Isolation Divergence Research Articles

Microgeographic speciation in a complex of Anatolian bush crickets facilitated by fast evolution of reproductive isolation.

Identifying the drivers of microgeographic speciation (i.e., speciation over small, local geographic scales) is key to understand the origin of speciose groups. Here, we use genomic data to infer the demographic processes underlying diversification in Poecilimon luschani (Orthoptera: Tettigoniidae), a species complex belonging to the most diverse genus of bush crickets from the Mediterranean region (>170 taxa) that comprises three recognized subspecies with small allopatric distributions in the topographically complex Teke Peninsula, southwestern Anatolia. Phylogenomic reconstructions that include all other taxa within the species group confirmed that subspecies of P. luschani originated from a common ancestor during the Pleistocene, supporting recent (<1 Ma) diversification within a small geographical area (ca. 120 × 80 km). Genetic clustering analyses corroborated the distinctiveness of each subspecies and the cohesiveness of their respective populations, with abrupt genetic discontinuities coinciding with contemporary range boundaries. Indeed, our analyses uncovered the presence of two sympatric cryptic sister lineages that diverged <300 ka ago and do not admix despite being co-distributed. Collectively, these results support that all lineages within the complex represent independently evolving entities corresponding to full-fledged species. Statistical evaluation of alternative models of speciation strongly supports a scenario of divergence in isolation followed by a period of limited gene flow during the last glacial period, when all lineages experienced marked expansions according to demographic reconstructions. Our study exemplifies how localized allopatric divergence and fast evolution of reproductive isolation can promote microgeographic speciation and explain the high rates of endemism characterizing biodiversity hotspots.

How does speciation in marine plankton work?

Marine plankton species are ecologically important, yet, it remains unclear how they originate in the ocean, where few barriers are apparent to cause the most common type of speciation - divergence in isolation. Here I discuss the use of modern evolutionary genetic approaches to shed light on longstanding questions regarding their evolution.

Variable hybridization between two Lake Tanganyikan cichlid species in recent secondary contact.

Closely related taxa frequently exist in sympatry before the evolution of robust reproductive barriers, which can lead to substantial gene flow. Post-divergence gene flow can promote several disparate trajectories of divergence ranging from the erosion of distinctiveness and eventual collapse of the taxa to the strengthening of reproductive isolation. Among many relevant factors, understanding the demographic history of divergence (e.g. divergence time and extent of historical gene flow) can be particularly informative when examining contemporary gene flow between closely related taxa because this history can influence gene flow's prevalence and consequences. Here, we used genotyping-by-sequencing data to investigate speciation and contemporary hybridization in two closely related and sympatrically distributed Lake Tanganyikan cichlid species in the genus Petrochromis. Demographic modelling supported a speciation scenario involving divergence in isolation followed by secondary contact with bidirectional gene flow. Further investigation of this recent gene flow found evidence of ongoing hybridization between the species that varied in extent between different co-occurring populations. Relationships between abundance and the degree of admixture across populations suggest that the availability of conspecific mates may influence patterns of hybridization. These results, together with the observation that sets of recently diverged cichlid taxa are generally geographically separated in the lake, suggest that ongoing speciation in Lake Tanganyikan cichlids relies on initial spatial isolation. Additionally, the spatial heterogeneity of admixture between the Petrochromis species illustrates the complexities of hybridization when species are in recent secondary contact.

Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization

Alpine biotas are paradigmatic of the countervailing roles of geographical isolation and dispersal during diversification. In temperate regions, repeated distributional shifts driven by Pleistocene climatic oscillations produced both recurrent pulses of population fragmentation and opportunities for gene flow during range expansions. Here, we test whether a model of divergence in isolation vs. with gene flow is more likely in the diversification of flightless alpine grasshoppers of the genus Podisma from the Iberian Peninsula. The answer to this question can also provide key insights about the pace of evolution. Specifically, if the data fit a divergence in isolation model, this suggests rapid evolution of reproductive isolation. Genomic data confirm a Pleistocene origin of the species complex, and multiple analytical approaches revealed limited asymmetric historical hybridization between two taxa. Genomic-based demographic reconstructions, spatial patterns of genetic structure and range shifts inferred from palaeodistribution modelling suggest severe range contraction accompanied by declines in effective population sizes during interglacials (i.e., contemporary populations confined to sky islands are relicts) and expansions during the coldest stages of the Pleistocene in each taxon. Although limited hybridization during secondary contact leads to phylogenetic uncertainty if gene flow is not accommodated when estimating evolutionary relationships, all species exhibit strong genetic cohesiveness. Our study lends support to the notion that the accumulation of incipient differences during periods of isolation were sufficient to lead to lineage persistence, but also that the demographic changes, dispersal constraints and spatial distribution of the sky islands themselves mediated species diversification in temperate alpine biotas.

Geography is more important than host plant use for the population genetic structure of a generalist insect herbivore.

Population divergence can occur due to mechanisms associated with geographic isolation and/or due to selection associated with different ecological niches. Much of the evidence for selection-driven speciation has come from studies of specialist insect herbivores that use different host plant species; however, the influence of host plant use on population divergence of generalist herbivores remains poorly understood. We tested how diet breadth, host plant species and geographic distance influence population divergence of the fall webworm (Hyphantria cunea; FW). FW is a broadly distributed, extreme generalist herbivore consisting of two morphotypes that have been argued to represent two different species: black-headed and red-headed. We characterized the differentiation of FW populations at two geographic scales. We first analysed the influence of host plant and geographic distance on genetic divergence across a broad continental scale for both colour types. We further analysed the influence of host plant, diet breadth and geographic distance on divergence at a finer geographic scale focusing on red-headed FW in Colorado. We found clear genetic and morphological distinction between red- and black-headed FW, and Colorado FW formed a genetic cluster distinct from other locations. Although both geographic distance and host plant use were correlated with genetic distance, geographic distance accounted for up to 3× more variation in genetic distance than did host plant use. As a rare study investigating the genetic structure of a widespread generalist herbivore over a broad geographic range (up to 3,000km), our study supports a strong role for geographic isolation in divergence in this system.

The impacts of geographic and host species isolation on population divergence of Myxobolus lentisuturalis

Samples of Myxobolus lentisuturalis were found in the gallbladder of Carassius auratus in Chongqing, China, without obvious disease symptoms, which were different from samples reported in Hubei, China, and Italy which were described as highly pathogenic muscle-infecting species. In order to improve our understanding of the relationships between these different samples, we analyzed geography, DNA sequence data, and site specificity. The results indicated that (1) the genetic relationship between Chongqing and Italy samples of M. lentisuturalis was much closer than relationship between each of them and the Hubei samples; (2) host species isolation was more important than the geographic isolation in divergence of M. lentisuturalis samples, and the species might be specialized among its different host species; and (3) geographic isolation and infection-site variation played a limited impact in genetic differentiation among different samples of M. lentisuturalis infecting the same host species.

Population genetic structure and assessment of allochronic divergence in the Macoun’s Arctic (Oeneis macounii) butterfly

Patterns in the genetic variation of species can be used to infer their specific demographic and evolutionary history and provide insight into the general mechanisms underlying population divergence and speciation. The Macoun’s Arctic (Oeneis macounii (W.H. Edwards, 1885); MA) butterfly occurs across Canada and parts of the northern United States in association with jack pine (Pinus banksiana Lamb.) and lodgepole pine (Pinus contorta Douglas ex Loudon). MA’s current distribution is highly fragmented, and the extent of reproductive isolation among allopatric populations is unknown. Furthermore, although MA is biennial, adults emerge every year in some populations. These populations presumably consist of two alternate-year cohorts, providing the opportunity for sympatric divergence via allochronic isolation. Using mitochondrial DNA (mtDNA) and amplified fragment length polymorphism (AFLP) markers, we analyzed MA’s genetic structure to determine the current and historical role of allopatric and allochronic isolation in MA population divergence. Both markers revealed high diversity and a low, but significant, degree of spatial structure and pattern of isolation by distance. Phylogeographic structure was generally absent, with low divergence among mtDNA haplotypes. MA likely exhibits low dispersal and gene flow among most allopatric populations; however, there was no evidence of differentiation resulting from allochronic isolation for sympatric cohorts.

Genome-wide markers reveal a complex evolutionary history involving divergence and introgression in the Abert\u2019s squirrel (Sciurus aberti) species group

BackgroundGenetic introgression between divergent lineages is now considered more common than previously appreciated, with potentially important consequences for adaptation and speciation. Introgression is often asymmetric between populations and patterns can vary for different types of loci (nuclear vs. organellar), complicating phylogeographic reconstruction. The taxonomy of the ecologically specialized Abert’s squirrel species group has been controversial, and previous studies based on mitochondrial data have not fully resolved the evolutionary relationships among populations. Moreover, while these studies identified potential areas of secondary contact between divergent lineages, the possibility for introgression has not been tested.ResultsWe used RAD-seq to unravel the complex evolutionary history of the Abert’s squirrel species group. Although some of our findings reinforce inferences based on mitochondrial data, we also find significant areas of discordance. Discordant signals generally arise from previously undetected introgression between divergent populations that differentially affected variation at mitochondrial and nuclear loci. Most notably, our results support earlier claims (disputed by mitochondrial data) that S. aberti kaibabensis, found only on the north rim of the Grand Canyon, is highly divergent from other populations. However, we also detected introgression of S. aberti kaibabensis DNA into other S. aberti populations, which likely accounts for the previously inferred close genetic relationship between this population and those south of the Grand Canyon.ConclusionsOverall, the evolutionary history of Abert’s squirrels appears to be shaped largely by divergence during periods of habitat isolation. However, we also found evidence for interbreeding during periods of secondary contact resulting in introgression, with variable effects on mitochondrial and nuclear markers. Our results support the emerging view that populations often diversify under scenarios involving both divergence in isolation and gene flow during secondary contact, and highlight the value of genome-wide datasets for resolving such complex evolutionary histories.

The roles of geography and environment in divergence within and between two closely related plant species inhabiting an island‐like habitat

AbstractAimIn island‐like habitats, geographic isolation facilitates population and species divergence by constraining gene flow, while environmental isolation can enhance divergence. We tested the relative contribution of geographic and environmental isolation in genetic and phenotypic divergence within and between two species of the figwort Ameroglossum (Scrophulariaceae) inhabiting spatially isolated habitats, known as inselbergs.LocationBorborema Plateau, north‐eastern Brazil.MethodsMultivariate models of redundancy (RDAs) and partial redundancy analyses (pRDAs) were used to partition the geographic and climate components of genetic variation in 48 microsatellite alleles, and phenotypic variation in 11 leaf and flower traits. We also used linear mixed‐effect models (LMEs) to test independent associations of floral tube length variation among inselbergs with local pollinator phenotypes, climate and geography. In each approach, we analysed the data for each species separately and in pooled models for both species.ResultsRDAs revealed that genetic variation within and between the species of Ameroglossum was associated similarly with geography and climate. Phenotypic variation within A. manoel‐felixii and between species was also associated similarly with geography and climate but, within A. pernambucense, phenotype was more strongly associated with climate. Linear mixed‐effect models revealed that flower divergence in A. manoel‐felixii was associated only with the bill length of local hummingbirds, whereas floral variation in A. pernambucense was associated with geography, bill length and climate. Only climate was associated with flower divergence between species.Main conclusionsGenetic and phenotypic variation in Ameroglossum are associated with geographic and environmental isolation. These findings indicate a significant role of ecological factors shaping plant divergence among inselbergs, irrespective of their spatial distances.

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes.

Evaluating mechanisms of diversification in a Guineo-Congolian tropical forest frog using demographic model selection.

The accumulation of biodiversity in tropical forests can occur through multiple allopatric and parapatric models of diversification, including forest refugia, riverine barriers and ecological gradients. Considerable debate surrounds the major diversification process, particularly in the West African Lower Guinea forests, which contain a complex geographic arrangement of topographic features and historical refugia. We used genomic data to investigate alternative mechanisms of diversification in the Gaboon forest frog, Scotobleps gabonicus, by first identifying population structure and then performing demographic model selection and spatially explicit analyses. We found that a majority of population divergences are best explained by allopatric models consistent with the forest refugia hypothesis and involve divergence in isolation with subsequent expansion and gene flow. These population divergences occurred simultaneously and conform to predictions based on climatically stable regions inferred through ecological niche modelling. Although forest refugia played a prominent role in the intraspecific diversification of S.gabonicus, we also find evidence for potential interactions between landscape features and historical refugia, including major rivers and elevational barriers such as the Cameroonian Volcanic Line. We outline the advantages of using genomewide variation in a model-testing framework to distinguish between alternative allopatric hypotheses, and the pitfalls of limited geographic and molecular sampling. Although phylogeographic patterns are often species-specific and related to life-history traits, additional comparative studies incorporating genomic data are necessary for separating shared historical processes from idiosyncratic responses to environmental, climatic and geological influences on diversification.

Testing models of refugial isolation, colonization and population connectivity in two species of montane salamanders.

Pleistocene glaciations have profoundly affected patterns of genetic diversity within many species. Temperate alpine organisms likely experienced dramatic range shifts, given that much of their habitat was glaciated during this time. While the effects of glaciations are relatively well understood, the spatial locations of refugia and processes that gave rise to current patterns of diversity are less well known. We use a microsatellite data set to test hypotheses of population connectivity and refugial isolation in the web-toed salamanders (Hydromantes) of the Sierra Nevada. We reject models of refugia with subsequent expansion into either the high southern Sierra or low-elevation Owens Valley, in favor of a simple isolation model with no migration between current populations. We find no evidence of migration at even moderate spatial scales using a variety of analyses in the southern Sierra, and limited migration in the northern Sierra. These results suggest that divergence in isolation following fragmentation is the dominant process structuring genetic variation in these salamander species. In the context of anthropogenic climate change and habitat degradation, these results imply that salamanders and other low-vagility alpine organisms are at risk of decline as they are unlikely to migrate across large distances.

Assessing conservation risks to populations of an anadromous Arctic salmonid, the northern Dolly Varden (Salvelinus malma malma), via estimates of effective and census population sizes and approximate Bayesian computation

Census population size (N c ) is crucial to the development of resource management strategies, however, monitoring the effective population size (N e ) of managed populations has proliferated because of this parameter’s relationship to the short-term impacts of genetic stochasticity and long-term population viability. Thus, having a sound understanding of both N c and N e , including population connectivity, provides valuable insights into both the demographic and genetic risks to extinction. Here, we assessed microsatellite DNA variation in four (of five known) anadromous northern Dolly Varden (NDV, Salvelinus malma malma) populations from Canada’s western Arctic region, to estimate N e using both temporal-based and single-sample estimators and to test for associations between N e and N c . We also employed approximate Bayesian computation (ABC) to evaluate several evolutionary scenarios that have potentially shaped contemporary population structure in this species, focusing particularly on population size and connectivity. We found evidence for moderate to large contemporary and historical N e , suggesting that short- and long-term extinction risks are low for these populations. Estimates of contemporary and long-term N e were variable within and among populations and overall estimates could not be reliably linked with N c or available spawning habitat. The overall estimate of N e /N c , was 0.152 and ranged from 0.024 to 0.442 when including errors around the estimate of N e and N c . Finally, ABC analyses suggest that NDV had a common origin followed by divergence in isolation while maintaining large effective sizes, but also that these populations were bottlenecked in the past, likely the result of post-glacial colonization processes. These results corroborate indications of limited gene flow at present, indicating independent demographic and evolutionary trajectories that imply NDV is best managed on a per-river-population basis. Overall, the results of this study further our general understanding of N e , N e /N c and demographic independence in NDV, and provide a comprehensive and quantitative assessment of the potential genetic and demographic risk status of Arctic anadromous salmonids, including baselines for future monitoring.

Understanding the mechanisms of antitropical divergence in the seabird White-faced Storm-petrel (Procellariiformes: Pelagodroma marina) using a multilocus approach.

Analytical methods that apply coalescent theory to multilocus data have improved inferences of demographic parameters that are critical to understanding population divergence and speciation. In particular, at the early stages of speciation, it is important to implement models that accommodate conflicting gene trees, and benefit from the presence of shared polymorphisms. Here, we employ eleven nuclear loci and the mitochondrial control region to investigate the phylogeography and historical demography of the pelagic seabird White-faced Storm-petrel (Pelagodroma marina) by sampling subspecies across its antitropical distribution. Groups are all highly differentiated: global mitochondrial ΦST = 0.89 (P < 0.01) and global nuclear ΦST varies between 0.22 and 0.83 (all P < 0.01). The complete lineage sorting of the mitochondrial locus between hemispheres is corroborated by approximately half of the nuclear genealogies, suggesting a long-term antitropical divergence in isolation. Coalescent-based estimates of demographic parameters suggest that hemispheric divergence of P. marina occurred approximately 840 000 ya (95% HPD 582 000-1 170 000), in the absence of gene flow, and divergence within the Southern Hemisphere occurred 190 000 ya (95% HPD 96 000-600 000), both probably associated with the profound palaeo-oceanographic changes of the Pleistocene. A fledgling sampled in St Helena (tropical South Atlantic) suggests recent colonization from the Northern Hemisphere. Despite the great potential for long-distance dispersal, P. marina antitropical groups have been evolving as independent, allopatric lineages, and divergence is probably maintained by philopatry coupled with asynchronous reproductive phenology and local adaptation.

Genetic, ecological and morphological divergence between populations of the endangered Mexican Sheartail hummingbird (Doricha eliza).

The Mexican Sheartail (Doricha eliza), an endangered hummingbird, is endemic to Mexico where two populations have a disjunct distribution. One population is distributed along the northern tip of the Yucatan Peninsula whereas the other is mostly restricted to central Veracruz. Despite their disjunct distribution, previous work has failed to detect morphological or behavioral differences between these populations. Here we use variation in morphology, mtDNA and nuDNA sequences to determine the degree of morphological and molecular divergence between populations, their divergence time, and historical demography. We use species distribution modeling and niche divergence tests to infer the relative roles of vicariance and dispersal in driving divergence in the genus. Our Bayesian and maximum likelihood phylogenetic analyses revealed that Doricha eliza populations form a monophyletic clade and support their sister relationship with D. enicura. We found marked genetic differentiation, with reciprocal monophyly of haplotypes and highly restricted gene flow, supporting a history of isolation over the last 120,000 years. Genetic divergence between populations is consistent with the lack of overlap in environmental space and slight morphological differences between males. Our findings indicate that the divergence of the Veracruz and Yucatan populations is best explained by a combination of a short period of isolation exacerbated by subsequent divergence in climate conditions, and that rather than vicariance, the two isolated ranges of D. eliza are the product of recent colonization and divergence in isolation.

Phylogeography of the Sponge Suberites diversicolor in Indonesia: Insights into the Evolution of Marine Lake Populations

The existence of multiple independently derived populations in landlocked marine lakes provides an opportunity for fundamental research into the role of isolation in population divergence and speciation in marine taxa. Marine lakes are landlocked water bodies that maintain a marine character through narrow submarine connections to the sea and could be regarded as the marine equivalents of terrestrial islands. The sponge Suberites diversicolor (Porifera: Demospongiae: Suberitidae) is typical of marine lake habitats in the Indo-Australian Archipelago. Four molecular markers (two mitochondrial and two nuclear) were employed to study genetic structure of populations within and between marine lakes in Indonesia and three coastal locations in Indonesia, Singapore and Australia. Within populations of S. diversicolor two strongly divergent lineages (A & B) (COI: p = 0.4% and ITS: p = 7.3%) were found, that may constitute cryptic species. Lineage A only occurred in Kakaban lake (East Kalimantan), while lineage B was present in all sampled populations. Within lineage B, we found low levels of genetic diversity in lakes, though there was spatial genetic population structuring. The Australian population is genetically differentiated from the Indonesian populations. Within Indonesia we did not record an East-West barrier, which has frequently been reported for other marine invertebrates. Kakaban lake is the largest and most isolated marine lake in Indonesia and contains the highest genetic diversity with genetic variants not observed elsewhere. Kakaban lake may be an area where multiple putative refugia populations have come into secondary contact, resulting in high levels of genetic diversity and a high number of endemic species.

Complex evolutionary history of the pallid dotted-blue butterfly (Lycaenidae:Euphilotes pallescens) in the Great Basin of western North America

Aim The aim of this study was to investigate patterns of genetic isolation associated with populations in discrete habitat patches in a North American cold desert through analysis of the pallid dotted-blue butterfly, Euphilotes pallescens. This small butterfly is largely restricted to low-elevation habitats across the Great Basin. The apparent geographical isolation and reported morphological variation among E. pallescens populations makes this species an ideal candidate with which to investigate patterns of genetic isolation and diversification in this arid region. Location Great Basin, western North America. Methods We used sequence data from nuclear and mitochondrial genes to investigate genetic diversity among E. pallescens populations, and among E. pallescens and a number of closely related Euphilotes species, using Bayesian phylogenetic analyses, as well as population genetic analyses. In conjunction with genetic variation, morphological variation was examined in the context of geographical and subspecific differentiation. Results Our genetic and morphological analyses suggest a moderate amount of isolation among populations, consistent with the hypothesis of restricted gene flow among isolated dune habitats, and possibly associated with isolation in distinct Pleistocene refugia. The patterns of diversification within E. pallescens and among closely related species are complicated by discordance among phylogenetic reconstructions based on nuclear and mitochondrial genes. Discordance among gene genealogies suggests a complex evolutionary history, perhaps involving alternating periods of reticulation and divergence in isolation. Main conclusions Although E. pallescens may be a vagile species, we find that persistence on isolated dunes in the Great Basin is associated with appreciable genetic and morphological differentiation among populations. However, genetic, morphological and taxonomic axes of variation are only partially in agreement. More generally, the discordance we find among genetic regions is consistent with the ascendant paradigm in phylogenetic reconstruction: gene genealogies often do not perfectly match species trees. Thus we present Euphilotes as a model for future biogeographical and phylogenetic reconstructions employing larger data sets of independent sequence markers.

Origins of species richness in the Indo‐Malay‐Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis

AbstractThe Indo‐Malay‐Philippine (IMP) biodiversity hotspot, bounded by the Philippines, the Malay Peninsula and New Guinea, is the epicentre of marine biodiversity. Hypotheses to explain the source of the incredible number of species found there include the centre of overlap hypothesis, which proposes that in this region the distinct faunas of the Pacific and Indian Oceans overlap. Here we review the biogeographical evidence in support of this hypothesis. We examined tropical reef fish distributions, paying particular attention to sister species pairs that overlap in the IMP hotspot. We also review phylogeographical studies of wide‐ranging species for evidence of lineage divergence and overlap in the IMP region. Our synthesis shows that a pattern of isolation between the Pacific and the Indian Ocean faunas is evident across a wide range of taxa. The occurrence of sister species, with one member in each ocean, indicates that the mechanism(s) of isolation has been in effect since at least the Miocene, while phylogeographical studies indicate more recent divergences in the Pleistocene. Divergence in isolation followed by population expansion has led to an overlap of closely related taxa or genetic lineages in the hotspot, contributing to diversity and species richness in the region. These findings are consistent with the centre of overlap hypothesis and highlight the importance of this process in generating biodiversity within the IMP.

Crossing the Species Barrier: Genomic Hotspots of Introgression between Two Highly Divergent Ciona intestinalis Species

Inferring a realistic demographic model from genetic data is an important challenge to gain insights into the historical events during the speciation process and to detect molecular signatures of selection along genomes. Recent advances in divergence population genetics have reported that speciation in face of gene flow occurred more frequently than theoretically expected, but the approaches used did not account for genome-wide heterogeneity (GWH) in introgression rates. Here, we investigate the impact of GWH on the inference of divergence with gene flow between two cryptic species of the marine model Ciona intestinalis by analyzing polymorphism and divergence patterns in 852 protein-coding sequence loci. These morphologically similar entities are highly diverged molecular-wise, but evidence of hybridization has been reported in both laboratory and field studies. We compare various speciation models and test for GWH under the approximate Bayesian computation framework. Our results demonstrate the presence of significant extents of gene flow resulting from a recent secondary contact after >3 My of divergence in isolation. The inferred rates of introgression are relatively low, highly variable across loci and mostly unidirectional, which is consistent with the idea that numerous genetic incompatibilities have accumulated over time throughout the genomes of these highly diverged species. A genomic map of the level of gene flow identified two hotspots of introgression, that is, large genome regions of unidirectional introgression. This study clarifies the history and degree of isolation of two cryptic and partially sympatric model species and provides a methodological framework to investigate GWH at various stages of speciation process.

Environmental change as a driver of diversification in temporary aquatic habitats: does the genetic structure of extant fairy shrimp populations reflect historic aridification?

SummaryOver the past 65 my, theAustralian continent experienced a pronounced shift from predominantly wet, tropical, conditions to a much drier climate. Little is known, however, about the effect of this important continent‐wide event on freshwater organisms and ecosystems. Fairy shrimps (Crustacea;Anostraca) are ancient and specialist inhabitants of temporary and saline aquatic habitats that typically prevail under semiarid conditions. Therefore, they present suitable evolutionary models to study scenarios of historic environmental change and the impact of a drying climate on aquatic ecosystems in particular.Focussing on both macro‐ and micro‐evolution in the fairy shrimp genusBranchinellaand using mitochondrialDNAdata (16SandCOI), we evaluated whether patterns of contemporary genetic variation reflect historic climate change.There is a close match between episodes ofCenozoic climate change and macro‐evolutionary diversification inAustralian fairy shrimps, presumably mediated by a progressive increase in the abundance and diversity of temporary aquatic habitats on the continent. Micro‐evolutionary patterns reflect both range expansion and recent contraction, linked to extreme drying events during the Pleistocene glacial periods.This study effectively illustrates the potential long‐term effects of environmental change on the diversity and the evolutionary trajectories of the fauna of temporary waters. Moreover, it demonstrates the importance of adaptation to new environments and non‐adaptive processes, such as divergence in isolation, for explaining extant diversity patterns in this particular environment.