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Recurrent Collection of Drosophila melanogaster from Wild African Environments and Genomic Insights into Species History.

ABSTRACT: A long-standing enigma concerns the geographic and ecological origins of the intensively studied vinegar fly, Drosophila melanogaster. This globally distributed human commensal is thought to originate from sub-Saharan Africa, yet until recently, it had never been reported from undisturbed wilderness environments that could reflect its precommensal niche. Here, we document the collection of 288 D. melanogaster individuals from multiple African wilderness areas in Zambia, Zimbabwe, and Namibia. The presence of D. melanogaster in these remote woodland environments is consistent with an ancestral range in southern-central Africa, as opposed to equatorial regions. After sequencing the genomes of 17 wilderness-collected flies collected from Kafue National Park in Zambia, we found reduced genetic diversity relative to town populations, elevated chromosomal inversion frequencies, and strong differences at specific genes including known insecticide targets. Combining these genomes with existing data, we probed the history of this species' geographic expansion. Demographic estimates indicated that expansion from southern-central Africa began ∼10,000 years ago, with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,400 years ago. This improved model of demographic history will provide an important resource for future evolutionary and genomic studies of this key model organism. Our findings add context to the history of D. melanogaster, while opening the door for future studies on the biological basis of adaptation to human environments.

SUBMITTER: Sprengelmeyer QD

PROVIDER: S-EPMC7038662 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Drosophila melanogaster has played a pivotal role in the development of modern population genetics. However, many basic questions regarding the demographic and adaptive history of this species remain unresolved. 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 within an African population, between African populations, and between European and African populations. A disproportionate number of candidate selective sweep regions were located near genes with varied roles in gene regulation. Outliers for Europe-Africa F(ST) 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.

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Recurrent Collection of Drosophila melanogaster from Wild African Environments and Genomic Insights into Species History.

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