Nicolas Bierne

Adaptive introgression, the transfer of beneficial alleles between species through hybridization, is increasingly recognized as an important source of adaptation to novel environments. However, the theory of adaptive introgression has primarily been developed for a single panmictic population, whereas many empirical examples involve spatially subdivided populations. In such systems, a low-frequency adaptive allele may either represent the leading edge of an adaptive travelling wave or occur in a subpopulation where the introgressed allele is locally selected against. We explored how the relationship between adaptive allele frequency and introgressed tract length differs between these two scenarios. During the spread of an adaptive wave, introgressed tracts are progressively eroded by recombination with the genetic background of the receiving species, so that tract length, like allele frequency, reflects the distance traveled by the wave. Under local adaptation, however, allele frequency depends on the local balance between selection and migration, generally breaking this relationship. Simulations predicted a positive correlation between allele frequency and tract length during the spread of an unconditionally advantageous allele, but no correlation under local adaptation. We tested this prediction in a well-characterized case of adaptive introgression in the sea squirt Ciona intestinalis, using haplotagging to reconstruct phased genomes and local ancestry. We found no evidence of a relationship between adaptive allele frequency and introgressed tract length, supporting a model of local adaptation rather than an ongoing travelling wave. Author summary: Hybridization between species can transfer beneficial genetic variants from one species to another, enabling the latter to adapt to a new environment. However, such variants are not necessarily advantageous throughout the recipient species range. In geographically subdivided populations, a low-frequency introgressed allele may either have arrived recently or be selected against locally. Using simulations, we show that combining allele frequency with introgressed tract lengths clarifies this ambiguity, offering a straightforward method to distinguish between globally positive and locally varying selection. When an adaptive allele is beneficial everywhere, it spreads through populations as a travelling wave. Over time, recombination progressively shortens introgressed tracts. Populations reached first have higher frequencies of the adaptive allele sitting on longer introgressed tracts, whereas recently reached populations have lower frequencies and shorter tracts. When selection varies among populations, this relationship disappears because allele frequency reflects local selection rather than the history of the adaptive wave. We tested this prediction in a confirmed case of adaptive introgression in a sea squirt species by characterizing the footprint of introgressed tract length using local ancestry reconstruction. We found no correlation between allele frequency and introgressed tract length, supporting the hypothesis that variation in introgressed allele frequency reflects local selection rather than a traveling adaptive wave.

The European flat oyster (Ostrea edulis), like numerous other oyster species, has been exploited for millennia and cultivated and translocated for centuries. Following a severe population decline, and in the context of ongoing conservation and restoration programs, genetic considerations must now be addressed to avoid mistakes. The objective of our study was to complement population genetic studies conducted at various scales along European coasts. Our sampling primarily targeted the French Atlantic, English Channel, and Mediterranean coasts, aiming to provide a fine-scale genetic characterization of populations in these regions. By integrating SNP array and low-coverage sequencing datasets, we obtained a comprehensive overview of the population genetic structure of Ostrea edulis across western Europe. Most previously identified clusters in Western Europe were confirmed. In France, populations assigned to these clusters exhibited notable within-patch homogeneity. However, two key findings emerged: (1) an extensive overlap zone between the Atlantic and western Mediterranean clusters, spanning at least from southern Portugal to southern France, and (2) the detection of a novel, clearly distinct cryptic cluster east of the English Channel, whose geographic range remains to be better delineated. These insights are critical for informing management decisions, particularly as restoration and conservation plans are currently being implemented across the species' range.

The study of present-day species distributions often raises questions about historical demography. A particularly interesting phenomenon to put in historical context is contemporary human-induced atlantification and its role in reshaping Arctic ecosystems. Despite this, the colonisation history of the Arctic remains generally understudied. In this study, we investigated the demographic history of the northern acorn barnacle, Semibalanus balanoides, a typically boreal species on the Svalbard Archipelago. Our focus was to determine the source and timing of its colonisation of this Arctic archipelago. Using low-coverage whole-genome sequence data, we evaluated two competing hypotheses: whether S. balanoides populations colonised Svalbard through ancient natural processes before the Anthropocene, or if their appearance is more recent, either natural or a consequence of growing anthropogenic influences, such as increased connectivity and global warming. Our results suggest that this boreal species expanded into the Arctic during the later phase of the Holocene Thermal Optimum, well before human-induced climate change.

How the interplay of biotic and abiotic factors shapes current genetic diversity at the community level remains an open question, particularly in the deep sea. Comparative phylogeography of multiple species can reveal the influence of past climatic events, geographic barriers, and species life history traits on spatial patterns of genetic structure across lineages. To shed light on the factors that shape community-level genetic variation and to improve our understanding of deep-sea biogeographic patterns, we conducted a comparative population genomics study on seven hydrothermal vent species co-distributed in the Back-Arc Basins of the Southwest Pacific region. Using ddRAD-seq, we compared the range-wide distribution of genomic diversity across species and discovered a shared phylogeographic break. Demogenetic inference revealed shared histories of lineage divergence and a secondary contact. Low levels of asymmetric gene flow probably occurred in most species between the Woodlark and North Fiji basins, but the exact location of contact zones varied from species to species. For two species, we found individuals from the two lineages co-occurring in sympatry in Woodlark Basin. Although species exhibit congruent patterns of spatial structure (Eastern vs. Western sites), they also show variation in the degree of divergence among lineages across the suture zone. Our results also show heterogeneous gene flow across the genome, indicating possible partial reproductive isolation between lineages and early speciation. Our comparative study highlights the pivotal role of historical and contemporary factors, underscoring the need for a comprehensive approach—especially in addressing knowledge gaps on the life history traits of deep-sea species.

How the interplay of biotic and abiotic factors shapes current genetic diversity at the community level remains an open question, particularly in the deep sea. Comparative phylogeography of multiple species can reveal the influence of past climatic events, geographic barriers, and species life history traits on spatial patterns of genetic structure across lineages. To shed light on the factors that shape community-level genetic variation and to improve our understanding of deep-sea biogeographic patterns, we conducted a comparative population genomics study on seven hydrothermal vent species co-distributed in the Back-Arc Basins (BABs) of the Southwest Pacific region. Using ddRAD-seq, we compared the range-wide distribution of genomic diversity across species and discovered a shared phylogeographic break. Demogenetic inference revealed shared histories of lineage divergence and a secondary contact. Low levels of asymmetric gene flow probably occurred in most species between the Woodlark and North Fiji basins, but the exact location of contact zones varied from species to species. For two species, we found individuals from the two lineages co-occurring in sympatry in Woodlark Basin. Although species exhibit congruent patterns of spatial structure (Eastern vs Western sites), they also show variation in the degree of divergence among lineages across the suture zone. Our results also show heterogeneous gene flow across the genome, indicating possible partial reproductive isolation between lineages and early speciation. Our comparative study highlights the pivotal role of historical and contemporary factors, underscoring the need for a comprehensive approach—especially in addressing knowledge gaps on the life history traits of deep-sea species.

Inter-individual transmission of cancer cells represents a unique form of microparasites increasingly reported in marine bivalves. In this study, we sought to understand the ecology of the propagation of Mytilus trossulus Bivalve Transmissible Neoplasia 2 (MtrBTN2), a transmissible cancer affecting four Mytilus mussel species worldwide. We investigated the prevalence of MtrBTN2 in the mosaic hybrid zone of M. edulis and M. galloprovincialis along the French Atlantic coast, sampling contrasting natural and anthropogenic habitats. We observed a similar prevalence in both species, probably due to the spatial proximity of the two species in this region. Our results showed that ports had higher prevalence of MtrBTN2, with a possible hotspot observed at a shuttle landing dock. No cancer was found in natural beds except for two sites close to the hotspot, suggesting spillover. Ports may provide favourable conditions for the transmission of MtrBTN2, such as high mussel density, stressful conditions, sheltered and confined shores or buffered temperatures. Ships may also spread the disease through biofouling. Our results suggest ports may serve as epidemiological hubs, with maritime routes providing artificial gateways for MtrBTN2 propagation. This highlights the importance of preventing biofouling on docks and ship hulls to limit the spread of marine pathogens hosted by fouling species.

Transmissible cancer cell lines are rare biological entities giving rise to diseases at the crossroads of cancer and parasitic diseases. These malignant cells have acquired the amazing capacity to spread from host to host. They have been described only in dogs, Tasmanian devils and marine bivalves. The Mytilus trossulus bivalve transmissible neoplasia 2 (MtrBTN2) lineage has even acquired the capacity to spread inter-specifically between marine mussels of the Mytilus edulis complex worldwide. To identify the oncogenic processes underpinning the biology of these atypical cancers we performed transcriptomics of MtrBTN2 cells. Differential expression, enrichment, protein–protein interaction network, and targeted analyses were used. Overall, our results suggest the accumulation of multiple cancerous traits that may be linked to the long-term evolution of MtrBTN2. We also highlight that vertebrate and lophotrochozoan cancers could share a large panel of common drivers, which supports the hypothesis of an ancient origin of oncogenic processes in bilaterians.

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.

Human transport of species across oceans disrupts natural dispersal barriers and facilitates hybridisation 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, C. 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 alien genes 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, non-indigenous and hybrid individuals and in detecting introgressed haplotypes. Adaptive alien genes were detected where they had been found 20 generations ago, as well as in some newly sampled ports. The core region of the introgression, where the frequency of C. robusta alleles is the highest and locally adaptive genes must be, remains stable in both space and time. In contrast, we observed an 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 incompatible introgressed alleles. Our study reveals how the shoulders of an adaptive introgression island fall over time after the initial sweep.

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 over time until one arrangement becomes fixed. Many questions remain about how these different inversion polymorphisms arise, how the mechanisms responsible for their long-term maintenance interact, and ultimately how they contribute to speciation. The long-snouted seahorse ( Hippocampus guttulatus ) is known to be subdivided into partially isolated lineages and marine-lagoon ecotypes differentiated by structural variation. Here, we aim to characterise these differences along the entire genome, and to reconstruct their history and role in ecotype formation. We generated a near chromosome-level reference 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. Combined with linked-read sequencing data, we found evidence for two megabase-scale chromosomal inversions showing contrasted allele frequency patterns across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one being likely maintained by divergent selection, and the other by associative overdominance. Haplotype combinations characterising Mediterranean ecotypes also suggest the existence of potential interactions between the two inversions, possibly driven by environment-dependent fitness effects. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels between the two inversions, with a likely impact on their long-term dynamics.