Non-African Populations of Drosophila melanogaster Have a Unique Origin

The nonrecombining Drosophila melanogaster Y chromosome is heterochromatic and has few genes. Despite these limitations, there remains ample opportunity for natural selection to act on the genes that are vital for male fertility and on Y factors that modulate gene expression elsewhere in the genome. Y chromosomes of many organisms have low levels of nucleotide variability, but a formal survey of D. melanogaster Y chromosome variation had yet to be performed. Here we surveyed Y-linked variation in six populations of D. melanogaster spread across the globe. We find surprisingly low levels of variability in African relative to Cosmopolitan (i.e., non-African) populations. While the low levels of Cosmopolitan Y chromosome polymorphism can be explained by the demographic histories of these populations, the staggeringly low polymorphism of African Y chromosomes cannot be explained by demographic history. An explanation that is entirely consistent with the data is that the Y chromosomes of Zimbabwe and Uganda populations have experienced recent selective sweeps. Interestingly, the Zimbabwe and Uganda Y chromosomes differ: in Zimbabwe, a European Y chromosome appears to have swept through the population.T HE Drosophila melanogaster Y chromosome is highly functionally specialized in male-related activities (Hardy et al. 1981;Kennison 1981;Goldstein et al. 1982). Although it comprises 13% of the male genome (40 Mb;Hoskins et al. 2002), the D. melanogaster Y chromosome has only 13 known protein-coding genes (Goldstein et al. 1982;Carvalho et al. 2000Carvalho et al. , 2001Vibranovski et al. 2008;Krsticevic et al. 2010), all thought to be active only in primary spermatocytes in the testis (Hardy et al. 1981). The remainder of the Y chromosome is heterochromatic and dense in repetitive elements (Hoskins et al. 2002).Although the D. melanogaster Y chromosome is highly repetitive and gene poor, several lines of evidence suggest that it harbors functionally important variation (Chippindale and Rice 2001;Rohmer et al. 2004;Lemos et al. 2008;Lemos et al. 2010). The Y chromosome has contributed to variation in thermotolerance across D. melanogaster populations (Rohmer et al. 2004), has epistatic effects on male fitness (Chippindale and Rice 2001), and has epigenetic effects on the expression of genes across the genome (Lemos et al. 2008Jiang et al. 2010), including specifically in the male germline (Zhang 2000). The functional variation on the Y chromosome has been somewhat of a paradox because, while there is evidence for structural polymorphism (Lyckegaard and Clark 1989), the haploid transmission of the Y chromosome makes it far more difficult to maintain substantial levels of genetic variation (Clark 1987). In one small survey of Y chromosomal variation in a protein-coding gene, kl-5 (DhcYh3), only a single segregating site was discovered in 11 lines of D. melanogaster and no variants were found in 10 lines of Drosophila simulans (Zurovcova and Eanes 1999). A more recent study in a closely related species, D. simulans,...

Section: Population Structuresupporting

confidence: 87%

Section: Population Structuresupporting

confidence: 84%

Surprising Differences in the Variability of Y Chromosomes in African and Cosmopolitan Populations ofDrosophila melanogaster

Larracuente

Clark

2013

“…Our simulations predict a pooling effect over a wide range of migration rates, implying one way to test the null hypothesis of panmixia, i.e., that the genealogies of local samples are indistinguishable from those of scattered samples. Very few published studies have performed separate analyses of local population samples and the pooled sample consisting of several local samples, but many studies can, in principle, be used to test our predictions because several local samples have been included [Drosophila (Baudry et al 2004(Baudry et al , 2006Nolte and Schlö tterer 2008), humans (Marth et al 2004;Voight et al 2005;Keinan et al 2007;Garrigan et al 2007), and plants (Heuertz et al 2006;Pyhäjärvi et al 2007)]. Pool and Aquadro (2006) demonstrated the pooling effect in sub-Saharan D. melanogaster, as have several studies in plants (Ingvarsson 2005;Arunyawat et al 2007;Moeller et al 2007) and humans (e.g., Ptak and Przeworski 2002;Hammer et al 2003).…”

Section: Discussionmentioning

confidence: 99%

The Impact of Sampling Schemes on the Site Frequency Spectrum in Nonequilibrium Subdivided Populations

Städler

Haubold

Merino³

et al. 2009

199

296

Using coalescent simulations, we study the impact of three different sampling schemes on patterns of neutral diversity in structured populations. Specifically, we are interested in two summary statistics based on the site frequency spectrum as a function of migration rate, demographic history of the entire substructured population (including timing and magnitude of specieswide expansions), and the sampling scheme. Using simulations implementing both finite-island and two-dimensional stepping-stone spatial structure, we demonstrate strong effects of the sampling scheme on Tajima's D (D T ) and Fu and Li's D (D FL ) statistics, particularly under specieswide (range) expansions. Pooled samples yield average D T and D FL values that are generally intermediate between those of local and scattered samples. Local samples (and to a lesser extent, pooled samples) are influenced by local, rapid coalescence events in the underlying coalescent process. These processes result in lower proportions of external branch lengths and hence lower proportions of singletons, explaining our finding that the sampling scheme affects D FL more than it does D T . Under specieswide expansion scenarios, these effects of spatial sampling may persist up to very high levels of gene flow (Nm . 25), implying that local samples cannot be regarded as being drawn from a panmictic population. Importantly, many data sets on humans, Drosophila, and plants contain signatures of specieswide expansions and effects of sampling scheme that are predicted by our simulation results. This suggests that validating the assumption of panmixia is crucial if robust demographic inferences are to be made from local or pooled samples. However, future studies should consider adopting a framework that explicitly accounts for the genealogical effects of population subdivision and empirical sampling schemes.A LTHOUGH most (if not all) species are characterized by various degrees of population subdivision, population geneticists continue to employ models of panmictic populations of constant size (the neutral equilibrium, NE, model) when testing for selection and/ or demographic changes through time. Motivated by empirical data sets that were found to be incompatible with expectations under the NE model, recent largescale studies have employed coalescent simulations of demographic changes such as bottlenecks and/or population expansions in attempts to estimate parameters of such (arguably) biologically more realistic scenarios (e.g., Marth et al. 2004;Nordborg et al. 2005;Ometto et al. 2005;Schmid et al. 2005;Heuertz et al. 2006;Li and Stephan 2006;Pyhäjärvi et al. 2007;Ross-Ibarra et al. 2008). However, such simulations still assume unstructured populations, while the empirical data may derive from subdivided species and a variety of sampling schemes. The data typically collected in such projects consist of multilocus DNA sequences from which genealogical information is extracted, e.g., on the number of segregating sites (S ), the average pairwise sequence diversity...

“…Using an experimental design in which a consistent set of populations was sequenced for the same loci in both species, Baudry et al (2004Baudry et al ( , 2006) studied four Xlinked genes in African D. melanogaster (Kenya, Zimbabwe, Ivory Coast, and Niger) and D. simulans populations (Madagascar, Mayotte, Tanzania, and Kenya). Although it is not discussed by the authors, these studies revealed similar levels of variability in both species, even if only the most variable populations from the ''Eastern group'' (Madagascar, Mayotte, Tanzania, and Kenya) are considered for D. simulans:…”

Section: Discussionmentioning

confidence: 99%

AfricanDrosophila melanogasterandD. simulansPopulations Have Similar Levels of Sequence Variability, Suggesting Comparable Effective Population Sizes

Nolte

Schlötterer

2008

Drosophila melanogaster and D. simulans are two closely related species with a similar distribution range. Many studies suggested that D. melanogaster has a smaller effective population size than D. simulans. As most evidence was derived from non-African populations, we readdressed this question by sequencing 10 X-linked loci in five African D. simulans and six African D. melanogaster populations. Contrary to previous results, we found no evidence for higher variability, and thus larger effective population size, in D. simulans. Our observation of similar levels of variability of both species will have important implications for the interpretation of patterns of molecular evolution. DROSOPHILA melanogaster and D. simulans are two closely related species, which have a similar, but not identical, distribution range and demographic history (David and Capy 1988;Irvin et al. 1998;Capy and Gibert 2004;Lachaise and Silvain 2004). This species pair has been used in numerous comparative studies highlighting their similarities and differences. One of the central conclusions emerging from these studies was that the effective population size (N e ) differs between the two species, with D. simulans having the larger size.The level of neutral polymorphism which scales with effective population size was found to be higher in D. simulans than in D. melanogaster (Aquadro et al. 1988;Aquadro 1992;Moriyama and Powell 1996). In contrast, due to the higher efficacy of selection in large populations, nonneutral characters are expected to be less variable in the species with the larger population size. Consistent with D. simulans having a larger effective population size, D. melanogaster was repeatedly found to harbor higher levels of nonsynonymous polymorphism (Moriyama and Powell 1996;Morton et al. 2004). Similarly, the efficacy of selection for synonymous codon usage is expected to depend on population size, with selection being more effective in larger populations (Muto and Osawa 1987;Akashi 1995). Concordant with a smaller population size, and thus relaxed selective constraint, the D. melanogaster lineage has fixed a much higher number of unpreferred codons than the D. simulans lineage (Akashi 1995(Akashi , 1996(Akashi , 1997Akashi and Schaeffer 1997;Akashi et al. 1998;McVean and Vieira 2001). Allozymes which evolve under selective constraints, have consistently been shown to be much less variable in D. simulans than in D. melanogaster Singh et al. 1987;Choudhary et al. 1992). Finally, morphological data that can be directly interpreted as reflecting adaptive constraints also support the picture of lower variability and less differentiation between worldwide D. simulans than D. melanogaster populations ½reviewed in Capy and Gibert (2004).Unfortunately, the majority of data, from which evidence for different effective population sizes of D. simulans and D. melanogaster was derived, is based on comparisons of non-African populations ½e.g., Moriyama and Powell (1996). Given that both species underwent changes in effective p...