Academic journal article Genetics

African Sequence Variation Accounts for Most of the Sequence Polymorphism in Non-African Drosophila Melanogaster

Academic journal article Genetics

African Sequence Variation Accounts for Most of the Sequence Polymorphism in Non-African Drosophila Melanogaster

Article excerpt

ABSTRACT

We compared the sequence polymorphism of 12 genomic fragments in six geographically dispersed African populations to one European Drosophila melanogaster population. On the basis of one African and one European population half of these fragments have strongly reduced levels of variability outside of Africa. Despite this striking difference in European variation, we detected no significant difference in African variation between the two fragment classes. The joint analysis of all African populations indicated that all high-frequency European alleles are of African origin. We observed a negative Tajima's D in all African populations, with three populations deviating significantly from neutral equilibrium. Low, but statistically significant, population differentiation was observed among the African populations. Our results imply that the population structure and demographic past of African D. melanogaster populations need to be considered for the inference of footprints of selection in non-African populations.

IN the wake of a steadily growing number of sequenced genomes, hitchhiking mapping has become a popular approach for the identification of genomic regions, which were recently subjected to positive directional selection (SCHLOTTERER 2003). The underlying idea is that the spread of a beneficial mutation is not limited to the target of selection alone, but also neutral flanking variation is affected [(hitchhiking) KAPLAN et al. 1989; MAYNARD SMITH and HAIGH 1974]. Thus, any neutral genetic marker linked to a beneficial mutation could be used to identify the genomic region affected by such a selective sweep. Different approaches to the identification of nonneutral evolution in hitchhiking mapping studies have been suggested, such as the reduction in variability, increased level of linkage disequilibrium, and a skewed allele frequency spectrum (KoHN et al. 2000; KIM and STEPHAN 2002; PAYSEUR et al. 2002; SCHLÔTTERER 2002, 2003). Apart from humans, Drosophila melanogasteris probably the organism for which most in-depth hitchhiking studies have been performed (SCHLOTTERER et al. 1997; HARR et al. 2002; GLINKA et al. 2003; KAUER et al. 2003a; ORENGO and AGUADÉ 2004).

Biogeographical and genetic data suggest that D. melanogaster evolved in tropical Africa and colonized the rest of the world only recently (DAVID and CAPY 1988; LACHAISE et al. 1988). Estimates for the colonization time range from ^15,0OO to 10,000 years ago for Europe and Asia, to some 100 years ago for the Am ericas and Australia (DAVID and CAPY 1988). The colonization of novel environments outside the ancestral species range probably imposed new selection pressure such as novel climatic conditions or food resources. Thus, it is likely that a burst of adaptations associated with the outof-Africa habitat expansion occurred in the derived populations. Hence, the comparison of African and non-African Z). melanogaster populations is a promising approach to gain insight into the genetic changes required for a habitat expansion from Africa to the rest of the world.

Consistent with previous microsatellite surveys (KAUER et al. 2003a), a genomic scan based on 105 X-linked intergenic and intronic fragments (GLINKA et al. 2003) identified a large number of genomic regions deviating from neutral expectations. While microsatellite-based surveys focus mainly on the reduction of variability, the analysis of DNA sequences also provides information on the frequency spectrum of ancestral and derived sequence variants. GLINKA et al. (2003) observed a pronounced difference between genomic regions putatively affected by a recent selective sweep and genomic regions, which showed no deviation from neutral expectations. Compared to neutrally evolving fragments, those with low levels of sequence polymorphism in a European population (i.e., putatively selected ones) displayed a pronounced excess of derived sites fixed in Europe but absent or rare in the African sample. …

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