Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the south‐eastern United States and Caribbean Islands

Abstract

Drosophila melanogaster is postulated to have colonized North America in the past several 100 years in two waves. Flies from Europe colonized the east coast United States while flies from Africa inhabited the Caribbean, which if true, make the south-east US and Caribbean Islands a secondary contact zone for African and European D. melanogaster. This scenario has been proposed based on phenotypes and limited genetic data. In our study, we have sequenced individual whole genomes of flies from populations in the south-east US and Caribbean Islands and examined these populations in conjunction with population sequences from the west coast US, Africa, and Europe. We find that west coast US populations are closely related to the European population, likely reflecting a rapid westward expansion upon first settlements into North America. We also find genomic evidence of African and European admixture in south-east US and Caribbean populations, with a clinal pattern of decreasing proportions of African ancestry with higher latitude. Our genomic analysis of D. melanogaster populations from the south-east US and Caribbean Islands provides more evidence for the Caribbean Islands as the source of previously reported novel African alleles found in other east coast US populations. We also find the border between the south-east US and the Caribbean island to be the admixture hot zone where distinctly African-like Caribbean flies become genomically more similar to European-like south-east US flies. Our findings have important implications for previous studies examining the generation of east coast US clines via selection.

Revisiting classic clines in Drosophila melanogaster in the age of genomics

“…Importantly, parallelism is found even among less-differentiated alleles in North American and Australian populations of D. melanogaster , suggesting that many polymorphic sites are targets of clinal selection [52] (Figure 2). One cautionary note is that migrants from Europe or Africa founded the North American and Australian populations, likely bringing along both the high- and low-latitude adapted alleles [55]. Therefore, any neutral variants linked to the causal variants in the migrant population could also show patterns of clinal selection simply because of their proximity to recently selected sites.…”

Postmating reproductive barriers contribute to the incipient sexual isolation of the United States and Caribbean Drosophila melanogaster

“…2010; Kao et al. 2015), recently came into secondary contact (Bergland et al. 2014) via two waves of colonization: west African flies migrating to the Caribbean Islands during the transatlantic slave trade 400–500 years ago, and then the European flies arriving to the east coast United States with the agency of European colonists <200 years ago (Capy et al.…”

“…1986; Caracristi and Schlötterer 2003; Yukilevich and True 2008a; Kao et al. 2015). Sequence data also suggest that the United States flies display a higher proportion of African alleles than do European flies, suggesting Caribbean populations as a potential source of African alleles introgression for North America populations (Capy et al.…”

“…2010; Kao et al. 2015). Mating preferences and other premating/prezygotic reproductive barriers have been formally treated in this system, showing partial sexual isolation between west African flies and American flies, but not Caribbean flies (Yukilevich and True 2008a,b).…”

“…By looking at these roles, we provide general insight into how these isolating mechanisms arise in a genetically admixed system (Kao et al. 2015). …”