Beyond genetic indicators: how reproductive mode and hybridization challenge freshwater mussel conservation

Abstract

Genetic diversity is a fundamental component of biodiversity that should be monitored and preserved. Unionid freshwater mussels provide essential ecosystem services but are among the most imperilled aquatic organisms worldwide. Here, we assess key genetic Essential Biodiversity Variables (EBVs)--genetic diversity, genetic differentiation, inbreeding, and effective population size--in all Anodonta species in Switzerland. After generating draft genomes for Anodonta cygnea and Anodonta anatina, we performed whole-genome resequencing of 421 individuals (243 A. anatina, 151 A. cygnea, 17 A. exulcerata and 10 Anodonta sp.) from 31 populations. While A. anatina populations followed a metapopulation structure shaped by catchment areas, genetic diversity correlated positively with waterbody size, suggesting greater vulnerability in small ponds compared with large lakes. Inbreeding levels were low, however effective population sizes were consistently below 100, indicating serious extinction risks. We also detected hybridization between A. cygnea and A. exulcerata, indicating genomic permeability between these species. Furthermore, genomic data suggested facultative selfing in A. cygnea, leading to a marked reduction in genetic diversity, increased population structure and inbreeding, and a decline in effective population size compared to the outcrossing A. anatina, emphasizing that A. cygnea faces a particularly high risk of extinction due to its reproductive strategy. Our study reveals the vulnerability of freshwater mussels and emphasizes the need for genetic indicators to reflect species-specific reproductive strategies. More broadly, it calls for conservation policies to integrate genetic monitoring and consider reproductive modes to tailor conservation efforts and better assess extinction risks.