The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study "replicated" instances of secondary contact between closely-related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry-informative panel of such SNPs. We then compared their frequencies in newly-sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bistable variants (Dobzhansky-Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact.

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

The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic-Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels. AbstractThe 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, and both facts can explain 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 with 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 the two lineages can live in sympatry with ample opportunities to interbreed in a large area, but hardly do. This implies 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 an 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 natural barriers mostly explain the position of genetic breaks while their maintenance must additionally require genetic barriers.

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.

Molecular approaches have proven efficient to identify cryptic lineages within single taxonomic entities. Sometimes these cryptic lineages maybe previously unreported or unknown invasive taxa. The genetic structure of the marine gastropod Stramonita haemastoma has been examined in the Western Mediterranean and North‐Eastern Atlantic populations with mtDNA COI sequences and three newly developed microsatellite markers. We identified two cryptic lineages, differentially fixed for alternative mtDNA COI haplogroups and significantly differentiated at microsatellite loci. The mosaic distribution of the two lineages is unusual for a warm‐temperate marine invertebrate with a teleplanic larval stage. The Atlantic lineage was unexpectedly observed as a patch enclosed in the north of the Western Mediterranean Sea between eastern Spain and the French Riviera, and the Mediterranean lineage was found in Macronesian Islands. Although cyto‐nuclear disequilibrium is globally maintained, asymmetric introgression occurs in the Spanish region where the two lineages co‐occur in a hybrid zone. A first interpretation of our results is mito‐nuclear discordance in a stable postglacial hybrid zone. Under this hypothesis, though, the location of genetic discontinuities would be unusual among planktonic dispersers. An alternative interpretation is that the Atlantic lineage, also found in Senegal and Venezuela, has been introduced by human activities in the Mediterranean area and is introgressing Mediterranean genes during its propagation, as theoretically expected. This second hypothesis would add an additional example to the growing list of cryptic marine invasions revealed by molecular studies.

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