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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.

International audience; 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 are 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.

Human-mediated introductions are reshuffling species distribution on a global scale. Consequently, an increasing number of allopatric taxa are now brought into contact, promoting introgressive hybridization between incompletely isolated species and new adaptive gene transfer. The broadcast spawning marine species, Ciona robusta, has been recently introduced in the native range of its sister taxa, Ciona intestinalis, in the English Channel and North-East Atlantic. These sea squirts are highly divergent, yet hybridization has been reported by crossing experiments and genetic studies in the wild. Here, we examined the consequences of secondary contact between C. intestinalis and C. robusta in the English Channel. We produced genomes phased by transmission to infer the history of divergence and gene flow, and analyzed introgressed genomic tracts. Demographic inference revealed a history of secondary contact with a low overall rate of introgression. Introgressed tracts were short, segregating at low frequency, and scattered throughout the genome, suggesting traces of past contacts during the last 30 ky. However, we also uncovered a hotspot of introgression on chromosome 5, characterized by several hundred kb-long C. robusta haplotypes segregating in C. intestinalis, that introgressed during contemporary times the last 75 years. Although locally more frequent than the baseline level of introgression, C. robusta alleles are not fixed, even in the core region of the introgression hotspot. Still, linkage-disequilibrium patterns and haplotype-based tests suggest this genomic region is under recent positive selection. We further detected in the hotspot an over-representation of candidate SNPs lying on a cytochrome P450 gene with a high copy number of tandem repeats in the introgressed alleles. Cytochromes P450 are a superfamily of enzymes involved in detoxifying exogenous compounds, constituting a promising avenue for functional studies. These findings support that introgression of an adaptive allele is possible between very divergent genomes and that anthropogenic hybridization can provide the raw material for adaptation of native lineages in the Anthropocene.

WOS:000777071200001; International audience; 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.

Reticulated evolution -i.e. secondary introgression/admixture between sister taxa- is increasingly recognized as a key evolutionary process that may play a role in structuring infra-specific genetic variation, and possibly promoting adaptation. Mytilus spp. is an ideal system to assess its importance, because these marine mussels form semi-isolated species that remain reproductively compatible over large time-scales. It includes three taxa that hybridize in the Northern Hemisphere (M. edulis, M. galloprovincialis and M. trossulus) and two taxa of uncertain ancestry in the Southern Hemisphere (M. platensis: South America and the Kerguelen Islands; and M. planulatus: Australasia). The Kerguelen mussels are of particular interest to investigate the potential role of admixture in enhancing micro-geographic structure, as they inhabit a small and isolated island in the Southern Ocean characterized by a highly heterogeneous environment, and genomic reticulation between Northern and Southern lineages has been suspected. Here, we extended a previous analysis by using targeted-sequencing data (51,878 SNPs) across the three Northern species and the Kerguelen population, coupled with a panel of 33 SNPs genotyped on 695 mussels across 35 sites in the Kerguelen Islands. The panel was enriched with ancestry-informative SNPs, i.e. SNPs that were more differentiated than the genomic average between Northern lineages, to evaluate whether reticulated evolution contributed to micro-geographic structure. We first showed that the Kerguelen population belongs to a divergent Southern lineage, most related to M. edulis mussels, that experienced secondary admixture with non-indigenous Northern species. We then demonstrated that the Kerguelen mussels were significantly differentiated over small spatial distance, and that this local genetic structure was associated with environmental variation and mostly revealed by ancestry-informative markers. Although local adaptation can explain the association with the environment we believe it more likely that environment variables better describe population connectivity than geographic distance. Our study highlights genetic connectivity of populations is more easily revealed by non-equilibrium secondary introgression clines at a subset of loci, while association with the environment should not be hastily advocated to support adaptation from admixture variation.

Transmissible cancers are parasitic malignant cell lineages that have acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukaemia-like disease. In Mytilus mussels, two lineages of bivalve transmissible neoplasia (BTN) have been described to date (MtrBTN1 and MtrBTN2), both of which emerged in a Mytilus trossulus founder individual. Here, we performed extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping 106single nucleotide polymorphisms of 5,907 European Mytilus mussels. Genetic analysis allowed us to simultaneously obtain the genotype of hosts - Mytilus edulis, M.galloprovincialis or hybrids - and the genotype of tumours of heavily infected individuals. In addition, a subset of 222 individuals were systematically genotyped and analysed by histology to screen for possible nontransmissible cancers. We detected MtrBTN2 at low prevalence in M. edulis, and also in M.galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found, but eight individuals with nontransmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M.trossulus individuals. The observed polymorphism is probably due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two sublineages divergent by 10% fixed somatic null alleles and one nonsynonymous mtCOI (mitochondrial cytochrome oxidase I) substitution are cospreading in the same geographical area, suggesting a complex diversification of MtrBTN2since its emergence and host species shift.

The implementation of One Health/EcoHealth/Planetary Health approaches has been identified as key (i) to address the strong interconnections between risk for pandemics, climate change and biodiversity loss, and (ii) to develop and implement solutions to these interlinked crises. As a response to the multiple calls of scientists in that direction, we have put forward seven long term research questions regarding COVID-19 and emerging infectious diseases (EIDs) that are based on an effective integration of environmental, ecological, evolutionary, and social sciences to better anticipate and mitigate EIDs. Research needs cover the social-ecology of infectious disease agents, their evolution, the determinants of susceptibility of humans and animals to infections, and the human and ecological factors accelerating infectious disease emergence. For comprehensive investigation, they include the development of nature-based solutions to interlinked global planetary crises, addressing ethical and philosophical questions regarding the relationship of humans to nature and regarding transformative changes to safeguard the environment and human health. In support of this research, we propose the implementation of innovative multidisciplinary facilities embedded in social-ecosystems locally: the “ecological health observatories” and the “living laboratories”. This work has been carried out in the frame of the EC project HERA (www.HERAresearchEU.eu) that aims to set the priorities for an environment, climate and health research agenda in the EU by adopting a systemic approach in the face of global environmental change.

International audience; Introduced species can impose profound impacts on the evolution of receiving communities with which they interact. If native and introduced taxa remain reproductively semi-isolated, human-mediated secondary contact may promote genetic exchange across newly created hybrid zones, potentially impacting native genetic diversity and invasive species spread. Here, we investigate the contributions of recent divergence histories and ongoing (post-introduction) gene flow between the invasive marine mussel, Mytilus galloprovincialis, and a morphologically indistinguishable and taxonomically contentious native Australian taxon, Mytilus planulatus. Using transcriptome-wide markers, we demonstrate that two contemporary M. galloprovincialis introductions into southeastern Australia originate from genetically divergent linecommunities with which they interact. If native and introduced taxa remain reproductively semi‐isolated, human‐mediated secondary contact may promote genetic exchange across newly created hybrid zones, potentially impacting native genetic diversity and invasive species spread. Here, we investigate the contributions of recent divergence histories and ongoing (post‐introduction) gene flow between the invasive marine mussel, Mytilus galloprovincialis, and a morphologically indistinguishable andtaxonomically contentious native Australian taxon, Mytilus planulatus. Using transcriptome‐wide markers, we demonstrate that two contemporary M. galloprovincialis introductions into south‐eastern Australia originate from genetically divergent lineages from its native range in the Mediterranean Sea and Atlantic Europe, where both introductions have led to repeated instances of admixture between introduced and endemic populations. Through increased genome‐wide resolution of species relationships, combined with demographic modelling, we validate that mussels sampled in Tasmania are representative of the endemic Australian taxon (M. planulatus), but share strong genetic affinities to M. galloprovincialis. Demographic inferences indicate late‐Pleistocene divergence times and historical gene flow between the Tasmanian endemic lineage and northern M. galloprovincialis, suggesting that native and introduced taxa have experienced a period of historical isolation of at least 100,000 years. Our results demonstrate that many genomic loci and sufficient sampling of closely related lineages in both sympatric (e.g. Australian populations) and allopatric (e.g. northernhemisphere Mytilus taxa) ranges are necessary to accurately (a) interpret patterns of intraspecific differentiation and to (b) distinguish contemporary invasive introgression from signatures left by recent divergence histories in high dispersal marine species. More broadly, our study fills a significant gap in systematic knowledge of native Australian biodiversity and sheds light on the intrinsic challenges for invasive species research when native and introduced species boundaries are not well defined.

International audience; The management of endangered species is complicated in the marine environment owing to difficulties to directly access, track and monitor in situ. Population genetics provide a genuine alternative to estimate population size and inbreeding using non-lethal procedures. The long-snouted seahorse, Hippocampus guttulatus, is facing multiple threats such as human disturbance or by-catch, and has been listed in the red list of IUCN. One large population is found in the Thau lagoon, in the south of France. A recent study has shown this population belongs to a genetic lineage only found in Mediterranean lagoons that can be considered as an Evolutionarily Significant Unit (ESU) and should be managed with dedicated conservation strategies. In the present study, we used genetic analysis of temporal samples to estimate the effective population size of the Thau population and correlations between individual multilocus heterozygosity and fitness traits to investigate the possible expression of inbreeding depression in the wild. Non-invasive sampling of 172 seahorses for which profiles were pictured and biometric data recorded were genotyped using 291 informative SNPs. Genetic diversity remained stable over a 7-year time interval. In addition, very low levels of close relatedness and inbreeding were observed, with only a single pair of related individuals in 2008 and two inbreds in 2013. We did not detect departure from identity equilibrium. The effective population size was estimated to be ­Ne=2742 (~40 reproductive seahorses per ­km2), larger than previously thought. No correlation was observed between heterozygosity and fluctuating asymmetry or other morphometric traits, suggesting a population with low variance in inbreeding. Together these results suggest this population does not meet conventional genetic criteria of an endangered population, as the population seems sufficiently large to avoid inbreeding and its detrimental effects. This study paves the way for the genetic monitoring of this recently discovered ESU of a species with patrimonial and conservation concerns.

Fishery of blue mussels Mytilus edulis constitutes a very important economic activity in Denmark, whereas mussel farming on long-lines or nets is a new, growing sector. Spawning from natural mussel beds takes place during early summer, and larvae disperse via water currents before settling on the bottom or on spat collectors in the farms. In the present study, we coupled a 3D physical model system (FlexSem) with an agent-based model in order to examine the connectivity of this marine system in terms of mussel larval dispersal and settling potential. To address this question, we (1) estimated the dispersal and connectivity between 17 areas in the Limfjorden, (2) identified the main donor and receiver areas of mussel larvae and (3) identified possible dispersal barriers. The results show that the central narrow strait in the Limfjorden was the main donor area in all the studied years, and that the adjacent eastern areas were the main receiver areas. Towards the inner basins of the Limfjorden, isolation increased and limited connectivity was observed. The results from the cluster analysis grouped the Limfjorden into 3 to 5 clusters, but there was still some exchange of simulated larvae observed among these clusters. Analysis of molecular markers revealed no genetic differentiation between areas and supports the model results, indicating that despite distinguishable hydrographic boundaries, the mussel populations in the Limfjorden are well connected. This study demonstrates how connectivity modeling can be used to support site selection processes in aquaculture.

Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN), both emerged in a M. trossulus founder individual, have been described to date (MtrBTN1 and MtrBTN2). Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping hundred SNPs of thousands of European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts -M. edulis, M. galloprovincialis or hybrids- and the genotype of tumors of heavily infected individuals. In addition, a subset of individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M. edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found but a few individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two divergent sublineages, confirmed by mtCOI sequences, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

When the ranges of closely-related lineages are large, and overlapping, we can often study introgression at many “replicated” contacts, with different locations and spatial scales. Here we analysed multiple contact zones of the M. edulis complex of marine mussel species, which represent a mosaic distribution of heterogeneously differentiated, semi-isolated genomes. Our aim was to contrast ongoing introgression at the heart of hybrid zones, with past introgression between similar parental populations, at increasing distance from the contact. Using a panel of ancestry-informative SNPs derived from a previous genomic study, we first confirm, with a broader sampling, that local introgression, affecting one but not all of the populations compared, is both widespread and heterogeneous across the genome. Some outlier loci show patterns of complete introgression in certain populations, and an absence of introgression in others. Genomic cline analyses reveal a globally high concordance among loci at a local scale, albeit with signals of asymmetric introgression at a few loci. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi-stable variants, or less loaded alleles. Given the mosaic structure of the M. edulis complex, with a succession of genetic barriers to gene flow, variants with enhanced introgression through one barrier can be trapped, maybe transiently, at the next barrier, confining introgression locally. This makes the Mytilus complex an ideal model of the heterogeneous porosity of species barriers.

This zenodo archive contains the vcf files and the R scripts used for thestatistical analyses of the paper "An introgression breakthrough left by an anthropogenic contact between two ascidians" published in Molecular Ecology in 2021. The fastq files processed by the stacks reference pipeline to produce the vcf files in this archive are available on NCBI under the bioproject "PRJNA759193". The analyses of the paper available here are divided in three parts: Analyses of the fine-scale population structure of Ciona intestinalis across the English Channel, the Iroise Sea, and the Bay of biscay Genotype file: Ciona_data1_finescale.vcf.gz Genotype file pruned for physical linkage: Ciona_dataset1_fine_scale_maf_thin.vcf R script file for pop. structure : Finescale_structure_dataset1.R Analyses of the large-scale population structure of C. instestinalis, C. robusta and C. roulei across the Atlantic and the Mediteranean sea Genotype file: Ciona_data2_Largescale.vcf.gz Genotype file pruned for physical linkage: Ciona_dataset2_largescale_maf_thin.vcf R script file for pop. structure : Largescale_structure_dataset2.R Linux + R script file for phylogeny: Phylogeny.R Analyse of introgression from C. robusta into C. intestinalis background: Genotype file: Ciona_data2_Largescale.vcf.gz Ancestry informative genotype: Ciona_diagnistic_SNPs_order.vcf R script for admixture across all chromosome: Ancestry_chromosome.R R script for HMM to detect introgression breakthrough from ancestry informative SNPs: HMM_log10FST+1_3norm_introgression_hotspot.R* *this script is a modified version of the script by Marques et al. (2016) available here: https://github.com/marqueda/HMM-detection-of-genomic-islands

When divergent populations form hybrids, hybrid fitness can vary with genome composition, current environmental conditions, and the divergence history of the populations. We develop analytical predictions for hybrid fitness, which incorporate all three factors. The predictions are based on Fisher's geometric model, and apply to a wide range of population genetic parameter regimes and divergence conditions, including allopatry and parapatry, local adaptation, and drift. Results show that hybrid fitness can be decomposed into intrinsic effects of admixture and heterozygosity, and extrinsic effects of the (local) adaptedness of the parental lines. Effect sizes are determined by a handful of geometric distances, which have a simple biological interpretation. These distances also reflect the mode and amount of divergence, such that there is convergence toward a characteristic pattern of intrinsic isolation. We next connect our results to the quantitative genetics of line crosses in variable or patchy environments. This means that the geometrical distances can be estimated from cross data, and provides a simple interpretation of the “composite effects.” Finally, we develop extensions to the model, involving selectively induced disequilibria, and variable phenotypic dominance. The geometry of fitness landscapes provides a unifying framework for understanding speciation, and wider patterns of hybrid fitness.

We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single-population or two-population datasets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: 1) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, 2) the best genomic model to determine whether the effective sizeNeand migration rateN.mare heterogeneously distributed along the genome (implying linked selection) and 3) loci in genomic regions most associated with barriers to gene flow. Also availableviaa web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations, and finally apply the method to published data on a divergence continuum composed by 28 pairs ofMytilusmussel populations/species.

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.

International audience; Non-native species experience novel selection pressures in introduced environments and may interbreed with native lineages. Species introductions therefore provide opportunities to investigate repeated patterns of adaptation and introgression across replicated contact zones. Here, we investigate genetic parallelism between multiple introduced populations of the invasive marine mussel, Mytilus galloprovincialis, in the absence (South Africa and California) and presence of hybridisation with a native congener (Mytilus planulatus in Batemans Bay and Sydney Harbour, Australia). Repeatability in post-introduction differentiation from native-range populations varied between genetically distinct Atlantic and Mediterranean lineages, with Atlantic-derived introductions displaying high differentiation (maxFST>0.4) and parallelism at outlier loci. Identification of long non-coding RNA transcripts (lncRNA) additionally allowed us to clarify that parallel responses are largely limited to protein-coding loci, with lncRNAs likely evolving under evolutionary constraints. Comparisons of independent hybrid zones revealed differential introgression most strongly in Batemans Bay, with an excess of M. galloprovincialis ancestry and resistance to introgression at loci differentiating parental lineages (M. planulatus and Atlantic M. galloprovincialis). Additionally, contigs putatively introgressed with divergent alleles from a closely related species, Mytilus edulis, showed stronger introgression asymmetries compared to genome-wide trends and also diverged in parallel in both Atlantic-derived introductions. These results suggest that divergent demographic histories experienced by introduced lineages, including pre-introduction introgression, influences contemporary admixture dynamics. Our findings build on previous investigations reporting contributions of historical introgression to intrinsic reproductive architectures shared between marine lineages and illustrate that interspecific introgression history can shape differentiation between colonising populations and their hybridisation with native congeners.

The development of male genital tract by female gastropods, or imposex, can be caused by the tributyltin used in antifouling paints. A spatial survey of imposex in the gastropod Stramonita haemastoma was conducted across five Western Mediterranean and eleven North-Eastern Atlantic sites, in order to monitor the effectiveness of the tributyltin regulation imposed in the International Maritime Organisation. Imposex still occurs in eight out of eleven Mediterranean sites and in three out of five Atlantic sites. Extreme values of imposex incidence (I%) and degree (VDSI) were recorded in Tunisia, mainly in Bizerta channel (I% = 96.2%, VDSI = 0.96). However, the Relative Penis Length index (RPLI) was higher in Western Mediterranean sites where values varied between 0.56 in Algiers (Algeria) and 11.80 in Bouznika (Morocco). In the European sites, moderate to low imposex level and degree were recorded. All the affected sites were below the Ecotoxicological Assessment Criteria (EAC) derived for TBT.

Transmissible cancers, in which cancer cells themselves act as an infectious agent, have been identified in Tasmanian devils, dogs, and four bivalves. We investigated a disseminated neoplasia affecting geographically distant populations of two species of mussels (Mytilus chilensis in South America and M. edulis in Europe). Sequencing alleles from four loci (two nuclear and two mitochondrial) provided evidence of transmissible cancer in both species. Phylogenetic analysis of cancer-associated alleles and analysis of diagnostic SNPs showed that cancers in both species likely arose in a third species of mussel (M. trossulus), but these cancer cells are independent from the previously identified transmissible cancer in M. trossulus from Canada. Unexpectedly, cancers from M. chilensis and M. edulis are nearly identical, showing that the same cancer lineage affects both. Thus, a single transmissible cancer lineage has crossed into two new host species and has been transferred across the Atlantic and Pacific Oceans and between the Northern and Southern hemispheres., eLife digest Cancer cells can grow and spread in one individual, but they normally do not spread to others. There are a few exceptions to this rule. For example, there are cancers in Tasmanian devils, dogs and bivalve shellfish that can spread to other members of the same species. In these creatures, cancer from one individual evolved the ability to spread throughout the population. These cancer cells infect animals like a pathogen. A fatal cancer called disseminated neoplasia affects many species of bivalves. In four bivalve species, including the marine mussel Mytilus trossulus, scientists have shown that the cancer can spread from one individual to another. This transmissible cancer has been found in M. trossulus mussels in British Columbia, Canada; but related species of mussels in other parts of the world also develop disseminated neoplasia. It is possible these other cancers are transmissible and have spread from one population of mussels to another. Yonemitsu et al. performed genetic analyses to show that cancers found in two other mussel species – Mytilus chilensis in South America and Mytilus edulis in Europe – are transmissible and arose in M. trossulus. The cancers in the South American and European mussels were nearly identical genetically, which suggests that they came from a single M. trossulus mussel with cancer at some point in the past. Somehow cancer cells spread between the Northern and the Southern Hemispheres and across the Atlantic Ocean, infecting multiple species across the world. The analyses also show that this cancer lineage is different from the one previously identified in British Columbia. These analyses show that bivalve transmissible neoplasia was able to spread worldwide, most likely through accidental transport of infected mussels on international shipping vessels. This suggests that human activities unwittingly introduced the disease to new areas. Learning more about transmissible cancers may help scientists understand how cancers evolve with their hosts in extreme situations.

International audience; Marine mussel production is of substantial economic interest in numerous coastal areas worldwide, making crucial the study of pathologies that affect them. Disseminated neoplasia (DN) has recently been suggested to be linked to blue mussel, Mytilus edulis, mortality outbreaks observed in France since 2014, although the evidence remains indirect. In order to improve DN detection and monitoring, we compared the sensitivity of four diagnostic tools, namely haemocytology, histology, flow cytometry, and genetics. Haemocytological examination gave the best results in sensitivity and had the advantage of being non-invasive, allowing disease progression to be followed in affected mussels. Using this approach, we showed that DN progression is usually slow, and we provide evidence of remission events. We observed a high diversity of forms and mitotic features of neoplastic cells located in the vesicular connective tissue but rarely in the haemolymph. Circulating cells occur as four main types but are homogenous in morphology and DNA content within a single individual. Polyploidy proved very high, from 8 N to 18 N. Genetic analysis of haemolymph DNA showed that a Mytilus trossulus genetic signal was associated with almost all the DN cases here diagnosed by haemocytological examination, regardless of the DN type. This result corroborates DN is a transmissible cancer that first originated in a M. trossulus host and subsequently crossed into M. edulis. No pre-neoplastic conditions were detectable. The prevalence of the disease was quite low, which, together with the low morbidity observed in the lab, suggest DN is unlikely to be the direct cause of mortality outbreaks in France.

International audience; Speciation often involves repeated episodes of genetic contact between divergent populations before reproductive isolation (RI) is complete. Whole-genome sequencing (WGS) holds great promise for unravelling the genomic bases of speciation. We have studied two ecologically divergent, hybridizing species of the 'model tree' genus Populus (poplars, aspens, cottonwoods), Populus alba and P. tremula, using >8.6 million single nucleotide polymorphisms (SNPs) from WGS of population pools. We used the genomic data to (i) scan these species' genomes for regions of elevated and reduced divergence, (ii) assess key aspects of their joint demographic history based on genomewide site frequency spectra (SFS) and (iii) infer the potential roles of adaptive and deleterious coding mutations in shaping the genomic landscape of divergence. We identified numerous small, unevenly distributed genome regions without fixed polymorphisms despite high overall genomic differentiation. The joint SFS was best explained by ancient and repeated gene flow and allowed pinpointing candidate interspecific migrant tracts. The direction of selection (DoS) differed between genes in putative migrant tracts and the remainder of the genome, thus indicating the potential roles of adaptive divergence and segregating deleterious mutations on the evolution and breakdown of RI. Genes affected by positive selection during divergence were enriched for several functionally interesting groups, including well-known candidate 'speciation genes' involved in plant innate immunity. Our results suggest that adaptive divergence affects RI in these hybridizing species mainly through intrinsic and demographic processes. Integrating genomic with molecular data holds great promise for revealing the effects of particular genetic pathways on speciation.

Research in speciation genetics has uncovered many robust patterns in intrinsic reproductive isolation, and fitness landscape models have been useful in interpreting these patterns. Here, we examine fitness landscapes based on Fisher's geometric model. Such landscapes are analogous to models of optimizing selection acting on quantitative traits, and have been widely used to study adaptation and the distribution of mutational effects. We show that, with a few modifications, Fisher's model can generate all of the major findings of introgression studies (including "speciation genes" with strong deleterious effects, complex epistasis and asymmetry), and the major patterns in overall hybrid fitnesses (including Haldane's Rule, the speciation clock, heterosis, hybrid breakdown, and male-female asymmetry in the F1). We compare our approach to alternative modeling frameworks that assign fitnesses to genotypes by identifying combinations of incompatible alleles. In some cases, the predictions are importantly different. For example, Fisher's model can explain conflicting empirical results about the rate at which incompatibilities accumulate with genetic divergence. In other cases, the predictions are identical. For example, the quality of reproductive isolation is little affected by the manner in which populations diverge.

Species introductions promote secondary contacts between taxa with long histories of allopatric divergence. Anthropogenic contact zones thus offer valuable contrasts to speciation studies in natural systems where past spatial isolations may have been brief or intermittent. Investigations of anthropogenic hybridization are rare for marine animals, which have high fecundity and high dispersal ability, characteristics that contrast to most terrestrial animals. Genomic studies indicate that gene flow can still occur after millions of years of divergence, as illustrated by invasive mussels and tunicates. In this context, we highlight three issues: (i) the effects of high propagule pressure and demographic asymmetries on introgression directionality, (ii) the role of hybridization in preventing introduced species spread, and (iii) the importance of postzygotic barriers in maintaining reproductive isolation. Anthropogenic contact zones offer evolutionary biologists unprecedented large scale hybridization experiments. In addition to breaking the highly effective reproductive isolating barrier of spatial segregation, they allow researchers to explore unusual demographic contexts with strong asymmetries. The outcomes are diverse, from introgression swamping to strong barriers to gene flow, and lead to local containment or widespread invasion. These outcomes should not be neglected in management policies of marine invasive species. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first 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. Many natural populations must fall into intermediate regimes, with multiple types of gene interaction, but these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, involving mildly deleterious recessives, or discrete hybrid incompatibilities. The model yields several new predictions, which we test with genomic data fromMytilusmussels, and published data from plants (Zea, PopulusandSenecio) and animals (Mus, TeleogryllusandDrosophila). The predictions are generally supported, and the model explains surprising empirical patterns that have been observed in both extreme regimes. 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.

This preprint has been peer-reviewed and recommended by Peer Community in Evolutionary Biology (PCI Evol Biol, doi: 10.24072/pci.evolbiol.100056). 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 can contribute to isolation. Rarely these two patterns of spatial distribution are 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 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. Surprisingly, 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. These parallel outlier SNPs cluster on a single chromosome-wide island of differentiation. Since Atlantic lineages do not match the 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 vs. ecological. We discuss how a genomic hotspot of parallel differentiation could have evolved and become associated either with space or with a patchy environment in a single study system.

The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and Crassostrea angulata, which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and the high degree of morphologic similarity. In particular, whether the presence of ecological and/or intrinsic isolating mechanisms contributes to species divergence is unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation is maintained under new environmental and demographic conditions. We generated a pseudochromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.

Speciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unlinked to speciation can interfere. Here, we used haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. We show that genomic islands first emerged in allopatry through the effect of linked selection acting on a heterogeneous recombination landscape. Upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we found that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.