Limited population structure but signals of recent selection in introduced African Fig Fly (Zaprionus indianus) in North America

Abstract

Invasive species have devastating consequences for human health, food security, and the environment. Many invasive species adapt to new ecological niches following invasion, but little is known about the early steps of adaptation. Here we examine population genomics of a recently introduced drosophilid in North America, the African Fig Fly, Zaprionus indianus. This species is likely intolerant of subfreezing temperatures and recolonizes temperate environments yearly. We generated a new chromosome-level genome assembly for Z. indianus. Using resequencing of over 200 North American individuals collected over four years in temperate Virginia, plus a single collection from subtropical Florida, we tested for signatures of population structure and adaptation within invasive populations. We show founding populations are sometimes small and contain close genetic relatives, yet temporal population structure and differentiation of populations is mostly absent across North America. However, we identify two haplotypes that are differentiated between African and invasive populations and show signatures of selective sweeps. Both haplotypes contain genes in the cytochrome P450 pathway, indicating these sweeps may be related to pesticide resistance. X chromosome evolution in invasive populations is strikingly different from the autosomes, and a haplotype on the X chromosome that is highly differentiated between Virginia and Florida populations is a candidate for temperate adaptation. These results show that despite limited population structure, populations may rapidly evolve genetic differences early in an invasion. Further uncovering how these genomic regions influence invasive potential and success in new environments will advance our understanding of how organisms evolve in changing environments. Article SummaryInvasive species (organisms that have been moved outside their natural range by human activities) can cause problems for both humans and the environment. We studied the genomes of over 200 individuals of a newly invasive fruit fly in North America, the African Fig Fly. We found genetic evidence that these recently introduced flies may be evolving in their new environments, which could make them stronger competitors and more likely to become pests.