Interplay between purging and admixture shapes genetic load in an invasive guppy population

Abstract

Demographic history can shape the genetic load of populations by influencing the efficacy of selection, levels of heterozygosity, and the incorporation of new variants via gene flow. Understanding these dynamics is crucial for identifying threats to population viability and predicting evolutionary trajectories of invasive populations translocated by humans into non-native environments. We investigate these processes in Trinidadian guppies (Poecilia reticulata) by estimating genetic loads across multiple populations, with a particular focus on a single expanding population in which translocated individuals have rapidly spread and replaced native individuals. Overall, we observe the expected negative relationship between neutral genetic diversity and relative genetic load. In the translocated population, patterns differ between strongly and weakly deleterious mutations. Strongly deleterious alleles are purged at the isolated translocation site but tend to accumulate along the expansion front. In contrast, the genetic load estimated based on weakly deleterious variants declines along the expansion gradient. These differing patterns can be explained by admixture with native populations (which carried fewer weakly deleterious mutations) reducing the overall genetic load of the population at the expansion front. However, admixture has also increased genetic diversity and introduced new strongly deleterious alleles, thereby reversing the purging effect. Together, our findings illustrate the complex interactions determining genetic load in subdivided populations, offering important insights into the evolutionary aspects of biological invasions.