Genetic Correlates of Host Use in Scotland's Pearl Mussels
The freshwater pearl mussel (Margaritifera margaritifera) is an ecologically important and highly endangered bivalve native to running freshwaters across Europe and eastern North America. Its life cycle includes an obligate parasite stage in which newly emerged larvae attach to the gills of juvenile salmonid fishes. In northern Europe, populations specialize on one of two hosts: Atlantic salmon (Salmo salar) or brown trout (S. trutta). Previous microsatellite studies of pearl mussels in the Nordic region have shown an association between host specialization and population genetic characteristics. Scotland is considered a remaining stronghold for freshwater pearl mussel, however current knowledge of genetic characteristics and host association of Scottish M. margaritifera populations is limited. We combined minimally-invasive viscera swabbing with reduced-representation sequencing (nextRAD) to examine genetic diversity of pearl mussels at 5,486 genome-wide SNP markers across 18 populations in Scotland. Our results revealed a substantial variation among populations in genetic diversity and interpopulation differentiation which was strongly related to known host. Populations known to specialize on Atlantic salmon exhibited high genetic diversity (mean He = 0.24) and low inter-population differentiation (Fst = 0.026), even between rivers draining to opposite coasts. In contrast, populations known to specialize on brown trout or occurring where only trout are available consistently showed lower genetic diversity (mean He = 0.15 /0.14) and much higher inter-population differentiation (Fst = 0.160 /0.271), with many populations being highly genetically distinct even when geographically proximate. Principal component analysis and neighbor-joining trees confirmed this pattern, with salmon-specialist populations clustering together while trout-associated populations formed discrete, population-specific clusters. These findings mirror previously observed patterns in other parts of the M. margaritifera range and indicate that population sizes and migratory behavior of hosts may drive contrasting evolutionary trajectories in pearl mussel populations. The striking genetic differences between salmon- and trout-specialist populations have important implications for conservation planning, as they indicate differential capacity for local adaptation and vulnerability to reduced population sizes. Our results suggest that population genetic characteristics could be used to predict host associations for unstudied populations, providing a valuable tool for conservation management. The study emphasizes the importance of considering both direct impacts on pearl mussel populations and the status of their salmonid hosts when developing conservation strategies for this rapidly declining species.