Divergence and gene flow history at two large chromosomal inversions underlying ecotype differentiation in the long-snouted seahorse.

Chromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations until one arrangement becomes fixed. Many questions remain about how inversion polymorphisms arise, how they are maintained over the long term, and ultimately, whether and how they contribute to speciation. The long-snouted seahorse (Hippocampus guttulatus) is genetically subdivided into geographic lineages and marine-lagoon ecotypes, with shared structural variation underlying lineage and ecotype divergence. Here, we aim to characterize structural variants and to reconstruct their history and suspected role in ecotype formation. We generated a near chromosome-level genome assembly and described genome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequences from Atlantic, Mediterranean, and Black Sea populations. By also analysing linked-read sequencing data, we found evidence for two chromosomal inversions that were several megabases in length and showed contrasting allele frequency patterns between lineages and ecotypes across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one likely being maintained by divergent selection and the other by pseudo-overdominance. A possible selective coupling between the two inversions was further supported by the absence of specific haplotype combinations and a putative functional interaction between the two inversions in reproduction. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels for the two inversions, with a likely impact on their dynamics and contribution to divergence and speciation.

Unidirectional trans-Atlantic gene flow and a mixed spawning area shape the genetic connectivity of Atlantic bluefin tuna.

The commercially important Atlantic bluefin tuna (Thunnus thynnus), a large migratory fish, has experienced notable recovery aided by accurate resource assessment and effective fisheries management efforts. Traditionally, this species has been perceived as consisting of eastern and western populations, spawning respectively in the Mediterranean Sea and the Gulf of Mexico, with mixing occurring throughout the Atlantic. However, recent studies have challenged this assumption by revealing weak genetic differentiation and identifying a previously unknown spawning ground in the Slope Sea used by Atlantic bluefin tuna of uncertain origin. To further understand the current and past population structure and connectivity of Atlantic bluefin tuna, we have assembled a unique dataset including thousands of genome-wide single-nucleotide polymorphisms (SNPs) from 500 larvae, young of the year and spawning adult samples covering the three spawning grounds and including individuals of other Thunnus species. Our analyses support two weakly differentiated but demographically connected ancestral populations that interbreed in the Slope Sea. Moreover, we also identified signatures of introgression from albacore (Thunnus alalunga) into the Atlantic bluefin tuna genome, exhibiting varied frequencies across spawning areas, indicating strong gene flow from the Mediterranean Sea towards the Slope Sea. We hypothesize that the observed genetic differentiation may be attributed to increased gene flow caused by a recent intensification of westward migration by the eastern population, which could have implications for the genetic diversity and conservation of western populations. Future conservation efforts should consider these findings to address potential genetic homogenization in the species.

Inter-Specific Genetic Exchange Despite Strong Divergence in Deep-Sea Hydrothermal Vent Gastropods of the Genus Alviniconcha.

Deep hydrothermal vents are highly fragmented and unstable habitats at all temporal and spatial scales. Such environmental dynamics likely play a non-negligible role in speciation. Little is, however, known about the evolutionary processes that drive population-level differentiation and vent species isolation and, more specifically, how geography and habitat specialisation interplay in the species history of divergence. In this study, the species range and divergence of Alviniconcha snails that occupy active Western Pacific vent fields was assessed by using sequence variation data of the mitochondrial Cox1 gene, RNAseq, and ddRAD-seq. Combining morphological description and sequence datasets of the three species across five basins, we confirmed that A. kojimai, A. boucheti, and A. strummeri, while partially overlapping over their range, display high levels of divergence in the three genomic compartments analysed that usually encompass values retrieved for reproductively isolated species with divergences rang from 9% to 12.5% (mtDNA) and from 2% to 3.1% (nuDNA). Moreover, the three species can be distinguished on the basis of their external morphology by observing the distribution of bristles and the shape of the columella. According to this sampling, A. boucheti and A. kojimai form an east-to-west species abundance gradient, whereas A. strummeri is restricted to the Futuna Arc/Lau and North Fiji Basins. Surprisingly, population models with both gene flow and population size heterogeneities among genomes indicated that these three species are still able to exchange genes due to secondary contacts at some localities after a long period of isolation.

Subtle limits to connectivity revealed by outlier loci within two divergent metapopulations of the deep-sea hydrothermal gastropod Ifremeria nautilei.

Hydrothermal vents form archipelagos of ephemeral deep-sea habitats that raise interesting questions about the evolution and dynamics of the associated endemic fauna, constantly subject to extinction-recolonization processes. These metal-rich environments are coveted for the mineral resources they harbour, thus raising recent conservation concerns. The evolutionary fate and demographic resilience of hydrothermal species strongly depend on the degree of connectivity among and within their fragmented metapopulations. In the deep sea, however, assessing connectivity is difficult and usually requires indirect genetic approaches. Improved detection of fine-scale genetic connectivity is now possible based on genome-wide screening for genetic differentiation. Here, we explored population connectivity in the hydrothermal vent snail Ifremeria nautilei across its species range encompassing five distinct back-arc basins in the Southwest Pacific. The global analysis, based on 10,570 single nucleotide polymorphism (SNP) markers derived from double digest restriction-site associated DNA sequencing (ddRAD-seq), depicted two semi-isolated and homogeneous genetic clusters. Demogenetic modeling suggests that these two groups began to diverge about 70,000 generations ago, but continue to exhibit weak and slightly asymmetrical gene flow. Furthermore, a careful analysis of outlier loci showed subtle limitations to connectivity between neighbouring basins within both groups. This finding indicates that migration is not strong enough to totally counterbalance drift or local selection, hence questioning the potential for demographic resilience at this latter geographical scale. These results illustrate the potential of large genomic data sets to understand fine-scale connectivity patterns in hydrothermal vents and the deep sea.

Age-specific survivorship and fecundity shape genetic diversity in marine fishes.

Genetic diversity varies among species due to a range of eco-evolutionary processes that are not fully understood. The neutral theory predicts that the amount of variation in the genome sequence between different individuals of the same species should increase with its effective population size ( N e ). In real populations, multiple factors that modulate the variance in reproductive success among individuals cause N e to differ from the total number of individuals ( N ). Among these, age-specific mortality and fecundity rates are known to have a direct impact on the N e / N ratio. However, the extent to which vital rates account for differences in genetic diversity among species remains unknown. Here, we addressed this question by comparing genome-wide genetic diversity across 16 marine fish species with similar geographic distributions but contrasted lifespan and age-specific survivorship and fecundity curves. We sequenced the whole genome of 300 individuals to high coverage and assessed their genome-wide heterozygosity with a reference-free approach. Genetic diversity varied from 0.2% to 1.4% among species, and showed a negative correlation with adult lifespan, with a large negative effect ( s l o p e = - 0.089 per additional year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset ( s l o p e = - 0.129 per additional year of lifespan). Using published vital rates for each species, we showed that the N e / N ratio resulting simply from life tables parameters can predict the observed differences in genetic diversity among species. Using simulations, we further found that the extent of reduction in N e / N with increasing adult lifespan is particularly strong under Type III survivorship curves (high juvenile and low adult mortality) and increasing fecundity with age, a typical characteristic of marine fishes. Our study highlights the importance of vital rates as key determinants of species genetic diversity levels in nature.

Systematics of European coastal anchovies (genus Engraulis Cuvier).

Reports of morphological differences between European anchovy (Engraulis cf. encrasicolus) from coastal and marine habitats have long existed in the ichthyologic literature and have given rise to a long-standing debate on their taxonomic status. More recently, molecular studies have confirmed the existence of genetic differentiation between the two anchovy ecotypes. Using ancestry-informative markers, we show that coastal anchovies throughout the Mediterranean share a common ancestry and that substantial genetic differentiation persists in different pairs of coastal/marine populations despite the presence of limited gene flow. On the basis of genetic and ecological arguments, we propose that coastal anchovies deserve a species status of their own (E. maeoticus) and argue that a unified taxonomical framework is critical for future research and management.

Chromosome anchoring in Senegalese sole (Solea senegalensis) reveals sex-associated markers and genome rearrangements in flatfish.

The integration of physical and high-density genetic maps is a very useful approach to achieve chromosome-level genome assemblies. Here, the genome of a male Senegalese sole (Solea senegalensis) was de novo assembled and the contigs were anchored to a high-quality genetic map for chromosome-level scaffolding. Hybrid assembled genome was 609.3 Mb long and contained 3403 contigs with a N50 of 513 kb. The linkage map was constructed using 16,287 informative SNPs derived from ddRAD sequencing in 327 sole individuals from five families. Markers were assigned to 21 linkage groups with an average number of 21.9 markers per megabase. The anchoring of the physical to the genetic map positioned 1563 contigs into 21 pseudo-chromosomes covering 548.6 Mb. Comparison of genetic and physical distances indicated that the average genome-wide recombination rate was 0.23 cM/Mb and the female-to-male ratio 1.49 (female map length: 2,698.4 cM, male: 2,036.6 cM). Genomic recombination landscapes were different between sexes with crossovers mainly concentrated toward the telomeres in males while they were more uniformly distributed in females. A GWAS analysis using seven families identified 30 significant sex-associated SNP markers located in linkage group 18. The follicle-stimulating hormone receptor appeared as the most promising locus associated with sex within a region with very low recombination rates. An incomplete penetrance of sex markers with males as the heterogametic sex was determined. An interspecific comparison with other Pleuronectiformes genomes identified a high sequence similarity between homologous chromosomes, and several chromosomal rearrangements including a lineage-specific Robertsonian fusion in S. senegalensis.

Spatial gradients of introgressed ancestry reveal cryptic connectivity patterns in a high gene flow marine fish.

Assessing genetic connectivity among populations in high gene flow species is sometimes insufficient to evaluate demographic connectivity. Genetic differentiation quickly becomes zero as soon as a few dozen migrants are exchanged per generation. This provides little information to determine whether migration can ensure demographic coupling. The resulting difficulties in delineating conservation units for the management of commercially exploited marine fish species are well illustrated in the case of the European sea bass (Dicentrarchus labrax). Previous attempts to assess connectivity patterns in the northeast Atlantic have been hampered by a lack of spatial genetic structure. In contrast, mark-recapture data suggested low migration rates between regional spawning areas. Here, we show how a spatial gradient of introgressed Mediterranean ancestry across the northeast Atlantic reflects cryptic patterns of genetic and demographic connectivity. Using a 1K SNP chip data set in 827 individuals sampled from Portugal to the North Sea, we found null overall genetic differentiation across the northeast Atlantic. We however detected a subtle latitudinal admixture gradient originating at the edge of the contact zone with the Mediterranean sea bass lineage. Two significant breaks in the ancestry gradient at the tip of Galicia and northern Brittany indicated barriers to effective dispersal between demographically distinct units. Moreover, a northward expansion signal in Irish and North Seas was revealed by the surfing of rare Mediterranean alleles at the edge of the species range. Our results show that introgressed ancestry gradients offer a powerful alternative to assess genetic and demographic connectivity when the neutral migration-drift balance is not informative.

Comparative genomics approach to evolutionary process connectivity.

The influence of species life history traits and historical demography on contemporary connectivity is still poorly understood. However, these factors partly determine the evolutionary responses of species to anthropogenic landscape alterations. Genetic connectivity and its evolutionary outcomes depend on a variety of spatially dependent evolutionary processes, such as population structure, local adaptation, genetic admixture, and speciation. Over the last years, population genomic studies have been interrogating these processes with increasing resolution, revealing a large diversity of species responses to spatially structured landscapes. In parallel, multispecies meta-analyses usually based on low-genome coverage data have provided fundamental insights into the ecological determinants of genetic connectivity, such as the influence of key life history traits on population structure. However, comparative studies still lack a thorough integration of macro- and micro-evolutionary scales to fully realize their potential. Here, I present how a comparative genomics framework may provide a deeper understanding of evolutionary process connectivity. This framework relies on coupling the inference of long-term demographic and selective history with an assessment of the contemporary consequences of genetic connectivity. Standardizing this approach across several species occupying the same landscape should help understand how spatial environmental heterogeneity has shaped the diversity of historical and contemporary connectivity patterns in different taxa with contrasted life history traits. I will argue that a reasonable amount of genome sequence data can be sufficient to resolve and connect complex macro- and micro-evolutionary histories. Ultimately, implementing this framework in varied taxonomic groups is expected to improve scientific guidelines for conservation and management policies.

The contribution of ancient admixture to reproductive isolation between European sea bass lineages.

Understanding how new species arise through the progressive establishment of reproductive isolation (RI) barriers between diverging populations is a major goal in Evolutionary Biology. An important result of speciation genomics studies is that genomic regions involved in RI frequently harbor anciently diverged haplotypes that predate the reconstructed history of species divergence. The possible origins of these old alleles remain much debated, as they relate to contrasting mechanisms of speciation that are not yet fully understood. In the European sea bass (Dicentrarchus labrax), the genomic regions involved in RI between Atlantic and Mediterranean lineages are enriched for anciently diverged alleles of unknown origin. Here, we used haplotype-resolved whole-genome sequences to test whether divergent haplotypes could have originated from a closely related species, the spotted sea bass (Dicentrarchus punctatus). We found that an ancient admixture event between D. labrax and D. punctatus is responsible for the presence of shared derived alleles that segregate at low frequencies in both lineages of D. labrax. An exception to this was found within regions involved in RI between the two D. labrax lineages. In those regions, archaic tracts originating from D. punctatus locally reached high frequencies or even fixation in Atlantic genomes but were almost absent in the Mediterranean. We showed that the ancient admixture event most likely occurred between D. punctatus and the D. labrax Atlantic lineage, while Atlantic and Mediterranean D. labrax lineages were experiencing allopatric isolation. Our results suggest that local adaptive introgression and/or the resolution of genomic conflicts provoked by ancient admixture have probably contributed to the establishment of RI between the two D. labrax lineages.

Within-Generation Polygenic Selection Shapes Fitness-Related Traits across Environments in Juvenile Sea Bream.

Understanding the genetic underpinnings of fitness trade-offs across spatially variable environments remains a major challenge in evolutionary biology. In Mediterranean gilthead sea bream, first-year juveniles use various marine and brackish lagoon nursery habitats characterized by a trade-off between food availability and environmental disturbance. Phenotypic differences among juveniles foraging in different habitats rapidly appear after larval settlement, but the relative role of local selection and plasticity in phenotypic variation remains unclear. Here, we combine phenotypic and genetic data to address this question. We first report correlations of opposite signs between growth and condition depending on juvenile habitat type. Then, we use single nucleotide polymorphism (SNP) data obtained by Restriction Associated DNA (RAD) sequencing to search for allele frequency changes caused by a single generation of spatially varying selection between habitats. We found evidence for moderate selection operating at multiple loci showing subtle allele frequency shifts between groups of marine and brackish juveniles. We identified subsets of candidate outlier SNPs that, in interaction with habitat type, additively explain up to 3.8% of the variance in juvenile growth and 8.7% in juvenile condition; these SNPs also explained significant fraction of growth rate in an independent larval sample. Our results indicate that selective mortality across environments during early-life stages involves complex trade-offs between alternative growth strategies.

Genetic Characterization of Cupped Oyster Resources in Europe Using Informative Single Nucleotide Polymorphism (SNP) Panels.

The Pacific oyster, Crassostrea gigas, was voluntarily introduced from Japan and British Columbia into Europe in the early 1970s, mainly to replace the Portuguese oyster, Crassostrea angulata, in the French shellfish industry, following a severe disease outbreak. Since then, the two species have been in contact in southern Europe and, therefore, have the potential to exchange genes. Recent evolutionary genomic works have provided empirical evidence that C. gigas and C. angulata exhibit partial reproductive isolation. Although hybridization occurs in nature, the rate of interspecific gene flow varies across the genome, resulting in highly heterogeneous genome divergence. Taking this biological property into account is important to characterize genetic ancestry and population structure in oysters. Here, we identified a subset of ancestry-informative makers from the most differentiated regions of the genome using existing genomic resources. We developed two different panels in order to (i) easily differentiate C. gigas and C. angulata, and (ii) describe the genetic diversity and structure of the cupped oyster with a particular focus on French Atlantic populations. Our results confirm high genetic homogeneity among Pacific cupped oyster populations in France and reveal several cases of introgressions between Portuguese and Japanese oysters in France and Portugal.

Using Haplotype Information for Conservation Genomics.

The particular combinations of alleles that define haplotypes along individual chromosomes can be determined with increasing ease and accuracy by using current sequencing technologies. Beyond allele frequencies, haplotype data collected in population samples contain information about the history of allelic associations in gene genealogies, and this is of tremendous potential for conservation genomics. We provide an overview of how haplotype information can be used to assess historical demography, gene flow, selection, and the evolutionary outcomes of hybridization across different timescales relevant to conservation issues. We address technical aspects of applying such approaches to nonmodel species. We conclude that there is much to be gained by integrating haplotype-based analyses in future conservation genomics studies.

Speciation history of European (Anguilla anguilla) and American eel (A. rostrata), analysed using genomic data.

Speciation in the ocean could differ from terrestrial environments due to fewer barriers to gene flow. Hence, sympatric speciation might be common, with American and European eel being candidates for exemplifying this. They show disjunct continental distributions on both sides of the Atlantic, but spawn in overlapping regions of the Sargasso Sea from where juveniles are advected to North American, European and North African coasts. Hybridization and introgression are known to occur, with hybrids almost exclusively observed in Iceland. Different speciation scenarios have been suggested, involving either vicariance or sympatric ecological speciation. Using RAD sequencing and whole-genome sequencing data from parental species and F1 hybrids, we analysed speciation history based on the joint allele frequency spectrum (JAFS) and pairwise sequentially Markovian coalescent (PSMC) plots. JAFS supported a model involving a split without gene flow 150,000-160,000 generations ago, followed by secondary contact 87,000-92,000 generations ago, with 64% of the genome experiencing restricted gene flow. This supports vicariance rather than sympatric speciation, likely associated with Pleistocene glaciation cycles and ocean current changes. Whole-genome PSMC analysis of F1 hybrids from Iceland suggested divergence 200,000 generations ago and indicated subsequent gene flow rather than strict isolation. Finally, simulations showed that results from both approaches (JAFS and PSMC) were congruent. Hence, there is strong evidence against sympatric speciation in North Atlantic eels. These results reiterate the need for careful consideration of cases of possible sympatric speciation, as even in seemingly barrier-free oceanic environments palaeoceanographic factors may have promoted vicariance and allopatric speciation.

The role of recombination on genome-wide patterns of local ancestry exemplified by supplemented brook charr populations.

Assessing the immediate and long-term evolutionary consequences of human-mediated hybridization is of major concern for conservation biology. Several studies have documented how selection in interaction with recombination modulates introgression at a genome-wide scale, but few have considered the dynamics of this process within and among chromosomes. Here, we used an exploited freshwater fish, the brook charr (Salvelinus fontinalis), for which decades of stocking practices have resulted in admixture between wild populations and an introduced domestic strain, to assess both the temporal dynamics and local chromosomal variation in domestic ancestry. We provide a detailed picture of the domestic ancestry patterns across the genome using about 33,000 mapped single nucleotide polymorphisms genotyped in 611 individuals from 24 supplemented populations. For each lake, we distinguished early- and late-generation hybrids using information regarding admixture tracts. To assess the selective outcomes following admixture we then evaluated the relationship between recombination and admixture proportions at three different scales: the whole genome, chromosomes and within 2-Mb windows. This allowed us to detect a wide range of evolutionary mechanisms varying along the genome, as reflected by the finding of favoured or disfavoured introgression of domestic haplotypes. Among these, the main factor modulating local ancestry was probably the presence of deleterious recessive mutations in the wild populations, which can be efficiently hidden to selection in the presence of long admixture tracts. Overall, our results emphasize the relevance of taking into consideration local ancestry information to assess both the temporal and the chromosomal variation in local admixture ancestry toward better understanding post-hybridization evolutionary outcomes.

The spatial scale of dispersal revealed by admixture tracts.

Evaluating species dispersal across the landscape is essential to design appropriate management and conservation actions. However, technical difficulties often preclude direct measures of individual movement, while indirect genetic approaches rely on assumptions that sometimes limit their application. Here, we show that the temporal decay of admixture tracts lengths can be used to assess genetic connectivity within a population introgressed by foreign haplotypes. We present a proof-of-concept approach based on local ancestry inference in a high gene flow marine fish species, the European sea bass (Dicentrarchus labrax). Genetic admixture in the contact zone between Atlantic and Mediterranean sea bass lineages allows the introgression of Atlantic haplotype tracts within the Mediterranean Sea. Once introgressed, blocks of foreign ancestry are progressively eroded by recombination as they diffuse from the western to the eastern Mediterranean basin, providing a means to estimate dispersal. By comparing the length distributions of Atlantic tracts between two Mediterranean populations located at different distances from the contact zone, we estimated the average per-generation dispersal distance within the Mediterranean lineage to less than 50 km. Using simulations, we showed that this approach is robust to a range of demographic histories and sample sizes. Our results thus support that the length of admixture tracts can be used together with a recombination clock to estimate genetic connectivity in species for which the neutral migration-drift balance is not informative or simply does not exist.

Polygenic selection drives the evolution of convergent transcriptomic landscapes across continents within a Nearctic sister species complex.

In contrast to the plethora of studies focusing on the genomic basis of adaptive phenotypic divergence, the role of gene expression during speciation has been much less investigated and consequently less understood. Yet, the convergence of differential gene expression patterns between closely related species-pairs might reflect the role of natural selection during the process of ecological speciation. Here, we test for intercontinental convergence in differential transcriptional signatures between limnetic and benthic sympatric species-pairs of Lake Whitefish (Coregonus clupeaformis) and its sister lineage, the European Whitefish (Coregonus lavaretus), using six replicated sympatric species-pairs (two in North America, two in Norway and two in Switzerland). We characterized both sequence variation in transcribed regions and differential gene expression between sympatric limnetic and benthic species across regions and continents. Our first finding was that differentially expressed genes (DEG) between limnetic and benthic whitefish tend to be enriched in shared polymorphism among sister lineages. We then used both genotypes and covariation in expression in order to infer polygenic selection at the gene level. We identified parallel outliers and DEG involving genes primarily overexpressed in limnetic species relative to the benthic species. Our analysis finally revealed the existence of shared genomic bases underlying parallel differential expression across replicated species-pairs from both continents, such as a cis-eQTL affecting the pyruvate kinase expression level involved in glycolysis. Our results are consistent with a long-standing role of natural selection in maintaining trans-continental diversity at phenotypic traits involved in ecological speciation between limnetic and benthic whitefishes.

Development of a large SNPs resource and a low-density SNP array for brown trout (Salmo trutta) population genetics.

BACKGROUND: The brown trout (Salmo trutta) is an economically and ecologically important species for which population genetic monitoring is frequently performed. The most commonly used genetic markers for this species are microsatellites and mitochondrial markers that lack replicability among laboratories, and a large genome coverage. An alternative that may be particularly efficient and universal is the development of small to large panels of Single Nucleotide Polymorphism markers (SNPs). Here, we used Restriction site Associated DNA sequences (RADs) markers to identify a set of 12,204 informative SNPs positioned on the brown trout linkage map and suitable for population genetics studies. Then, we used this novel resource to develop a cost-effective array of 192 SNPs (96 × 2) evenly spread on this map. This array was tested for genotyping success in five independent rivers occupied by two main brown trout evolutionary lineages (Atlantic -AT- and Mediterranean -ME-) on a total of 1862 individuals. Moreover, inference of admixture rate with domestic strains and population differentiation were assessed for a small river system (the Taurion River, 190 individuals) and results were compared to a panel of 13 microsatellites. RESULTS: A high genotyping success was observed for all rivers (< 1% of non-genotyped loci per individual), although some initially used SNP failed to be amplified, probably because of mutations in primers, and were replaced. These SNPs permitted to identify patterns of isolation-by-distance for some rivers. Finally, we found that microsatellite and SNP markers yielded very similar patterns for population differentiation and admixture assessments, with SNPs having better ability to detect introgression and differentiation. CONCLUSIONS: The novel resources provided here opens new perspectives for universality and genome-wide studies in brown trout populations.

Model-based demographic inference of introgression history in European whitefish species pairs'.

Parallel phenotypic differentiation is generally attributed to parallel adaptive divergence as an evolutionary response to similar environmental contrasts. Such parallelism may actually originate from several evolutionary scenarios ranging from repeated parallel divergence caused by divergent selection to a unique divergence event followed by gene flow. Reconstructing the evolutionary history underlying parallel phenotypic differentiation is thus fundamental to understand the relative contribution of demography and selection on genomic divergence during speciation. In this study, we investigate the divergence history of replicate European whitefish (Coregonus lavaretus), limnetic and benthic species pairs from two lakes in Norway and two lakes in Switzerland. Demographic models accounting for semi-permeability and linked selection were fitted to the unfolded joint allele frequency spectrum built from genome-wide SNPs and compared to each other in each species pair. We found strong support for a model of asymmetrical post-glacial secondary contact between glacial lineages in all four lakes. Moreover, our results suggest that heterogeneous genomic differentiation has been shaped by the joint action of linked selection accelerating lineage sorting during allopatry, and heterogeneous migration eroding divergence at different rates along the genome following secondary contact. Our analyses reveal how the interplay between demography, selection and historical contingency has influenced the levels of diversity observed in previous whitefish phylogeographic studies. This study thus provides new insights into the historical demographic and selective processes that shaped the divergence associated with ecological speciation in European whitefish.

Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages.

Diverging semi-isolated lineages either meet in narrow clinal hybrid zones, or have a mosaic distribution associated with environmental variation. Intrinsic reproductive isolation is often emphasized in the former and local adaptation in the latter, although both reduce gene flow between groups. Rarely are these two patterns of spatial distribution reported in the same study system. Here, we report that the long-snouted seahorse Hippocampus guttulatus is subdivided into discrete panmictic entities by both types of hybrid zones. Along the European Atlantic coasts, a northern and a southern lineage meet in the southwest of France where they coexist in sympatry-i.e., in the same geographical zone-with little hybridization. In the Mediterranean Sea, two lineages have a mosaic distribution, associated with lagoon-like and marine habitats. A fifth lineage was identified in the Black Sea. Genetic homogeneity over large spatial scales contrasts with isolation maintained in sympatry or close parapatry at a fine scale. A high variation in locus-specific introgression rates provides additional evidence that partial reproductive isolation must be maintaining the divergence. We find that fixed differences between lagoon and marine populations in the Mediterranean Sea belong to the most differentiated SNPs between the two Atlantic lineages, against the genome-wide pattern of structure that mostly follow geography. These parallel outlier SNPs cluster on a single chromosome-wide island of differentiation. Since Atlantic lineages do not map to lagoon-sea habitat variation, genetic parallelism at the genomic island suggests a shared genetic barrier contributes to reproductive isolation in contrasting contexts-i.e., spatial versus ecological. We discuss how a genomic hotspot of parallel differentiation could have evolved and become associated both with space and with a patchy environment in a single study system.