Discovery ofDrosophila melanogasterfrom 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, a globally widespread species [1] which "has invariably appeared to be a strict human commensal" [2]. In spite of its sub-Saharan origins, this species has never been reported from undisturbed wilderness environments that might reflect its pre-commensal niche [3]. Here, we document the collection of 288 D. melanogaster individuals from African wilderness areas in Zambia, Zimbabwe, and Namibia. After sequencing the genomes of 17 flies collected from Kafue National Park, 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 new genomes with prior data enabled us to gain novel insights into the history of this species' geographic expansion. Our demographic estimates indicated that an expansion from southern Africa began approximately 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 a critical resource for future evolutionary and genomic studies of this key model organism. Our results add historical context to the species' human association, and the opportunity to study wilderness populations opens the door for future studies on the biological basis of its adaptation to human environments. RESULTS AND DISCUSSIONDrosophila melanogaster persists in African wilderness D. melanogaster is among the most intensivelystudied species in the world, and yet it remains "among the commonest species whose exact place of origin and even ancestry have never been satisfactorily explained" [2]. Its relatives are distributed across sub-Saharan Africa and nearby islands, and a biogeographic analysis proposed an ancestral range in western and central Africa [3]. Despite considerable efforts to collect D. melanogaster from this equatorial region, it was never discovered in undisturbed wilderness, instead occurring only in human-settled areas and "seminatural habitats" [3]. However, a recent population genomic analysis suggested that D. melanogaster originated in southern Africa: populations from Zambia and Zimbabwe have the species' highest levels of genetic variation, whereas other populations may have lost diversity due to founder event bottlenecks during geographic expansion [4]. These findings raise the possibility that D. melanogaster originated (and might still persist) in wild environments of southern-central Africa, which are primarily characterized by seasonally dry Miombo and Mopane woodlands [5]. Although D. melanogaster has occasionally been sampled from human settlements near natural areas in Zimbabwe [6,7], its hypothesized persistence in wild Miombo/ Mopane forests [4] remains unconfirmed. Sprengelmeyer 1 ARTICLES PREPRINTHere, we report the collection of D. melanogaster in five distinct...

Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit

“…At $9,500 years ago, marula harvesting reached massive proportions, finally ebbing out $8,000 years ago [7]. These dates coincide with demographic data from D. melanogaster, which point to a within-Africa expansion starting $10,000 years ago [9,31], an expansion presumably representing the dispersal of the commensal population throughout its new niche. In short, archeological and demographic data would support the notion that marula use by the San may have been a factor in turning the woodland species D. melanogaster into the cosmopolitan species of today ( Figure 4E).…”

“…Southern Africa, we refer interested readers to an accompanying paper [9]. We next provided the forest flies with a choice of marula versus orange, the favorite breeding substrate of domestic D. melanogaster [5].…”

“…The distribution pattern of D. melanogaster in the Matopos hence indicates niche confinement and, in turn, a specialized lifestyle. D. melanogaster as a seasonal fruit specialist would actually not be surprising given (1) the scarcity of the species in Miombo and Mopane forests outside of marula season [9], (2) the observed presence of a distinct egg-laying preference [5], and (3) the fact that host specialization is a prevalent feature in the melanogaster subgroup. Drosophila sechellia exclusively breeds in noni fruit [10], whereas Drosophila erecta and Drosophila orena are seasonal specialists on Pandanus cones [2] and Syzygium waterberries [11] respectively.…”

“…Nucleotide diversity of flanking sequences, which should accrue on the order of 4 Ne z 10 million generations in this species, is at or above typical levels among Zambia haplotypes carrying this deletion ( Figure S3B). Hence, it is likely that the fusion variant existed well before the species expanded beyond its ancestral range on the order of 150,000 generations ago, or $10,000 years ago [9,31]. In contrast, putatively ancestral full-length Or22a/Or22b haplotypes from Zambia show strongly reduced diversity across the deletion region ( Figure S3B).…”

“…Genetic variation at olfactory receptor genes was analyzed based on previously-sequenced, town-collected population samples [38] and newly-sequenced genomes from Kafue National Park [9]. Sub-Saharan population samples with at least 10 sequenced genomes were included, in addition to population samples from Egypt and France.…”