François Bonhomme

The formation of ecotypes is driven by evolutionary mechanisms that reduce gene flow through complex interactions among ecological, historical and genomic factors. In the European anchovy ( Engraulis encrasicolus ), marine and coastal ecotypes have been identified in the northeast Atlantic and the Mediterranean Sea, yet the genomic basis of their divergence remains unclear. Here, we present the first genome-scale analysis of this species complex, integrating whole-genome sequencing (WGS) and RAD-seq data from populations spanning its distribution range. In addition to the known marine and coastal ecotypes, we identify a previously undetected lineage extending from southern Morocco, through the Canary Islands, to South Africa. This southern Atlantic lineage exhibits a gradient of admixture with northern populations near the Atlantic–Mediterranean transition zone. Genomic differentiation landscapes reveal large regions of high linkage disequilibrium, probably corresponding to 13 structural variants (SVs) segregating within or between lineages. Notably, three of the six SVs contributing to the gene flow barrier between northern ecotypes originated in the southern lineage, supporting a partially shared evolutionary history between the coastal ecotype and the southern lineage. This study highlights how SVs that arose in geographically isolated lineages can act as key genetic elements in ecotype formation, reinforcing reproductive isolation through distinct evolutionary pathways.

The house mouse, Mus musculus, is a widely used animal model in biomedical research, with classical laboratory strains (CLS) being the most frequently employed. However, the limited genetic variability in CLS hinders their applicability in evolutionary studies. Wild-derived strains (WDS), on the other hand, provide a suitable resource for such investigations. This study quantifies genetic and phenotypic data of 101 WDS representing 5 species, 3 subspecies, and 8 natural Y consomic strains and compares them with CLS. Genetic variability was estimated using whole mtDNA sequences, the Prdm9 gene, and copy number variation at two sex chromosome-linked genes. WDS exhibit a large natural variation with up to 2173 polymorphic sites in mitogenomes, whereas CLS display 92 sites. Moreover, while CLS have two Prdm9 alleles, WDS harbour 46 different alleles. Although CLS resemble M. m. domesticus and M. m. musculus WDS, they differ from them in 10 and 14 out of 16 phenotypic traits, respectively. The results suggest that WDS can be a useful tool in evolutionary and biomedical studies with great potential for medical applications.

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.

This article illustrates the potential contribution of modern techniques for analysing ancient DNA to recurrent questions concerning the origin of specimens deposited in museums, in this case that of the first described specimen of the polyspecific g...

Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multiallelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate major histocompatibility complex genes are well-established targets of long-term multiallelic balancing selection, so widespread adaptive major histocompatibility complex introgression is expected. Here, we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds, and mammals at advanced stages of speciation. The key prediction of more extensive major histocompatibility complex introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of major histocompatibility complex genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies major histocompatibility complex introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.

The formation of ecotypes is shaped by mechanisms that reduce gene flow through complex interactions between ecological, historical, and genomic factors. In the European anchovy ( Engraulis encrasicolus ), marine and coastal ecotypes have been identified in the North-East Atlantic and Mediterranean Sea, yet the genomic basis of their divergence remains unclear. Here, we present the first genome-scale analysis of this species complex, integrating whole-genome sequencing (WGS) and RAD-seq data from populations across its distribution range. In addition to the marine and coastal ecotypes, we identify a previously undetected lineage which is present in southern Morocco, the Canary Islands and even in South Africa. This southern Atlantic lineage exhibits a gradient of admixture with northern populations near the Atlantic-Mediterranean transition zone. Genomic differentiation landscapes reveal large regions of high linkage disequilibrium, likely corresponding to thirteen structural variants (SVs) segregating within or between the lineages. Notably, three of the six SVs contributing to the gene flow barrier between northern ecotypes originated in the southern lineage, supporting a partially shared evolutionary history between the coastal ecotype and the southern lineage. Our findings suggest that anchovy ecotype divergence has been shaped by a combination of ancient structural variation, admixture, and local adaptation. This study highlights how SVs that arose between geographically isolated lineages can act as key genetic elements in ecotype formation, reinforcing reproductive isolation through distinct evolutionary pathways.

Correctly delimiting species and populations is a prerequisite for studies of connectivity, adaptation and conservation. Genomic data are particularly useful to test species differentiation for organisms with few informative morphological characters or low discrimination of cytoplasmic markers, as in Scleractinians. Here we applied Restriction site Associated DNA sequencing (RAD-sequencing) to the study of species differentiation and genetic structure in populations of Pocillopora spp. from Oman and French Polynesia, with the objectives to test species hypotheses, and to study the genetic structure among sampling sites within species. We focused here on coral colonies morphologically similar to P. acuta (damicornis type β). We tested the impact of different filtering strategies on the stability of the results. The main genetic differentiation was observed between samples from Oman and French Polynesia. These samples corresponded to different previously defined primary species hypotheses (PSH), i.e., PSHs 12 and 13 in Oman, and PSH 5 in French Polynesia. In Oman, we did not observe any clear differentiation between the two putative species PSH 12 and 13, nor between sampling sites. In French Polynesia, where a single species hypothesis was studied, there was no differentiation between sites. Our analyses allowed the identification of clonal lineages in Oman and French Polynesia. The impact of clonality on genetic diversity is discussed in light of individual-based simulations.

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.

House mice ( Mus musculus ) have spread globally as a result of their commensal relationship with humans. In the form of laboratory strains, both inbred and outbred, they are also among the most widely-used model organisms in biomedical research. Although the general outlines of house mouse dispersal and population structure are well known, details have been obscured by either limited sample size or small numbers of markers. Here we examine ancestry, population structure and inbreeding using SNP microarray genotypes in a cohort of 814 wild mice spanning five continents and all major subspecies of Mus , with a focus on M. m. domesticus . We find that the major axis of genetic variation in M. m. domesticus is a south-to-north gradient within Europe and the Mediterranean. The dominant ancestry component in North America, Australia, New Zealand and various small offshore islands is of northern European origin. Next we show that inbreeding is surprisingly pervasive and highly variable, even between nearby populations. By inspecting the length distribution of homozygous segments in individual genomes, we find that inbreeding in commensal populations is mostly due to consanguinity. Our results offer new insight into the natural history of an important model organism for medicine and evolutionary biology.

Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental changes, and would be favored in variable environments. In this study, we investigated the thermal stress response in Pocillopora coral colonies from two contrasting environments by exposing them to heat stress. We compared the physiological state, bacterial and Symbiodiniaceae communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions and heat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and presented open and colored polyps during heat stress, with no change in bacterial and Symbiodiniaceae community composition. In contrast, they differed in their transcriptomic responses. The colonies from Oman displayed a more plastic transcriptome, but some genes had a higher basal expression level (frontloading) compared to the less thermotolerant colonies from New Caledonia. In terms of biological functions, we observed an increase in the expression of stress response genes (including induction of tumor necrosis factor receptors, heat shock proteins, and detoxification of reactive oxygen species), together with a decrease in the expression of genes involved in morpho-anatomical functions. Gene regulation (transcription factors, mobile elements, histone modifications and DNA methylation) appeared to be overrepresented in the Oman colonies, indicating possible epigenetic regulation. These results show that transcriptomic plasticity and frontloading can be co-occurring processes in corals confronted with highly variable thermal regimes.