Demographic Inference Reveals African and European Admixture in the North AmericanDrosophila melanogasterPopulation

Abstract

Drosophila melanogaster spread from sub-Saharan Africa to the rest of the world colonizing new environments. Here, we modeled the joint demography of African (Zimbabwe), European (The Netherlands), and North American (North Carolina) populations using an approximate Bayesian computation (ABC) approach. By testing different models (including scenarios with continuous migration), we found that admixture between Africa and Europe most likely generated the North American population, with an estimated proportion of African ancestry of 15%. We also revisited the demography of the ancestral population (Africa) and found-in contrast to previous work-that a bottleneck fits the history of the population of Zimbabwe better than expansion. Finally, we compared the site-frequency spectrum of the ancestral population to analytical predictions under the estimated bottleneck model. TO date, several studies have confirmed that Drosophila melanogaster originated in sub-Saharan Africa and spread to the rest of the world (Lachaise et al. 1988;David and Capy 1988;Begun and Aquadro 1993; Andolfatto 2001;Stephan and Li 2007). With its cosmopolitan distribution we expect that different populations have evolved and adapted differently to distinct environments, making D. melanogaster a perfect study system for both adaptation and population history. Extensive research has been performed to detect signatures of adaptation at the genome level (Sabeti et al. 2006;Li and Stephan 2006;Zayed and Whitfield 2008). Such detection usually depends on the underlying demographic scenario, since demographic events can leave similar patterns on the genome as adaptive (selective) events (Kim and Stephan 2002;Glinka et al. 2003;Jensen et al. 2005;Nielsen et al. 2005;Pavlidis et al. 2008Pavlidis et al. , 2010a. Therefore, a better understanding of the demography of a population will not only allow us to estimate past and present population sizes and the times of the population size changes but will also decrease the rate of false positives of signatures of adaptation. Here we study the demography of African, European, and North American populations, with an emphasis on the North American population.There is evidence that D. melanogaster colonized North America ,200 years ago (Johnson 1913;Sturtevant 1920;Keller 2007). D. melanogaster (then known as D. ampelophila) was first reported in New York in 1875 by New York State entomologist Lintner (Lintner 1882;Keller 2007). In the year 1879 several articles were published indicating the appearance of D. melanogaster in several parts of eastern North America, including Connecticut and Massachusetts (Johnson 1913). At that time the dipteran fauna was very well described. It is therefore unlikely that entomologists would have overlooked D. melanogaster for long (Keller 2007). Less than 25 years after its introduction, D. melanogaster became the most common dipteran species in North America (Howard 1900). Johnson (1913) suggested that North America could have been colonized from the tropics, since the fir...

Effects of Linked Selective Sweeps on Demographic Inference and Model Selection

“…It is therefore reasonable to assume that positive selection could have a substantial confounding effect on a variety of population genomic methods for demographic inference in practice, beyond those considered here. In the empirical literature, numerous recent studies of demographic history have found support for contractions and recent expansions of natural populations (Thornton and Andolfatto 2006;Fagundes et al 2007;Gravel et al 2011;Tennessen et al 2012;Duchen et al 2013). While such population size changes are probably common, and our results do not call the major findings of these studies into question, they do suggest that natural selection can exaggerate the inferred intensity of these changes.…”

“…In addition, C and D of Figure S8 suggest that the extent of exponential growth during the recovery phase is underestimated when very recent sweeps have occurred. Thus, we find that positive selection can dramatically skew population size histories deduced by PSMC.Positive selection produces spurious support for nonequilibrium demographic historiesDemographic inference methods are often used not only to infer parameters of a model, but increasingly to select the best fitting among several competing models (e.g., Adams and Hudson 2004;Fagundes et al 2007;Duchen et al 2013).To ask whether positive selection might affect the outcome of demographic model selection, we simulated genomes with constant population size, again sampling loci for which some fraction, f, is located within c/s # 1 of a selective sweep. We then performed model selection among our four demographic histories ( Figure 1) using both @a@i and ABC (Methods).…”

“…Demographic inference methods are often used not only to infer parameters of a model, but increasingly to select the best fitting among several competing models (e.g., Adams and Hudson 2004;Fagundes et al 2007;Duchen et al 2013).…”

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

“…This species originated in sub-Saharan Africa, and approximately 10,000-15,000 years ago a subpopulation expanded out of the ancestral range. During this expansion, the derived subpopulation experienced a population bottleneck that resulted in decreased nucleotide polymorphism, extended linkage disequilibrium within the derived population and substantial genetic differentiation between ancestral and derived populations [2,[35][36][37][38][39]. Hereafter, the ancestral population will be referred to as "African" and the derived population as "Cosmopolitan".…”

“…Following this bottleneck, descendant populations of African and Cosmopolitan D. melanogaster have admixed in numerous geographic regions [2,11,21]. Of particular relevance to this work, North America was colonized recently by a population descendent from African individuals from the South, and by a population descendent from cosmopolitan D. melanogaster in the North [11,21,38]. Where these populations encountered each other in eastern North America, they form an ancestry cline where southern populations have a greater contribution of African ancestry than northern populations [21].…”