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Abstract Background Few models of genetic hitchhiking in subdivided populations have been developed and the rarity of empirical examples is even more striking. We here provide evidences of genetic hitchhiking in a subdivided population of the marine mussel Mytilus edulis. In the Bay of Biscay (France), a patch of M. edulis populations happens to be separated from its North Sea conspecifics by a wide region occupied only by the sister species M. galloprovincialis. Although genetic differentiation between the two M. edulis regions is largely non-significant at ten marker loci (average FST~0.007), a strong genetic differentiation is observed at a single locus (FST = 0.25). We validated the outlier status of this locus, and analysed DNA sequence polymorphism in order to identify the nature of the selection responsible for the unusual differentiation. Results We first showed that introgression of M. galloprovincialis alleles was very weak in both populations and did not significantly affect their differentiation. Secondly, we observed the genetic signature of a selective sweep within both M. edulis populations in the form of a star-shaped clade of alleles. This clade was nearly fixed in the North Sea and was segregating at a moderate frequency in the Bay of Biscay, explaining their genetic differentiation. Incomplete fixation reveals that selection was not direct on the locus but that the studied sequence recombined with a positively selected allele at a linked locus while it was on its way to fixation. Finally, using a deterministic model we showed that the wave of advance of a favourable allele at a linked locus, when crossing a strong enough barrier to gene flow, generates a step in neutral allele frequencies comparable to the step observed between the two M. edulis populations at the outlier locus. In our case, the position of the barrier is now materialised by a large patch of heterospecific M. galloprovincialis populations. Conclusion High FST outlier loci are usually interpreted as being the consequence of ongoing divergent local adaptation. Combining models and data we show that among-population differentiation can also dramatically increase following a selective sweep in a structured population. Our study illustrates how a striking geographical pattern of neutral diversity can emerge from past indirect hitchhiking selection in a structured population. Note Nucleotide sequences reported in this paper are available in the GenBank™ database under the accession numbers EU684165 – EU684228.

Human transport of species across oceans disrupts natural dispersal barriers and facilitates hybridization between previously allopatric species. The recent introduction of the North Pacific sea squirt, Ciona robusta , into the native range of the North Atlantic sea squirt, Ciona intestinalis , is a good example of this outcome. Recent studies have revealed an adaptive introgression in a single chromosomal region from the introduced into the native species. Here, we monitored this adaptive introgression over time, examining both the frequency of adaptive alleles at the core and the hitchhiking footprint in the shoulders of the introgression island by studying a thousand Ciona spp. individuals collected in 22 ports of the contact zone, 14 of which were sampled 20 generations apart. For that purpose, we developed a KASP multiplex genotyping approach, which proved effective in identifying native, nonindigenous and hybrid individuals and in detecting introgressed haplotypes. We found no early generation hybrids in the entire sample, and field observations suggest a decline in the introduced species. At the core region of the introgression sweep, where the frequency of C. robusta alleles is the highest and local adaptation genes must be, we observed stable frequencies of adaptive alien alleles in both space and time. In contrast, we observed erosion of C. robusta ancestry tracts in flanking chromosomal shoulders on the edges of the core, consistent with the second phase of a local sweep and a purge of hitchhiked incompatible mutations. We hypothesize that adaptive introgression may have modified the competition relationships between the native and invasive species in human-altered environments., (© The Author(s) 2024. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEN).)

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., (© 2024 John Wiley & Sons Ltd.)

Anthropogenic impacts on the environment alter speciation processes by affecting both geographical contexts and selection patterns on a worldwide scale. Here we review evidence of these effects. We find that human activities often generate spatial isolation between populations and thereby promote genetic divergence but also frequently cause sudden secondary contact and hybridization between diverging lineages. Human-caused environmental changes produce new ecological niches, altering selection in diverse ways that can drive diversification; but changes also often remove niches and cause extirpations. Human impacts that alter selection regimes are widespread and strong in magnitude, ranging from local changes in biotic and abiotic conditions to direct harvesting to global climate change. Altered selection, and evolutionary responses to it, impacts early-stage divergence of lineages, but does not necessarily lead toward speciation and persistence of separate species. Altogether, humans both promote and hinder speciation, although new species would form very slowly relative to anthropogenic hybridization, which can be nearly instantaneous. Speculating about the future of speciation, we highlight two key conclusions: (1) Humans will have a large influence on extinction and "despeciation" dynamics in the short term and on early-stage lineage divergence, and thus potentially speciation in the longer term, and (2) long-term monitoring combined with easily dated anthropogenic changes will improve our understanding of the processes of speciation. We can use this knowledge to preserve and restore ecosystems in ways that promote (re-)diversification, increasing future opportunities of speciation and enhancing biodiversity., (Copyright © 2023 Cold Spring Harbor Laboratory Press; all rights reserved.)

Gene flow governs the contemporary spatial structure and dynamic of populations as well as their long-term evolution. For species that disperse using atmospheric or oceanic flows, biophysical models allow predicting the migratory component of gene flow, which facilitates the interpretation of broad-scale spatial structure inferred from observed allele frequencies among populations. However, frequent mismatches between dispersal estimates and observed genetic diversity prevent an operational synthesis for eco-evolutionary projections. Here we use an extensive compilation of 58 population genetic studies of 47 phylogenetically divergent marine sedentary species over the Mediterranean basin to assess how genetic differentiation is predicted by Isolation-By-Distance, single-generation dispersal and multi-generation dispersal models. Unlike previous approaches, the latter unveil explicit parents-to-offspring links (filial connectivity) and implicit links among siblings from a common ancestor (coalescent connectivity). We find that almost 70 % of observed variance in genetic differentiation is explained by coalescent connectivity over multiple generations, significantly outperforming other models. Our results offer great promises to untangle the eco-evolutionary forces that shape sedentary population structure and to anticipate climate-driven redistributions, altogether improving spatial conservation planning., (© 2022. The Author(s).)

Although all marine ecosystems have experienced global-scale losses, oyster reefs have shown the greatest. Therefore, substantial efforts have been dedicated to restoration of such ecosystems during the last two decades. In Europe, several pilot projects for the restoration of the native European flat oyster, Ostrea edulis , recently begun and recommendations to preserve genetic diversity and to conduct monitoring protocols have been made. In particular, an initial step is to test for genetic differentiation against homogeneity among the oyster populations potentially involved in such programs. Therefore, we conducted a new sampling of wild populations at the European scale and a new genetic analysis with 203 markers to (1) confirm and study in more detail the pattern of genetic differentiation between Atlantic and Mediterranean populations, (2) identify potential translocations that could be due to aquaculture practices and (3) investigate the populations at the fringe of the geographical range, since they seemed related despite their geographic distance. Such information should be useful to enlighten the choice of the animals to be translocated or reproduced in hatcheries for further restocking. After the confirmation of the general geographical pattern of genetic structure and the identification of one potential case of aquaculture transfer at a large scale, we were able to detect genomic islands of differentiation mainly in the form of two groups of linked markers, which could indicate the presence of polymorphic chromosomal rearrangements. Furthermore, we observed a tendency for these two islands and the most differentiated loci to show a parallel pattern of differentiation, grouping the North Sea populations with the Eastern Mediterranean and Black Sea populations, against geography. We discussed the hypothesis that this genetic parallelism could be the sign of a shared evolutionary history of the two groups of populations despite them being at the border of the distribution nowadays., Competing Interests: The authors do not declare any conflict of interest., (© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

Humans have built ports on all the coasts of the world, allowing people to travel, exploit the sea, and develop trade. The proliferation of these artificial habitats and the associated maritime traffic is not predicted to fade in the coming decades. Ports share common characteristics: Species find themselves in novel singular environments, with particular abiotic properties-e.g., pollutants, shading, protection from wave action-within novel communities in a melting pot of invasive and native taxa. Here, we discuss how this drives evolution, including setting up of new connectivity hubs and gateways, adaptive responses to exposure to new chemicals or new biotic communities, and hybridization between lineages that would have never come into contact naturally. There are still important knowledge gaps, however, such as the lack of experimental tests to distinguish adaptation from acclimation processes, the lack of studies to understand the putative threats of port lineages to natural populations or to better understand the outcomes and fitness effects of anthropogenic hybridization. We thus call for further research examining "biological portuarization," defined as the repeated evolution of marine species in port ecosystems under human-altered selective pressures. Furthermore, we argue that ports act as giant mesocosms often isolated from the open sea by seawalls and locks and so provide replicated life-size evolutionary experiments essential to support predictive evolutionary sciences., Competing Interests: None to declare., (© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

The Almeria-Oran Front (AOF) is a recognised hotspot of genetic differentiation in the sea, with genetic discontinuities reported in more than 50 species. The AOF is a barrier to dispersal and an ecological boundary; both can determine the position of these genetic breaks. However, the maintenance of genetic differentiation is likely reinforced by genetic barriers. A general drawback of previous studies is an insufficient density of sampling sites at the transition zone, with a conspicuous lack of samples from the southern coastline. We analysed the fine-scale genetic structure in the mussel Mytilus galloprovincialis using a few ancestry-informative loci previously identified from genome scans. We discovered a 600-km-wide mosaic hybrid zone eastward of the AOF along the Algerian coasts. This mosaic zone provides a new twist to our understanding of the Atlantic-Mediterranean transition because it demonstrates that the two lineages can live in sympatry with ample opportunities to interbreed in a large area, but they hardly do so. This implies that some form of reproductive isolation must exist to maintain the two genetic backgrounds locally cohesive. The mosaic zone ends with an abrupt genetic shift at a barrier to dispersal in the Gulf of Bejaia, Eastern Algeria. Simulations of endogenous or exogenous selection in models that account for the geography and hydrodynamic features of the region support the hypothesis that sister hybrid zones could have been differentially trapped at two alternative barriers to dispersal and/or environmental boundaries, at Almeria in the north and Bejaia in the south. A preponderantly unidirectional north-south gene flow next to the AOF can also maintain a patch of intrinsically maintained genetic background in the south and the mosaic structure, even in the absence of local adaptation. Our results concur with the coupling hypothesis that suggests that natural barriers can explain the position of genetic breaks, while their maintenance depends on genetic barriers.

Natural selection plays a variety of roles in hybridization, speciation, and admixture. Most research has focused on two extreme cases: crosses between closely related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. But many natural populations must fall into intermediate regimes, with multiple types of gene interaction, and these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, which were designed for the extreme cases, and invoke either mildly deleterious recessives, or discrete hybrid incompatibilities. Our model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants ( Zea , Populus , and Senecio ) and animals ( Mus , Teleogryllus , and Drosophila ). The predictions are generally supported, and the model explains a number of surprising empirical patterns. Our approach enables novel and complementary uses of genome-wide datasets, which do not depend on identifying outlier loci, or "speciation genes" with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

It is now common for population geneticists to estimate FST for a large number of loci across the genome, before testing for selected loci as being outliers to the FST distribution. One surprising result of such FST scans is the often high proportion (>1% and sometimes >10%) of outliers detected, and this is often interpreted as evidence for pervasive local adaptation. In this issue of Molecular Ecolog, Fourcade et al. (2013) observe that a particularly high rate of FST outliers has often been found in river organisms, such as fishes or damselflies, despite there being no obvious reason why selection should affect a larger proportion of the genomes of these organisms. Using computer simulations, Fourcade et al. (2013) show that the strong correlation in co-ancestry produced in long onedimensional landscapes (such as rivers, valleys, peninsulas, oceanic ridges or coastlines) greatly increases the neutral variance in FST, especially when the landscape is further reticulated into fractal networks. As a consequence, outlier tests have a high rate of false positives, unless this correlation can be taken into account. Fourcade et al.'s study highlights an extreme case of the general problem, first noticed by Robertson (1975a,b) and Nei & Maruyama (1975), that correlated co-ancestry inflates the neutral variance in FST when compared to its expectation under an island model of population structure. Similar warnings about the validity of outlier tests have appeared regularly since then but have not been widely cited in the recent genomics literature. We further emphasize that FST outliers can arise in many different ways and that outlier tests are not designed for situations where the genetic architecture of local adaptation involves many loci.

Marine bivalves show among the greatest allozyme diversity ever reported in Eukaryotes, putting them historically at the heart of the neutralist-selectionist controversy on the maintenance of genetic variation. Although it is now acknowledged that this high diversity is most probably a simple consequence of a large population size, convincing support for this explanation would require a rigorous assessment of the silent nucleotide diversity in natural populations of marine bivalves, which has not yet been done. This study investigated DNA sequence polymorphism in a set of 37 nuclear loci in wild samples of the flat oyster Ostrea edulis. Silent diversity was found to be only moderate (0.7%), and there was no departure from demographic equilibrium under the Wright-Fisher model, suggesting that the effective population size might not be as large as might have been expected. In accordance with allozyme heterozygosity, nonsynonymous diversity was comparatively very high (0.3%), so that the nonsynonymous to silent diversity ratio reached a value rarely observed in any other organism. We estimated that one-quarter of amino acid-changing mutations behave as neutral in O. edulis, and as many as one-third are sufficiently weakly selected to segregate at low frequency in the polymorphism. Finally, we inferred that one oyster is expected to carry more than 4800 non-neutral alleles (or 4.2 cM(-1)). We conclude that a high load of segregating non-neutral amino-acid polymorphisms contributes to high protein diversity in O. edulis. The high fecundity of marine bivalves together with an unpredictable and highly variable success of reproduction and recruitment (sweepstakes reproduction) might produce a greater decoupling between Ne and N than in other organisms with lower fecundities, and we suggest this could explain why a higher segregating load could be maintained for a given silent mutation effective size.

We studied the genetic basis of post-zygotic isolation in the marine mussels Mytilus edulis and Mytilus galloprovincialis. Evidence was obtained for a high number of recessive Dobzhansky-Muller substitutions in the genome of these two mussel taxa. We analysed the segregation of unlinked diagnostic markers in the progeny of two backcrosses and an F2 cross, 36 h and 200 days after fertilization. Directional selection favouring M. galloprovincialis genotypes was observed in both kinds of cross. In the F2, epistatic interactions between each pair of chromosome fragments mapped by the markers were identified in addition. Our results imply that homozygous-homozygous interactions are required for breakdown of coadaptation, in accordance with the dominance theory of post-zygotic isolation. Endogenous post-zygotic selection distributed over many loci throughout the genome provides the missing factor explaining the astonishing persistence and strength of barriers to neutral introgression in such a dispersive taxon as Mytilus.

Marine organisms challenge the classical theories of local adaptation and speciation because their planktonic larvae have the potential to maintain high gene flow. The marine-speciation paradox is illustrated by contact zones between incipient species that are so large that allopatric divergence seems unlikely. For this reason any mechanism preventing sympatric larvae of two incipient species from coexisting in the same habitats can be a powerful promoter of speciation. The contact zone between two hybridizing taxa of mussel, Mytilus edulis and M. galloprovincialis, in Europe provides an excellent example. Although the zone itself extends over thousands of kilometres, the opportunities for interbreeding are considerably reduced by the small-scale mosaic structure of the zone, where local patches of each taxon alternate at scales of kilometres or less, in response to locally variable ecological factors. Habitat choice by settling larvae would be a less costly mechanism than post-settlement selection to maintain such a mosaic structure. Unfortunately the role of selective settlement has remained hypothetical because larvae could not be scored by classical genetic markers. PCR markers allowed us to study larvae and settlement in ecologically contrasting sites within the zone. We show that only a subset of the genotypes present in the plankton settle in some sites, and that the adults on these sites show the same genetic bias. Genetically based variation in pre-settlement processes therefore accounts for the ecological segregation observed, though it is not the only factor involved in limiting successful interbreeding. The present dataset also supports previous reports of partial spawning asynchrony.