Genetic studies of two sister species in the Drosophila melanogaster subgroup, D. yakuba and D. santomea

Abstract

We performed genetic analysis of hybrid sterility and of one morphological difference (sex-comb tooth number) on D. yakuba and D. santomea, the former species widespread in Africa and the latter endemic to the oceanic island of São Tomé, on which there is a hybrid zone. The sterility of hybrid males is due to at least three genes on the X chromosome and at least one on the Y, with the cytoplasm and large sections of the autosomes having no effect. F1 hybrid females carrying two X chromosomes from either species are perfectly fertile despite their genetic similarity to completely sterile F1 hybrid males. This implies that the appearance of Haldane's rule in this cross is at least partially due to the faster accumulation of genes causing male than female sterility. The larger effects of the X and Y chromosomes than of the autosomes, however, also suggest that the genes causing male sterility are recessive in hybrids. Some female sterility is also seen in interspecific crosses, but this does not occur between all strains. This is seen in pure-species females inseminated by heterospecific males (probably reflecting incompatibility between the sperm of one species and the female reproductive tract of the other) as well as in inseminated F1 and backcross females, probably reflecting genetically based incompatibilities in hybrids that affect the reproductive system. The latter 'innate' sterility appears to involve deleterious interactions between D. santomea chromosomes and D. yakuba cytoplasm. The difference in male sex-comb tooth number appears to involve fairly large effects of the X chromosome. We discuss the striking evolutionary parallels in the genetic basis of sterility, in the nature of sexual isolation, and in morphological differences between the D. santomea/D. yakuba divergence and two other speciation events in the D. melanogaster subgroup involving island colonization.

Sex Combs are Important for Male Mating Success in Drosophila melanogaster

“…This variation makes the sex comb an attractive model for understanding the genetic basis of morphological evolution and the interaction between developmental pathways and natural selection in shaping animal form. Quantitative-genetic analyses in several species have shown that interspecific and intraspecific differences in sex comb size are determined by multiple, as yet unidentified, loci (True et al 1997;Macdonald and Goldstein 1999;Nuzhdin and Reiwitch 2000;Coyne et al 2004;Tatsuta and TakanoShimizu 2006;Graze et al 2007). At the same time, developmental-genetic approaches are beginning to elucidate the molecular pathways involved in the specification and differentiation of sex combs (Barmina et al 2005;Barmina and Kopp 2007).…”

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

“…Additionally, many studies have found that a disproportionately large percentage of genes relating to speciation, reproductive isolation, and mate choice map to the sex chromosomes (Dobzhansky 1974;Templeton 1977;Coyne 1985;Coyne and Orr 1989;Prowell 1998;Reinhold 1998;Ritchie and Phillips 1998;Presgraves 2002). This may be because sex-linked incompatibility loci evolve at a faster rate than autosomal incompatability sites (Tao and Hartl 2003;Coyne et al 2004). …”

Quantitative Trait Loci Affecting the Difference in Pigmentation BetweenDrosophila yakubaandD. santomea

“…The diagnostic differences between the species include male genital morphology and sex-comb tooth number (Lachaise et al 2000;Coyne et al 2004), but the most striking difference involves abdominal pigmentation. Among the nine species in the D. melanogaster subgroup, eight of them, including D. yakuba, have similar patterns of dark pigmentation: males possess thin black stripes along the posterior portions of tergites 2, 3, and 4, while tergites 5-7 are completely black.…”