Repeated signatures of balancing selection in small and large populations of guppies (Poecilia reticulata)

Abstract

Balancing selection is a powerful evolutionary force that maintains adaptive genetic and phenotypic diversity. Although methods to detect the footprints of balancing selection in genomic data have advanced, we still lack a clear understanding of how repeatable these signatures appear in wild populations, and how this repeatability is shaped by demographic history and existing genetic variation. The Trinidadian guppy (Poecilia reticulata) provides an ideal model to test the repeatability of balancing selection in the wild as there is strong evidence that negative frequency-dependent selection (NFDS) maintains colour polymorphism. Analysing whole-genome sequencing data from 11 guppy populations (n = 195) with contrasting demographic contexts, we apply scans of balancing selection to explore which genomic regions show evidence of repeatability. We find that populations with small Ne show less genetic repeatability but still exhibit population-specific regions of elevated diversity, implicating independent balancing selection or other evolutionary mechanisms. Despite this, we identify 23 regions with repeated signatures of balancing selection, including a region on LG22 containing genes involved in colour, vision, mate choice, and social behaviour. Investigating the repeatability of balancing selection in small and large populations improves our knowledge of how demographic factors interact with selective processes to shape natural variation.