Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture

TL;DR

This study sequenced genomes of 139 Drosophila melanogaster strains from sub-Saharan Africa and Europe, revealing extensive non-African admixture in Africa, regional diversity patterns, and genomic regions under positive selection.

Contribution

It introduces a novel admixture detection method and provides comprehensive insights into African D. melanogaster diversity, admixture patterns, and adaptive evolution.

Findings

Widespread non-African admixture in African populations.

Highest genetic diversity observed in southern Africa.

Identification of genomic regions under positive selection near regulatory genes.

Abstract

(ABRIDGED) We report the genome sequencing of 139 wild-derived strains of D. melanogaster, representing 22 population samples from the sub-Saharan ancestral range of this species, along with one European population. Most genomes were sequenced above 25X depth from haploid embryos. Results indicated a pervasive influence of non-African admixture in many African populations, motivating the development and application of a novel admixture detection method. Admixture proportions varied among populations, with greater admixture in urban locations. Admixture levels also varied across the genome, with localized peaks and valleys suggestive of a non-neutral introgression process. Genomes from the same location differed starkly in ancestry, suggesting that isolation mechanisms may exist within African populations. After removing putatively admixed genomic segments, the greatest genetic diversity was observed in southern Africa (e.g. Zambia), while diversity in other populations was largely consistent with a geographic expansion from this potentially ancestral region. The European population showed different levels of diversity reduction on each chromosome arm, and some African populations displayed chromosome arm-specific diversity reductions. Inversions in the European sample were associated with strong elevations in diversity across chromosome arms. Genomic scans were conducted to identify loci that may represent targets of positive selection. A disproportionate number of candidate selective sweep regions were located near genes with varied roles in gene regulation. Outliers for Europe-Africa FST were found to be enriched in genomic regions of locally elevated cosmopolitan admixture, possibly reflecting a role for some of these loci in driving the introgression of non-African alleles into African populations.