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Interspecific Hybrids of Drosophzla Heteroneura and D

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Interspecific Hybrids of Drosophzla Heteroneura and D Evolution, 43(2), 1989, pp. 347-361 INTERSPECIFIC HYBRIDS OF DROSOPHZLA HETERONEURA AND D. SZLVESTRZS I. COURTSHIP SUCCESS JAYNEN. AHEARN' Department of Genetics, University of Hawaii, Honolulu, HI 96822 AND ALANR. TEMPLETON Department of Biology, Washington University, St. Louis, MO 63130 Abstract. -Drosophila heteroneura and D. silvestris are well-defined, sympatric species of the plan- itibia subgroup of Hawaiian Drosophila. D. silvestris can be subdivided into two allopatric mor- photypes that differ in the number of bristle rows on the front tibia (two rows versus three rows). We measured courtship success of intraspecific and interspecifichybrids as the proportion of females inseminated during a two-week period with a single sib male. Proportions were arcsin-transformed so that the values were asymptotically normal in distribution, and tests of homogeneity and of mean differences were performed. Of key importance is the discovery of genetic variation for the proportion of inseminated females within both D. heteroneura and D. silvestris. The interspecific crosses and the D. silvestris intraspecific crosses also provide evidence for a coadapted gene complex with some dominance or heterosis. This coadapted gene complex correlates with the morphotypes of these flies, rather than with the D. heteroneura/D. silvestris contrasts per se. This observation stresses the importance of recognizing both behavioral and morphological components of the mate- recognition system. The incompatible coadaptation that separates the two-row from the three-row forms also supports recent molecular studies which indicate that the three-row form split from the two-row form prior to the split between D. heteroneura and two-row D. silvestris. The observations of intraspecific variability and coadaptation support the predictions of a genetic-transilience model which explains the origin of a new mate-recognition system in terms of sexual selection in the context of a founder-flush event. Received April 28, 1987. Accepted October 12, 1988 Nowhere on earth does there exist a better studies of Hawaiian Drosophila evolution natural laboratory for evolutionary studies have been concerned with understanding the than the Hawaiian Archipelago. Ofthe myr- genetic processes that lead to speciation. Ex- iad plant and animal groups that show ex- perimental work has focused on newly di- plosive speciation in this unique geological verged species pairs which are sympatric and situation, the drosophilids have been most homosequential (i.e., share a common poly- comprehensively investigated. The total tene-chromosome band sequence). Hawaiian drosophilid fauna is now esti- Drosophila silvestris and Drosophila het- mated at nearly 800 species. Among them, eroneura of the planitibia subgroup are such the picture-wings, so called because of pig- a pair of species endemic to the island of ment markings on the wings, are impres- Hawaii, which is less than 0.5 million-years sively large and long-lived and display com- old (McDougall and Swanson, 1972). They plex behaviors including territorial defense are sympatric everywhere except Kohala (the by males and elaborate courtships. Early oldest volcano of the five comprising the work centered on identifying the species and island), where D. heteroneu-ra is absent. The their relationships to one another and to the two species share a third-chromosome in- ecosystem. Phylogenetic relationships of 103 version polymorphism by which they differ picture-winged Hawaiian Drosophila species from other members of the planitibia have been determined, based upon banding subgroup. Drosophila silvestris is polymor- sequences and inversions in the salivary- phic for ten additional inversions which D. gland polytene chromosomes (Carson and heteroneura does not carry. However, mea- Yoon, 1982; Carson, 1983). More recently, sures of chromosome similarity are quite high (Craddock and Johnson, 1979; Rogers' S = 0.67). A careful analysis of heterochro- I Present address: 50 1 Hahaione Street, Apartment matin distribution by Chang (1984) using 10-G, Honolulu, HI 96824. C-banding and fluorescent-staining meth- 348 J. N. AHEARN AND A. R. TEMPLETON ods demonstrated that these two species are In all members of the planitibia subgroup identical for this character. of Hawaiian Drosophila, the dorsal tibia1 Genetic similarity based on electropho- bristles of the male foreleg are modified as retic variability for enzyme proteins is also long setae that are used in courtship (Spieth, extremely high. Ten populations of D. sil- 198 1). Heterogeneity between taxa exists in vestris and three populations of D. hetero- the number of bristles found in one row neura were surveyed for 12 loci by Crad- (called 5a) lying between rows 5 and 6. All dock and Johnson (1 979). Mean similarity D. heteroneura populations have at most between the two species, calculated by the one bristle while the north and east (Hilo- method of Rogers (1972), was 0.875. Sene side) D. silvestris populations have 10-45 and Carson (1977) sampled 25 loci in both setae in 5a (and are thus "three-rowed). species at three locations and found genetic The south and west (Kona-side) D. silvestris identity (Net's 7) equal to 0.939. This was populations are similar to D. heteroneura not significantly different from the similar- (as well as all other planitibia-subgroup ities among populations of D. silvestris (I = species), with the "two-rowed" form of this 0.96 1) or among populations of D. hetero- character (Carson and Bryant, 1979; Carson neura (I = 0.949). More recently, Hunt et et al., 1982). al. (198 1) and Hunt and Carson (1983) have In one of the earliest studies ofthis species compared DNA sequences of D. heteroneu- pair, Craddock (1975) discovered that ra and D. silvestris. The mean change in crosses of female D. silvestris x male het- average melting-point temperature (AT,,,) eroneura would give F, progeny that were for this pair was 0.68  0.2OC; interpreted fertile in both sexes. Aheam and Val (1975) as 0.6% difference in DNA sequences be- obtained fertile hybrids from the reciprocal tween them. Finally, DeSalle et al. (1 986b) cross. By morphological comparisons with studied restriction-site variation in the mi- laboratory reared F,'s, Kaneshiro and Val tochondrial DNA (mtDNA) of these two (1977) inferred that about 1°/ of the flies species. They found the Nei identity (7) be- from these taxa captured from the Kahuku tween populations ofD. silvestris to be 0.782, Ranch population were F, hybrids. Con- and that between populations of D. heter- trasts of mtDNA haplotypes with mor- oneura to be 0.704. The identities between phology also support the idea that a limited populations of different species were only amount of hybridization occurs in natural slightly lower, ranging from 0.633 to 0.689. populations (DeSalle et al., 1986b). How- Morphologically, these species are strik- ever, in spite of extensive collections over ingly different. D. heteroneura has a laterally many years, both the morphological and broadened, anterior-posteriorly com- mitochondria1 analyses indicate that hy- pressed head, in contrast to the character- bridization only occurs at a few locations istic drosophila shape of the D. silvestris (DeSalle and Templeton, 1987). head. In addition, there are several color- Aheam et al. (1 974) and Kaneshiro (1976) pattern differences, which give the overall showed that strong premating or ethological impression that D. heteroneura is a lighter isolation exists between D. silvestris and D. (almost yellow) fly than D. silvestris (nearly heteroneura. Using the "male-choice" black). Using hybridization methods to be method, isolation indices (the excess in fre- discussed shortly, Val (1 977) and Temple- quency of homogamic matings over heter- ton (1977) performed a genetic analysis of ogamic matings) of 0.92 were obtained for five morphological character differences. both female x male species combinations. They concluded that the head-shape differ- On a gross level, however, the courtship rit- ence is due primarily to a single X-linked, uals of the two species are identical (Spieth, sex-limited locus that is epistatically inter- 198 1). acting with several autosomal loci of minor Details of accumulated work on D. effect. Three additional characters (face col- heteroneura and D. silvestris have been or, wing spotting, and mesopleural pigmen- reviewed by Carson (1978, 1982). This tation) were also controlled by interactions species-pair continues to be of interest. Their of autosomal and X-linked genes. In total, chromosomal, allozyme, and DNA-se- the morphological species differences ana- quence similarities are in sharp contrast to lyzed could be attributed to 15-1 9 loci. the striking morphological differences de- COURTSHIP SUCCESS IN DROSOPHILA HYBRIDS 349 TABLE1. Laboratory stocks used in the hybrid crosses. Species Hawaii (Big Island) collection site Stock designation Chromosomal inversions - D. heteroneura Olaa Forest Reserve (Hilo side) Q71G12 monomorphic Pauahi (Kona side) R79G5 (no information) Hualalai (Kona side) U51Y40 3m D. silvestris Kilauea Forest Reserve (Hilo side) Q48F5 R59G4 U28T2 Pauahi (Kona side) S91B1 (no information) U21B1 (no information) Hualalai (Kona side) U35B (no information) U5 1B 4k2, 4t, 3m termined by as few as 15 loci. With the ap- instars are completed in 3-4 weeks; and parent fertility of F, interspecific hybrids, metamorphosis to adults lasts another 3-4 behavioral mechanisms are left as a major weeks. Adults that were to be used in ex-
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