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

Abstract

<jats:title>Abstract</jats:title> <jats:p>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 ∼13,000 years ago, with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,800 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.</jats:p>

Demographic analyses of a new sample of haploid genomes from a Swedish population of Drosophila melanogaster

“…Naturally, the use of a larger mutation rate and a shorter generation time yields smaller population sizes and younger ages for the split between the ancestral lineages of the European and African samples (T split = 4,139 years) as well as the African expansion (13,032 years, Table 1 ). Similar results have been recently published by Sprengelmeyer, et al 38 and altogether suggest that the spread of populations outside their center of origin may have coincided with the Neolithic demographic transition. Estimates using X-chromosomal data are markedly different from autosomal data, which likely reflects selective processes specifically affecting sex-chromosomes 39 .…”

Temperature, rainfall and wind variables underlie environmental adaptation in natural populations of Drosophila melanogaster

“…In addition, llili has been suggested to have a role in local adaptation, as it was recently reported to be part of a strong outlier region in a study comparing D . melanogaster collected in wilderness areas and collected in the nearby of towns in southern‐central Africa (Sprengelmeyer et al, 2020). FBti0018880 showed the second strongest association also with temperature, Isothermality (temperature variability index), and has been reported to play a role in oxidative stress response (Guio et al, 2014).…”

“…Drosophila melanogaster is a valuable model organism to study environmental adaptation. This species originated from Southern Africa and has recently expanded worldwide colonizing a wide range of environmental conditions (12,000–19,000 years ago; Arguello et al, 2019; Pool et al, 2012; Sprengelmeyer et al, 2020). In addition, this species offers many key advantages as it has a small and well‐annotated genome which facilitates the identification of putatively adaptive loci (Mohr et al, 2014), as well as a short lifecycle implying many generations in short periods of time (15 generations per year in nature; Pool, 2015).…”

Influence of the large–Z effect during contact between butterfly sister species

“…Although data for N e is unavailable for the species in Fig. 1, we can obtain a rough idea of how N e varies over time and among species from the study of Heliconius populations by van Belleghem et al [3] (for Drosophila, see [19]). interest is the index value F A 0.15, the smallest value of F A for different species (yellow and green data points) in Fig.…”