Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations

Abstract

Uncertainty about the demographic history of populations can hamper genome-wide scans for selection based on population genetic models. To obtain a portrait of the effects of demographic history on genome variability patterns in Drosophila melanogaster populations, we surveyed noncoding DNA polymorphism at 10 X-linked loci in large samples from three African and two non-African populations. All five populations show significant departures from expectations under the standard neutral model. We detect weak but significant differentiation between East (Kenya and Zimbabwe) and West/Central sub-Saharan (Gabon) African populations. A skew toward high-frequency-derived polymorphisms, elevated levels of linkage disequilibrium (LD) and significant heterogeneity in levels of polymorphism and divergence in the Gabon sample suggest that this population is further from mutation-drift equilibrium than the two Eastern African populations. Both non-African populations harbor significantly higher levels of LD, a large excess of high-frequency-derived mutations and extreme heterogeneity among loci in levels of polymorphism and divergence. Rejections of the neutral model in D. melanogaster populations using these and similar features have been interpreted as evidence for an important role for natural selection in shaping genome variability patterns. Based on simulations, we conclude that simple bottleneck models are sufficient to account for most, if not all, polymorphism features of both African and non-African populations. In contrast, we show that a steady-state recurrent hitchhiking model fails to account for several aspects of the data. Demographic departures from equilibrium expectations in both ancestral and derived populations thus represent a serious challenge to detecting positive selection in genome-wide scans using current methodologies.

Inferring population size changes with sequence and SNP data: lessons from human bottlenecks

“…This being said, moderate bottlenecks lead to large variances in the genealogical history of samples from different loci along a chromosome (McVean, 2002). Unexpected large values of the variance of the Tajima's D have been used as evidence for the human out-of-Africa bottleneck (Voight et al, 2005) as well as supporting a bottleneck affecting a non-African Drosophila population (Haddrill et al, 2005). By contrast, the observation of small among-locus variation of Tajima's D for African populations has shown evidence against a human 'speciation bottleneck' that would have occurred during the penultimate ice age 190-130 kya (Sjödin et al, 2012).…”

“…The human out-of-Africa bottleneck shaped many properties of human variation in non-Africans and, since this event has been extensively investigated, it provides a nice example illustrating the different methodologies of demographic reconstruction. The fruit fly, Drosophila melanogaster, also provides additional insights because the relationship between population size changes and polymorphism data has been thoroughly investigated in this species (Haddrill et al, 2005;Thornton and Andolfatto, 2006). Additionally, the fruit fly's demographic history shares a resemblance with human demographic history because of its African origin and a bottleneck that has left signatures in the genomes of non-African Drosophila melanogaster populations (Li and Stephan, 2006).…”

New insights on the speciation history and nucleotide diversity of three boreal spruce species and a Tertiary relict

“…The range of estimated y and r values from individual loci was later used to define previous uniform ranges in multilocus estimates of r and y with the software Rhothetapost (Haddrill et al, 2005).…”

Controlling the False-Positive Rate in Multilocus Genome Scans for Selection

“…Historically, studies of naturally occurring molecular variation were conducted at single loci, and uncertainties about the demographic history of natural populations frequently complicated inferences about selection. Current empirical work focuses on using either multilocus data sets (e.g., Glinka et al 2003;Tenaillon et al 2004;Haddrill et al 2005b;Ometto et al 2005;Williamson et al 2005;Wright et al 2005) or wholegenome polymorphism data (e.g., Carlson et al 2005;Nielsen et al 2005;Kelley et al 2006) to discern the locus-specific effects of selection from the genome-wide effects of nonequilibrium demographic history. In general, this approach has been dubbed a ''genome scan'' for selection.…”