Bottlenecked but Booming: Strong Inbreeding in a Highly Invasive Freshwater Mussel.

Abstract

The 'genetic paradox of invasions' refers to successful invasive populations originating from low founder numbers. Theory predicts that such invaders should exhibit reduced genetic diversity and increased inbreeding, which should restrict their evolutionary potential and often lead to inbreeding depression. Here, we provide evidence for an invader succeeding against these odds by demonstrating strikingly strong inbreeding in a highly successful, invasive freshwater mussel. Using whole-genome resequencing data, we show that zebra mussels (Dreissena polymorpha) from thriving invasive populations carry numerous and long runs of homozygosity (ROH) in their genomes, reflecting severe, sequential founder events followed by inbreeding during the invasion process. Additionally, predicted genetic load (accumulation of deleterious mutations) is correlated with inbreeding levels: more inbred invasive populations exhibit lower masked (i.e., heterozygous) but higher realised (i.e., homozygous) load compared to less inbred populations. These genomic consequences of inbreeding would be expected to decrease the fitness of invasives, but here have not prevented their success. Our study thus challenges conventional expectations that inbreeding and high numbers of putatively deleterious alleles should limit biological invasion success. This research provides a compelling example of an invader that defies genetic expectations, and is therefore broadly relevant for understanding invasion success and dynamics across taxa.