among species and many putative hybrids. We used biallelic SNPs generated with 3RAD sequencing to study the hybrid complex formed from the parent species P. blephariglottis, P. ciliaris, and P. cristata with high resolution. The genetic structure and phylogenetic relationship of the hybrid complex revealed site-dependent gene flow between species. We documented extensive hybridization and cryptic hybrids in sympatric sites. Interspecific genetic exchange is particularly common between P. blephariglottis and P. ciliaris, with cryptic hybrids among putative P. ciliaris samples being more common than parental assignments in sympatric sites. Hybridization across the triad species complex can reticulate lineages and introduce adaptive alleles. Conversely, it can reduce diversification rates and introduce maladaptive alleles. Investigation into whether anthropogenic forces are eroding species boundaries, particularly the permeable P. blephariglottis and P. ciliaris boundary, is appropriate for conservation efforts.

Standing genetic variation and chromosome differences drove rapid ecotype formation in a major malaria mosquito

Species distributed across heterogeneous environments often evolve locally adapted ecotypes, but understanding of the genetic mechanisms involved in their formation and maintenance in the face of gene flow is incomplete. In Burkina Faso, the major African malaria mosquito Anopheles funestus comprises two strictly sympatric and morphologically indistinguishable yet karyotypically differentiated forms reported to differ in ecology and behavior. However, knowledge of the genetic basis andenvironmental determinants of An. funestus diversification was impeded by lack of modern genomic resources. Here, we applied deep whole-genome sequencing and analysis to test the hypothesis that these two forms are ecotypes differentially adapted to breeding in natural swamps versus irrigated rice fields. We demonstrate genome-wide differentiation despite extensive microsympatry, synchronicity, and ongoing hybridization. Demographic inference supports a split only ~1,300 y ago, closely following the massive expansion of domesticated African rice cultivation ~1,850 y ago. Regions of highest divergence, concentrated in chromosomal inversions, were under selection during lineage splitting, consistent with local adaptation. The origin of nearly all variations implicated in adaptation, including chromosomal inversions, substantially predates the ecotype split, suggesting that rapid adaptation was fueled mainly by standing genetic variation. Sharp inversion frequency differences likely facilitated adaptive divergence between ecotypes by suppressing recombination between opposing chromosomal orientations of the two ecotypes, while permitting free recombination within the structurally monomorphic rice ecotype. Our results align with growing evidence from diverse taxa that rapid ecological diversification can arise from evolutionarily old structural genetic variants that modify genetic recombination.

Life on a beach leads to phenotypic divergence despite gene flow for an island lizard

Limited spatial separation within small islands suggests that observed population divergence may occur due to habitat differences without interruption to gene flow but strong evidence of this is scarce. The wall lizard Teira dugesii lives in starkly contrasting shingle beach and inland habitats on the island of Madeira. We used a matched pairs sampling design to examine morphological and genomic divergence between four beach and adjacent (<1 km) inland areas. Beach populations are significantly darker than corresponding inland populations. Geometric morphometric analyses reveal divergence in head morphology: beach lizards have generally wider snouts. Genotyping-by-sequencing allows the rejection of the hypothesis that beach populations form a distinct lineage. Bayesian analyses provide strong support for models that incorporate gene flow, relative to those that do not, replicated at all pairs of matched sites. Madeiran lizards show morphological divergence between habitats in the face of gene flow, revealing how divergence may originate within small islands.

Climate adaptation and vulnerability of foundation species in a global change hotspot.

Climate change is altering species ranges, and relative abundances within ranges, as populations become differentially adapted and vulnerable to the climates they face. Understanding present species ranges, whether species harbour and exchange adaptive variants, and how variants are distributed across landscapes undergoing rapid change, is therefore crucial to predicting responses to future climates and informing conservation strategies. Such insights are nonetheless lacking for most species of conservation concern. We assess genomic patterns of neutral variation, climate adaptation and climate vulnerability (offsets in predicted distributions of putatively adaptive variants across present and future landscapes) for sister foundation species, the marine tubeworms Galeolaria caespitosa and Galeolaria gemineoa, in a sentinel region for climate change impacts. We find that species are genetically isolated despite uncovering sympatry in their ranges, show parallel and nonparallel signals of thermal adaptation on spatial scales smaller than gene flow across their ranges, and are predicted to face different risks of maladaptation under future temperatures across their ranges. Our findings have implications for understanding local adaptation in the face of gene flow, and generate spatially explicit predictions for climatic disruption of adaptation and species distributions in coastal ecosystems that could guide experimental validation and conservation planning.

Genome-phenotype-environment associations identify signatures of selection in a panmictic population of threespine stickleback.

Adaptive genetic divergence occurs when selection imposed by the environment causes the genomic component of the phenotype to differentiate. However, genomic signatures of natural selection are usually identified without information on which trait is responding to selection by which selective agent(s). Here, we integrate whole-genome sequencing with phenomics and measures of putative selective agents to assess the extent of adaptive divergence in threespine stickleback occupying the highly heterogeneous lake Mývatn, NE Iceland. We find negligible genome wide divergence, yet multiple traits (body size, gill raker structure and defence traits) were divergent along known ecological gradients (temperature, predatory bird densities and water depth). SNP based heritability of all measured traits was high (h2 =0.42-0.65), indicating adaptive potential for all traits. Environment-association analyses further identified thousands of loci putatively involved in selection, related to genes linked to, for instance, neuron development and protein phosphorylation. Finally, we found that loci linked to water depth were concurrently associated with pelvic spine length variation - supporting the conclusion that divergence in pelvic spine length occurred in the face of gene flow. Our results suggest that whilst there is substantial genetic variation in the traits measured, phenotypic divergence of Mývatn stickleback is mostly weakly associated with environmental gradients, potentially as a result of substantial gene flow. Our study illustrates the value of integrative studies that combine genomic assays of multivariate trait variation with landscape genomics.

River‐of‐origin assignment of migratory Striped Bass, with implications for mixed‐stock analysis

AbstractObjectiveThe Striped Bass Morone saxatilis is an anadromous teleost with a native range extending north from the Gulf of Mexico into Canadian waters. Far‐ranging coastal migrations support one of the most popular recreational fisheries in the United States. Identifying the underlying population genetic structure of the spawning populations and the genetic markers capable of differentiating among them advances our understanding of these economically and ecologically important fish and enables more targeted management to occur.MethodsWe used a restriction site‐associated DNA sequencing approach to identify neutral and adaptive single‐nucleotide polymorphisms (SNPs), and we determined the population genetic structure of 438 adult Striped Bass sampled from nine spawning locations along the Atlantic coast from the Roanoke River, United States, to the Miramichi River, Canada.ResultThe two Canadian populations (Shubenacadie and Miramichi rivers) were genetically distinct from U.S. populations and from each other. Neutral loci differentiated Striped Bass from U.S. waters into four genetically distinct populations: Roanoke River, Hudson–Kennebec River, Upper Chesapeake Bay–Potomac River–Delaware River, and Choptank River (eastern Chesapeake Bay). Outlier loci further differentiated the Delaware River from the Chesapeake Bay tributaries, suggesting that there may be local adaptation in the face of gene flow. We identified 1300 highly informative SNPs (the top 10% [with respect to the genetic differentiation index FST] of the full suite of 13,361 SNPs in our study) capable of assigning fish with at least 90% accuracy to their river of origin; through simulations, we established their applicability for conducting robust mixed‐stock analyses of the coastal migratory Striped Bass fishery.ConclusionThis study demonstrated that neutral and adaptive loci together provide evidence for fine‐scale population structure of migratory Striped Bass, and these loci provide the most informative genetic panel for mixed‐stock analysis of Striped Bass to date, capable of assigning fish to their spawning river of origin.

Complex cycles of divergence and migration shape lineage structure in the common kingsnake species complex.

The Nearctic is a complex patchwork of habitats and geologic features that form barriers to gene flow resulting in phylogeographic structure and speciation in many lineages. Habitats are rarely stable over geologic time, and the Nearctic has undergone major climatic changes in the past few million years. We use the common kingsnake species complex to study how climate, geography, and history influence lineage formation over a large, complex landscape. Nearctic/North America. Common kingsnake, Lampropeltis getula, species complex. We analyzed genome-wide sequence data from 51 snakes spanning the majority of the species complex's range. We used population clustering, generalized dissimilarity modeling, and coalescent methods to identify the number of genetic clusters within the L. getula complex, infer the environmental correlates of genetic differentiation, and estimate models of divergence and gene flow among lineages. We identified three major lineages within the L. getula complex and further continuous spatial structure within lineages. The most important ecological correlates of genetic distance in the complex are related to aridity and precipitation, consistent with lineage breaks at the Great Plains/Desert ecotone and the Cochise Filter Barrier. Lineages are estimated to have undergone multiple rounds of isolation and secondary contact, with highly asymmetric migration occurring at present. Changing climates combined with a large and geologically complex landscape have resulted in a mosaic of discrete and spatially continuous genetic structure. Multiple rounds of isolation and secondary contact as climate fluctuated over the past ~4.4 My have likely driven the evolution of discrete lineages that maintain high levels of gene flow. Continuous structure is strongly shaped by aridity and precipitation, suggesting roles for major precipitation gradients in helping to maintain lineage identity in the face of gene flow when lineages are in geographic contact.

Inversion invasions: when the genetic basis of local adaptation is concentrated within inversions in the face of gene flow.

Across many species where inversions have been implicated in local adaptation, genomes often evolve to contain multiple, large inversions that arise early in divergence. Why this occurs has yet to be resolved. To address this gap, we built forward-time simulations in which inversions have flexible characteristics and can invade a metapopulation undergoing spatially divergent selection for a highly polygenic trait. In our simulations, inversions typically arose early in divergence, captured standing genetic variation upon mutation, and then accumulated many small-effect loci over time. Under special conditions, inversions could also arise late in adaptation and capture locally adapted alleles. Polygenic inversions behaved similarly to a single supergene of large effect and were detectable by genome scans. Our results show that characteristics of adaptive inversions found in empirical studies (e.g. multiple large, old inversions that are FST outliers, sometimes overlapping with other inversions) are consistent with a highly polygenic architecture, and inversions do not need to contain any large-effect genes to play an important role in local adaptation. By combining a population and quantitative genetic framework, our results give a deeper understanding of the specific conditions needed for inversions to be involved in adaptation when the genetic architecture is polygenic. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

Species Persistence with Hybridization in Toad-Headed Lizards Driven by Divergent Selection and Low Recombination.

Speciation plays a central role in evolutionary studies, and particularly how reproductive isolation (RI) evolves. The origins and persistence of RI are distinct processes that require separate evaluations. Treating them separately clarifies the drivers of speciation and then it is possible to link the processes to understand large-scale patterns of diversity. Recent genomic studies have focused predominantly on how species or RI originate. However, we know little about how species persist in face of gene flow. Here, we evaluate a contact zone of two closely related toad-headed lizards (Phrynocephalus) using a chromosome-level genome assembly and population genomics. To some extent, recent asymmetric introgression from Phrynocephalus putjatai to P. vlangalii reduces their genomic differences. However, their highly divergent regions (HDRs) have heterogeneous distributions across the genomes. Functional gene annotation indicates that many genes within HDRs are involved in reproduction and RI. Compared with allopatric populations, contact areas exhibit recent divergent selection on the HDRs and a lower population recombination rate. Taken together, this implies that divergent selection and low genetic recombination help maintain RI. This study provides insights into the genomic mechanisms that drive RI and two species persistence in the face of gene flow during the late stage of speciation.

Phylogenetic relationships and evolutionary patterns of the genus Psammolestes Bergroth, 1911 (Hemiptera: Reduviidae: Triatominae)

BackgroundThe evolutionary history of biodiversity in South America has been poorly studied in the seasonal dry tropical forest (SDTF). Species diversification in this ecosystem may have a twofold explanation. First, intermittent connections in the middle and late Pleistocene promoted species dispersal and/or genetic connectivity between lineages isolated in disjunct patches of forest. Second, allopatric speciation proceeded immediately after the formation and colonization of the SDTF in the Neogene. Here we studied the diversification of Psammolestes, a genus endemic of the SDTF and naturally infected with Trypanosoma cruzi (agent of Chagas disease), using a combination of phylogenetic, population genetics and niche model methods, and evaluated the reliability of the three morphospecies currently recognized.ResultsOur multilocus analyses recovered P. coreodes and P. tertius in a monophyletic clade sister to P. arthuri. Species delimitation tests recovered these lineages as different species despite the shared genetic variation observed between P. coreodes and P. tertius in five genes. Also, genetic variation of the genus clustered in three groups that were consistent with the three morphospecies. Our demographic model predicted a scenario of divergence in absence of gene flow, suggesting that mixed haplotypes may be the result of shared ancestral variation since the divergence of the subtropical-temperate species P. coreodes and P. tertius. In contrast, the tropical species P. arthuri was highly differentiated from the other two in all tests of genetic structure, and consistently, the Monmonier’s algorithm identified a clear geographical barrier that separates this species from P. coreodes and P. tertius.ConclusionsWe found three genetically structured lineages within Psammolestes that diverged in absence of gene flow in the late Miocene. This result supports a scenario of species formation driven by geographical isolation rather than by divergence in the face of gene flow associated with climatic oscillations in the Pleistocene. Also, we identified the Amazon basin as a climatic barrier that separates tropical from subtropical-temperate species, thus promoting allopatric speciation after long range dispersion. Finally, each species of Psammolestes occupies different climatic niches suggesting that niche conservatism is not crucial for species differentiation. These findings influence the current vector surveillance programs of Chagas disease in the region.

Demography and selection analysis of the incipient adaptive radiation of a Hawaiian woody species

Ecological divergence in a species provides a valuable opportunity to study the early stages of speciation. We focused on Metrosideros polymorpha, a unique example of the incipient radiation of woody species, to examine how an ecological divergence continues in the face of gene flow. We analyzed the whole genomes of 70 plants collected throughout the island of Hawaii, which is the youngest island with the highest altitude in the archipelago and encompasses a wide range of environments. The continuous M. polymorpha forest stands on the island of Hawaii were differentiated into three genetic clusters, each of which grows in a distinctive environment and includes substantial genetic and phenotypic diversity. The three genetic clusters showed signatures of selection in genomic regions encompassing genes relevant to environmental adaptations, including genes associated with light utilization, oxidative stress, and leaf senescence, which are likely associated with the ecological differentiation of the species. Our demographic modeling suggested that the glaberrima cluster in wet environments maintained a relatively large population size and two clusters split: polymorpha in the subalpine zone and incana in dry and hot conditions. This ecological divergence possibly began before the species colonized the island of Hawaii. Interestingly, the three clusters recovered genetic connectivity coincidentally with a recent population bottleneck, in line with the weak reproductive isolation observed in the species. This study highlights that the degree of genetic differentiation between ecologically-diverged populations can vary depending on the strength of natural selection in the very early phases of speciation.

A phylogeny of Antirrhinum reveals parallel evolution of alpine morphology.

Parallel evolution of similar morphologies in closely related lineages provides insight into the repeatability and predictability of evolution. In the genus Antirrhinum (snapdragons), as in other plants, a suite of morphological characters are associated with adaptation to alpine environments. We tested for parallel trait evolution in Antirrhinum by investigating phylogenetic relationships using restriction-site associated DNA (RAD) sequencing. We then associated phenotypic information to our phylogeny to reconstruct the patterns of morphological evolution and related this to evidence for hybridisation between emergent lineages. Phylogenetic analyses showed that the alpine character syndrome is present in multiple groups, suggesting that Antirrhinum has repeatedly colonised alpine habitats. Dispersal to novel environments happened in the presence of intraspecific and interspecific gene flow. We found support for a model of parallel evolution in Antirrhinum. Hybridisation in natural populations, and a complex genetic architecture underlying the alpine morphology syndrome, support an important role of natural selection in maintaining species divergence in the face of gene flow.

Use of Genomic Resources to Assess Adaptive Divergence and Introgression in Oaks

Adaptive divergence is widely accepted as a contributor to speciation and the maintenance of species integrity. However, the mechanisms leading to reproductive isolation, the genes involved in adaptive divergence, and the traits that shape the adaptation of wild species to changes in climate are still largely unknown. In studying the role of ecological interactions and environment-driven selection, trees have emerged as potential model organisms because of their longevity and large genetic diversity, especially in natural habitats. Due to recurrent gene flow among species with different ecological preferences, oaks arose as early as the 1970s as a model for understanding how speciation can occur in the face of interspecific gene flow, and what we mean by “species” when geographically and genomically heterogeneous introgression seems to undermine species’ genetic coherence. In this review, we provide an overview of recent research into the genomic underpinnings of adaptive divergence and maintenance of species integrity in oaks in the face of gene flow. We review genomic and analytical tools instrumental to better understanding mechanisms leading to reproductive isolation and environment-driven adaptive introgression in oaks. We review evidence that oak species are genomically coherent entities, focusing on sympatric populations with ongoing gene flow, and discuss evidence for and hypotheses regarding genetic mechanisms linking adaptive divergence and reproductive isolation. As the evolution of drought- and freezing-tolerance have been key to the parallel diversification of oaks, we investigate the question of whether the same or a similar set of genes are involved in adaptive divergence for drought and stress tolerance across different taxa and sections. Finally, we propose potential future research directions on the role of hybridization and adaptive introgression in adaptation to climate change.

Speciation and secondary contact in a fossorial island endemic, the São Tomé caecilian.

A period of isolation in allopatry typically precedes local adaptation and subsequent divergence among lineages. Alternatively, locally adapted phenotypes may arise and persist in the face of gene flow, resulting in strong correlations between ecologically-relevant phenotypic variation and corresponding environmental gradients. Quantifying genetic, ecological, and phenotypic divergence in such lineages can provide insights into the abiotic and biotic mechanisms that structure populations and drive the accumulation of phenotypic and taxonomic diversity. Low-vagility organisms whose distributions span ephemeral geographic barriers present the ideal evolutionary context within which to address these questions. Here, we combine genetic (mtDNA and genome-wide SNPs) and phenotypic data to investigate the divergence history of caecilians (Amphibia: Gymnophiona) endemic to the oceanic island of São Tomé in the Gulf of Guinea archipelago. Consistent with a previous mtDNA study, we find two phenotypically and genetically distinct lineages that occur along a north-to-south axis with extensive admixture in the centre of the island. Demographic modelling supports divergence in allopatry (~300kya) followed by secondary contact (~95kya). Consequently, in contrast to a morphological study that interpreted latitudinal phenotypic variation in these caecilians as a cline within a single widespread species, our analyses suggest a history of allopatric lineage divergence and subsequent hybridization that may have blurred species boundaries. We propose that late Pleistocene volcanic activity favoured allopatric divergence between these lineages with local adaptation to climate maintaining a stable hybrid zone in the centre of São Tomé Island. Our study joins a growing number of systems demonstrating lineage divergence on volcanic islands with stark environmental transitions across small geographic distances.