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

Genetic diversity is a fundamental aspect of biodiversity, yet it is rarely assessed and monitored in conservation practice. Unionid freshwater mussels exemplify the dramatic loss of biodiversity in freshwater ecosystems, yet genomic data for these ecologically important species remain scarce. Here, we conducted a high-resolution population genomics study of all Anodonta species in Switzerland, with a focus on two species with contrasting reproductive strategies. After generating draft genomes of the hermaphroditic Anodonta cygnea and the gonochoric Anodonta anatina, we performed whole-genome resequencing of 421 individuals from four Anodonta species collected in 31 localities. 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. Furthermore, we detected hybridization between A. cygnea and A. exulcerata, indicating genomic permeability between these species. In addition, 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. Our study underscores that reproductive strategy fundamentally shapes genetic indicators of biodiversity and influences extinction risk; conservation targets should therefore be adapted to the biology of the species of interest. To conclude, we advocate for integrating reproductive mode and genomic data into conservation planning to more accurately assess vulnerability and guide effective action.

This data package contains the three filtered vcf files, the COI alignment of all mussels, the genome assemblies used as references for mapping, as well as the metadata associated with the study. The raw reads for this study have been deposited in the European Nucleotide Archive (ENA) at EMBL-EBI under accession number PRJEB86155 (https://www.ebi.ac.uk/ena/browser/view/PRJEB86155)