Connectivity and selfing drives population genetic structure in a patchy landscape: a comparative approach of four co-occurring freshwater snail species

Abstract

The distribution of neutral genetic variation in subdivided populations is driven by the interplay between genetic drift, migration, local extinction and colonization. The influence of environmental and demographic factors has also been increasingly examined in empirical studies, but generally focusing on a single species. An open question is whether these factors will similarly, or idiosyncratically, affect a guild of species occupying the same, though exhibiting different traits, mating systems and histories. We addressed it by comparing the population genetic structure of the four most common species of hermaphroditic freshwater snails in Guadeloupe (Lesser Antilles), which occupy a network of patchily distributed sites experiencing temporal variation in water availability. We analyzed microsatellite variability in 21 to 43 populations per species, and built predictions on how several environmental and demographic variables, quantified from a long-term annual survey, as well as species traits, may affect the distribution of genetic variation. These species displayed similarities, such as fairly high levels of variation, but with marked differences among sites, as well as strong genetic differentiation and limited isolation by distance, which can be explained by passive dispersal (strong role of site connectivity), extinction/colonization dynamics and variation in local population size. They also exhibit differences, largely due to the mating system with less genetic diversity and more genetic differentiation in the two selfing species when compared to the two outcrossing ones. These differences can also be attributed to interspecific interactions resulting from the ongoing invasion of Guadeloupe by one of the species studied, which affects the demography of other species, and, to a limited extent, to local environmental factors. Our comparative approach shows both differences and uniqueness in the way species occupy the same landscape, and provides a possible entry to interspecific interactions in community assembly.