Abstract Horizontal transfer of genetic material in eukaryotes has rarely been documented over short evolutionary timescales. Here, we show that two retrotransposons,ShellderandSpoink, invaded the genomes of multiple species of themelanogastersubgroup within the last 50 years. Through horizontal transfer,Spoinkspread inD. melanogasterduring the 1980s, while bothShellderandSpoinkinvadedD. simulansin the 1990s. Possibly following hybridization,D. simulansinfected the island endemic speciesD. mauritiana(Mauritius) andD. sechellia(Seychelles) with both TEs after 1995. In the same approximate time-frame,Shellderalso invadedD. teissieri, a species confined to sub-Saharan Africa. We find that the donors ofShellderandSpoinkare likely AmericanDrosophilaspecies from thewillistoni,cardini, andrepletagroups. Thus, the described cascade of TE invasions could only become feasible afterD. melanogasterandD. simulansextended their distributions into the Americas 200 years ago, likely aided by human activity. Our work reveals that cascades of TE invasions, likely initiated by human-mediated range expansions, could have an impact on the genomic and phenotypic evolution of geographically dispersed species. Within a few decades, TEs could invade many species, including island endemics, with distributions very distant from the donor of the TE.
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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.
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- Award ID(s):
- 1737752
- PAR ID:
- 10161728
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 37
- Issue:
- 3
- ISSN:
- 0737-4038
- Page Range / eLocation ID:
- 627 to 638
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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