Academic journal article Genetics

The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila Ananassae

Academic journal article Genetics

The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila Ananassae

Article excerpt

ABSTRACT

The main evolutionary forces leading to genetic differentiation between populations are generally considered to be natural selection, random genetic drift, and limited migration. However, little empirical evidence exists to help explain the extent, mechanism, and relative role of these forces. In this study, we make use of the differential migration behavior of genes located in regions of low and high recombination to infer the role and demographic distribution of natural selection in Drosophila ananassae. Sequence data were obtained from 13 populations, representing almost the entire range of cosmopolitan D. ananassae. The pattern of variation at a 5.1-kb fragment of the furrowed gene, located in a region of very low recombination, appears strikingly different from that of 10 noncoding DNA fragments (introns) in regions of normal to high recombination. Most interestingly, two main haplotypes are present at furrowed, one being fixed in northern populations and the other being fixed or in high frequency in more southern populations. A cline in the frequency of one of these haplotypes occurs in parallel latitudinal transects. Taken together, significant clinal variation and a test against alternative models of natural selection provide evidence of two independent selective sweeps restricted to specific regions of the species range.

RECENT large-scale studies of genetic variation are beginning to confirm that species range expansion and the colonization of previously uninhabited territories are accompanied by genetic adaptation to changes in environmental conditions, the signature of which may be detected at the molecular level (HARR et al. 2002; GLINKA et al. 2003; KAUER et al. 2003). In the case of Drosophila melanogaster, such an expansion is believed to have started from Africa ~10,000-15,000 years ago (DAVID and CAPY 1988; LACHAISE et al. 1988). D. ananassae, another cosmopolitan species in the melanogaster group, is thought to have its origin in Southeast (SE) Asia (TOBARI 1993). A recent multilocus study of world-wide populations of D. ananassae substantiates this claim, defining the ancestral range of this species to be a region of SE Asia that existed as a single landmass (Sundaland) during the late Pleistocene (~18,000 years ago), while other populations including those in more temperate regions appear to be more recent colonizations (DAS et al. 2004, accompanying article in this issue). Thus, a similar scenario is emerging for this species, with the invasion of new climatic zones providing a priori expectation that local populations have adapted to their new environments. However, in contrast to D. melanogaster, D. ananassae is a species displaying significant population structure, enabling the footprints of natural selection at the DNA level to be analyzed in a subdivided population.

Previous studies of four D. ananassae populations (Nepal, Myanmar, India, and Sri Lanka) found compelling evidence for the action of natural selection at loci in regions of low recombination (STEPHAN et al. 1998; CHEN et al. 2000). At both the vermilion (v) and furrowed (fw) loci, a pattern of homogenization of allele frequencies within, but differentiation between geographic regions [i.e., North (Nepal, Myanmar) vs. South (India, Sri Lanka)] was found. In both studies, this homogenization of allele frequencies in the northern populations rejected a model of background selection against deleterious mutations (CHARLESWORTH et al. 1993), instead favoring a model of the spreading of a beneficial allele (the selective sweep model; MAYNARD Smith and HAIGH 1974; KAPLAN et al. 1989; STEPHAN et al. 1992). At the fw locus, the background selection model was rejected for the southern populations as well (CHEN et al. 2000), raising several important questions about the mode of selective sweeps in this subdivided species. Namely, is this pattern best explained by a single sweep (SLATKIN and WIEHE 1998), or have two independent sweeps occurred? …

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