Multigenerational hybridisation results in heterosis and facilitates adaptive introgression, with no evidence of outbreeding depression in a pair of marine gastropods

Abstract

Anthropogenic environmental changes continue to threaten species globally. On the one hand, anthropogenic movement of species has caused unintentional hybridisation, which has contributed to species declines. On the other hand (more recently), hybridisation has been viewed as a way to increase the evolutionary potential of species vulnerable to rapid environmental change. However, the benefits of mixing genetically divergent lineages do not come without risks to individual fitness and the long-term viability of populations. Here, we use a combination of genome-wide Single Nucleotide Polymorphism (SNP) markers, mitochondrial DNA sequencing and measurements of growth rate to determine the long-term genetic consequences of hybridisation between two congeneric marine gastropods. Multigeneration hybridisation resulted from the introduction of the intertidal periwinkle Bembicium vittatum (a direct developer) into the native range of its congener Bembicium auratum (a species with planktotrophic larval dispersal). Despite significant genetic divergences between the species, we found no direct evidence of outbreeding depression in the admixed population. Instead, we found evidence for heterosis, which dissipated over time. After an initial lag, the frequency of introduced B. vittatum alleles declined dramatically in the hybrid population, however, a few B. vittatum alleles (3.18%) increased significantly in frequency against the overall trend, providing evidence of adaptive introgression. In the context of hybridisation as a conservation management tool, our results provide some evidence of the potential benefits that can be gained and suggest that the costs due to outbreeding depression can be small.