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Genetics of a Difference in Pigmentation Between Drosophila Yakuba and Drosophila Santomea

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Genetics of a Difference in Pigmentation Between Drosophila Yakuba and Drosophila Santomea Evolution, 56(11), 2002, pp. 2262±2277 GENETICS OF A DIFFERENCE IN PIGMENTATION BETWEEN DROSOPHILA YAKUBA AND DROSOPHILA SANTOMEA ANA LLOPART,1,2 SUSANNAH ELWYN,1,3 DANIEL LACHAISE,4,5 AND JERRY A. COYNE1,6 1Department of Ecology and Evolution, The University of Chicago, 1101 East 57 Street, Chicago, Illinois 60637 2E-mail: [email protected] 3E-mail: [email protected] 4Laboratoire Populations, GeÂneÂtique et Evolution, CNRS, 91198 Gif-sur-Yvette, France 5E-mail: [email protected] 6E-mail: [email protected] Abstract. Drosophila yakuba is a species widespread in Africa, whereas D. santomea, its newly discovered sister species, is endemic to the volcanic island of SaÄo Tome in the Gulf of Guinea. Drosophila santomea probably formed after colonization of the island by its common ancestor with D. yakuba. The two species differ strikingly in pigmentation: D. santomea, unlike the other eight species in the D. melanogaster subgroup, almost completely lacks dark abdominal pigmentation. D. yakuba shows the sexually dimorphic pigmentation typical of the group: both sexes have melanic patterns on the abdomen, but males are much darker than females. A genetic analysis of this species difference using morphological markers shows that the X chromosome accounts for nearly 90% of the species difference in the area of abdomen that is pigmented and that at least three genes (one on each major chromosome) are involved in each sex. The order of chromosome effects on pigmentation area are the same in males and females, suggesting that loss of pigmentation in D. santomea may have involved the same genes in both sexes. Further genetic analysis of the interspeci®c difference between males in pigmentation area and intensity using molecular markers shows that at least ®ve genes are responsible, with no single locus having an overwhelming effect on the trait. The species difference is thus oligogenic or polygenic. Different chromosomal regions from each of the two species in¯uenced pigmentation in the same direction, suggesting that the species difference (at least in males) is due to natural or sexual selection and not genetic drift. Measurements of sexual isolation between the species in both light and dark conditions show no difference, suggesting that the pigmentation difference is not an important cue for interspeci®c mate discrimination. Using DNA sequence differences in nine noncoding regions, we estimate that D. santomea and D. yakuba diverged about 400,000 years ago, a time similar to the divergences between two other well-studied pair of species in the subgroup, both of which also involved island colonization. Key words. Drosophila, genetics, pigmentation, reproductive isolation, speciation. Received February 22, 2002. Accepted August 15, 2002. Recent genetic studies of reproductive isolation are begin- chromosomes? Rice (1984), for example, posits that species ning to reveal patterns that may help us understand speciation differences that evolved by antagonistic coevolution between (Coyne and Orr 1999). However, there are still relatively few males and females may be caused by genes preferentially genetic studies of species differencesÐthose morphological, located on the X chromosome, as will genes ®xed by natural physiological, and behavioral traits that distinguish closely selection whose favorable effects are partially recessive related species but do not necessarily cause reproductive iso- (Charlesworth et al. 1987). lation. A recent survey (Orr 2001) describes only 13 genetic Orr (2001) describes other ways that the genetic basis of studies of species differences, six in the genus Drosophila species differences can help us understand evolution. Such and four in the plant genus Mimulus. analyses are likely to become more important with the in- Such work, however, is important in answering long-stand- creasing use of quantitative-trait-locus (QTL) mapping, ing questions of evolutionary genetics. For example, are spe- which can be used to locate and estimate the effects of chro- cies differences caused by natural selection or other evolu- mosome regions affecting traits between any pair of crossable tionary forces such as genetic drift? Theoretical work shows species that meet two criteria: (1) hybrids are somewhat fer- that if alleles from one species act in a consistent direction tile; and (2) one can construct a molecular map based on on a trait, then the species difference is likely to have evolved DNA differences (for an exemplar of the use of QTL mapping by natural or sexual selection (Orr 1998b). Are such differ- in evolution see Bradshaw et al. 1998; Schemske and Brad- ences due to many genes of small effect, as Fisher (1930) shaw 1999). posited, or are fewer genes of larger effect involved? For Here we present a genetic analysis of a striking character example if species differences in male-limited traits such as differenceÐthe degree of abdominal pigmentationÐbetween plumage color prove to be highly polygenic, this would imply two closely related species of Drosophila, D. yakuba and D. that the trait evolved by gradual coevolution of males and santomea. Drosophila yakuba is widespread across western females (Coyne and Orr 1999). Theoretical studies show, Africa, but D. santomea, discovered in 1998, is endemic to however, that evolution by natural selection toward a ®xed the island of SaÄo TomeÂ, an 860-km2 volcanic island 320 km optimum should lead to an exponential distribution of gene west of Gabon (Lachaise et al. 2000). Drosophila yakuba also effects with many factors having small effects, but also with inhabits SaÄo TomeÂ, but tentative molecular evidence points some factors having relatively large effects (Orr 1998a). Do to D. santomea originating allopatrically after a colonization genes for species differences tend to be located on particular event by the ancestor of modern D. yakuba, with D. yakuba 2262 q 2002 The Society for the Study of Evolution. All rights reserved. PIGMENTATION DIFFERENCES IN DROSOPHILA 2263 subsequently invading the island a second time (Cariou et al. F1 hybrids, the relative effects of individual chromosome 2001). On SaÄo TomeÂ, D. yakuba is limited to lower elevations, segments could not be discerned because a lack of genetic whereas D. santomea lives in the mist forests at higher ele- markers in these species necessitated a biometrical analysis vations. A hybrid zone occurs between 1150 m and 1450 m (Hollocher et al. 2000b). elevation on the volcano, where one ®nds a low frequency Kopp et al. (2000) suggest that, in Drosophila, differences of hybrids (about 1%; Lachaise et al. 2000). in sexual dimorphism of pigmentation among species may Molecular phylogenetic analysis indicates that D. yakuba be based on changes at the bric-aÁ-brac (bab) locus, which and D. santomea are sister species within the eight species contains two adjacent genes (bab1 and bab2) whose wild- constituting the monophyletic D. melanogaster subgroup (La- type alleles repress male-speci®c pigmentation in females of chaise et al. 2000; Cariou et al. 2001). This pair thus rep- D. melanogaster. Their hypothesis rests on a correlation: most resents a speciation event independent of the well-studied species with darkly pigmented males show no expression of speciation event separating D. simulans and D. melanogaster bab in males (thus permitting the sex-speci®c pigmentation), and of the two speciation events in which the ancestor of D. whereas species lacking male pigmentation show expression simulans produced two island endemics, D. sechellia and D. of bab in males. Some species, however, do not obey this mauritiana (Lachaise et al. 1988). Molecular evidence puts generalization. Kopp et al. (2000) also posit that other genes, the divergence between D. yakuba and D. santomea at about including Abdominal-B and doublesex, may regulate bab, and 450,000 years ago (Cariou et al. 2001), a divergence time there are clearly many other steps in the melanin-synthesis similar to that separating D. simulans from each of its two and segment-identity pathways that might affect abdominal sister species (;260,000±410,000 year; Kliman et al. 2000). pigmentation (Wright 1987; Hopkins and Kramer 1992; True The D. melanogaster subgroup thus includes three episodes et al. 1999). Only direct genetic analysis can determine the of speciation following island colonization, all occurring at number, location, and effects of genes causing a species dif- roughly the same time. ference in pigmentation. The most striking aspect of D. santomea is that it is the Despite considerable sexual isolation between D. santomea only species in the D. melanogaster subgroup lacking pro- and D. yakuba and the sterility of hybrid males (Lachaise et nounced abdominal pigmentation in both sexes. Drosophila al. 2000; Coyne et al. 2002), one can perform genetic analysis yakuba and the seven other species share a single sexually by making backcrosses using the fertile F1 females. Here we dimorphic form of pigmentation: males have thin black report the results of two genetic studies of the interspeci®c stripes along the posterior portions of tergites 2, 3, and 4 difference in abdominal pigmentation. One study uses mor- (tergites are the sclerotized dorsal plates), whereas tergites phological mutants as markers to examine the effects of three 5±7 are completely black (Fig. 1c). Females have stripes chromosome regions on pigmentation. The other uses mo- along the posterior portions of all tergites, and tergites 5±7 lecular markers as tools and is limited to studying the pig- show substantial (but not complete) black pigmentation (Fig. mentation difference in males. Our goal is to provide a pre- 1d). In D. santomea males have virtually no pigmentation liminary analysis of this trait difference that will answer the (Fig. 1a), and females show very light striping on the pos- following questions: Does the species difference involve only terior parts of tergites 2±5 and no pigmentation on tergites a single gene, or is it more polygenic? Do certain chromo- 6 and 7 (Fig.
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