Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

Abstract

Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4,279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry‐informative markers. We identified a type of introduced mussels, called “dock mussels,” associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early‐stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.

An evolutionary perspective on marine invasions

“…The contribution by Simon et al (2019) advances understanding of the evolutionary mechanisms behind anthropogenic hybridization. The authors studied hybridization between native species and species introduced by shipping.…”

How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels

“…Reference populations were defined on previous knowledge of the M. edulis species complex (Fraïsse, Gunnarsson, Roze, Bierne, & Welch, 2016;Simon et al, 2019). We used three levels of differentiation representing the species level (L1), the ocean basin or continent (L2) and regional groupings (L3) ( Table 1).…”

“…A more stringent filtration was additionally applied to the edu_am population when used as a reference, given the presence of European ancestry in the Long Island Sound (populations 15 and 16, Figure S10, also described in Simon et al, 2019). Filtering yielded 514 individuals genotyped at 212 markers.…”

“…We used a partial genetic map produced in Simon et al (2019) based on an F2 cross between Mediterranean M. galloprovincialis and M. edulis, genotyped at a subset of the markers studied here (Bierne, Bonhomme, Boudry, Szulkin, & David, 2006;Bierne, David, Boudry, & Bonhomme, 2002;Simon, Bierne, & Welch, 2018). In addition to this genetic map, we extrapolated genetic distances from physical distance for markers present on the same contig using a recombination rate of 2 cM/Mb (rounded from the estimate in Bierne, 2010).…”

“…The study of enhanced introgression in one population, when compared to a reference parental population (sometimes called 'local introgression', Fraïsse, Belkhir, Welch, and Bierne, 2016) is an efficient approach to isolating the effect of introgression from other factors (Green et al, 2010;Martin, Davey, & Jiggins, 2015). In addition, the study of multiple cases of contact between similar lineages allows us to study the effect of the same barrier in multiple demographic and ecological contexts (Abbott et al, 2013), and to test the repeatability of introgression patterns (Harrison & Larson, 2016;Simon et al, 2019).…”