Recurrant collection of Drosophila melanogaster from wild African environments and genomic insights into species history

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.