Sexual Selection Operating in a Wild Population of Drosophila Robusta
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BRIEF COMMUNICATIONS Evuluriun, 50(5), 1996, pp. 2095-2100 SEXUAL SELECTION OPERATING IN A WILD POPULATION OF DROSOPHILA ROBUSTA WILLIAMJ. ETGES Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas 72701 E-mail: [email protected] Key words.-Breeding site ecology, Drosophila, inversion polymorphism, life cycle components, mating success, natural selection, sexual selection. Received July 18, 1995. Accepted January 9, 1996. Almost 60 years have elapsed since the discovery of vari- (e.g., Prout 1971; Bundgaard and Christiansen 1972). Inver- ation in the polytene chromosomes of Drosophila (Sturtevant sion polymorphisms in cactophilic D. buzzatii have been stud- and Dobzhansky 1936). Inversion polymorphism studies have ied this way, a species that feeds and breeds in the fermenting revealed some of the intricacies of evolutionary change, but tissues of several species of prickly pear cactus. In general, even now, when interest in them has waned, there is little cactophilic Drosophila have taught us much about mainte- understanding of the particular alleles contained within them nance of genetic variability, host specificity, chemical ecol- that alone or in relation to other genes influence any com- ogy, trophic adaptation, and life history evolution (Barker ponent of fitness. Perhaps the most important rule about in- and Starmer 1982; Barker et al. 1990). Despite the fact that version polymorphisms learned from a long history of lab- 48% (44191) of all described and undescribed D. repleta oratory experiments (cf. Lewontin et al. 1981) is their sen- group species possess inversion polymorphism (Wasserman sitivity to environmental features such as temperature and 1992), in only a few species has there been concerted effort nutrition. Therefore, laboratory studies alone may not predict to unravel the causes for maintenance of inversion poly- the consequences due to genotype (karyotype) by environ- morphism in nature, that is, D. buzzatii and D. mojavensis. ment interactions of selection in wild populations. Inversion polymorphism in the latter species, along with D. Only a few studies have documented selective mechanisms pachea, a cactophilic member of the D. nannoptera group, associated with preserving inversion polymorphisms in nat- has been recently summarized (Etges et al., in press). Ruiz ural populations beyond establishing correlations with tem- et al. (1986) demonstrated endocyclic selection, directional perature, rainfall, humidity, elevation, and other environ- selection in opposing directions during the life cycle, on gene mental features. Despite the long history of interest in the arrangements of D. buzzatii. However, this pattern is popu- ecology of Drosophila breeding and feeding sites (cf. Carson lation and host specific (Hasson et al. 1991) and not sur- 1951, 1971; Heed 1957, 1968, 1971), experimental analyses prisingly is limited to a few components of fitness including of inversion polymorphisms involving natural breeding sub- egg to third instar viability and adult body size, but not mating strates are few because the mating sites and larval ecology propensity (Santos et al. 1992; Barbadilla et al. 1994). Adult of most species with well described inversion polymorphisms are poorly known, e.g., D. pseudoobscura. An early exception size in Drosophila can be correlated with increased fitness to this problem was the comprehensive study of inversion as larger flies typically have greater reproductive potential polymorphism in D. jlavopilosa, a flower breeder from South (Robertson 1957) and dispersal ability (Mangan 1982). These America (Brncic 1962). Egg to adult viability differences studies of D. buzzatii deserve special note because they il- among karyotypes were observed among preadult stages in lustrate the complexity of factors that must be addressed in flowers returned to the lab and exposed to contrasting tem- understanding the maintenance of inversion polymorphisms peratures (Brncic 1968). More recently, analysis of the "sex- in natural populations. ratio" meiotic drive system in natural populations of D. pseu- Thus, studies of selection on inversion polymorphisms in doobscura suggested that most selection responsible for species with hard-to-find breeding sites have been restricted maintaining this polymorphism must be operating in preadult to adult flies because they can be captured in the wild. If we stages (Beckenbach 1996). A notable non-Drosophila ex- include the recent D. buzzatii studies mentioned above, sev- ample is the chromosome I polymorphism in seaweed flies, eral studies of genetic variation in male mating success (An- Coelopa frigida, that carry out their life cycle on decom- derson et al. 1979; Levine et al. 1980; Salceda and Anderson posing seaweed on beaches around the north Atlantic and 1988), the recent analysis of the "sex-ratio" polymorphism North Sea. Gene arrangement-based differences in egg to in D. pseudoobscura (Beckenbach 1996), and mate choice in adult development time, adult body size, and mate preference seaweed flies (Gilburn et al. 1992), most of what we know have been demonstrated in seaweed-reared flies (Day et al. of selection operating on inversion polymorphisms under nat- 1983; Engelhard et al. 1989; Gilburn et al. 1992). ural conditions has only recently been documented. It is in- For species that can be collected in nature throughout their teresting to note that not one example documenting an iden- life cycle, karyotype frequencies can be estimated from life tifiable selective agent operating on inversion polymorphisms stages reared in the wild and comparisons can be made be- was cited by Endler (1986) in his review, "Natural Selection tween stages of the life cycle in selection component analyses in the Wild," despite the long history of population genetics 2096 BRIEF COMMUNICATIONS research in Drosophila and other organisms with chromosome into different food vials in the laboratory. Each wild male polymorphisms. was mated to a stock homokaryotypic female and wild fe- Studies of inversion polymorphisms in D. robusta over the males were allowed to oviposit until they were depleted of last 40 years have revealed a wealth of information on clinal stored sperm. Remating is frequent in both sexes with cop- variation (Stalker and Carson 1948; Levitan 1978; Etges ulations lasting less than a minute (Prakash 1967a) and no 1984), temporal frequency changes (Carson 1958; Levitan insemination reaction is formed (Grant 1983). However, there 1973; Etges 1984, 1991), linkage disequilibrium (Carson is little evidence of multiple insemination, that is, mixtures 1953; Levitan 1958, 1992), and population structure (Carson of sperm from more than one male stored by wild females, 1959; Prakash 1973). Variation of karyotype-related fitness in the egg samples of D. robusta females from Fayetteville, components including viability, fertility, mating speed, egg- Arkansas (Etges 1991, unpubl. data). Therefore, five off- to-adult development time, age at first reproduction, and adult spring from each wild female were karyotyped, and in a longevity under laboratory conditions has also been assessed subset of 20 females, up to 10 larvae were scored to ascertain (Prakash 1967a,b, 1968; Etges 1989). This species is one of whether five larvae were a representative egg sample in this the more common members of the noncosmopolitan Dro- population. In no cases were additional gene arrangements souhila fauna in the east-central United States and Canada observed in the expanded progeny sets, suggesting that sam- with a species range roughly coincident with the eastern de- pling five larvae per female provided an adequate sample of ciduous forest (Carson 1958). the offspring each female would have contributed to nature. Drosophila robusta breeds in sap fluxes of several decid- Wild females were transferred to fresh food vials every few uous tree species, particularly American elm, Ulmus ameri- days until no larvae were seen. They were then mated to cana (Carson and Stalker 1951). Fourteen gene arrangements stock homokaryotypic males. The karyotypes of at least sev- distributed over the three metacentric chromosomes (X, 2, 3) en F, larvae from each of the wild adults crossed to stock have been found segregating in natural populations. Those homokaryotypes were determined to infer the karyotypes of on the X and second chromosomes are often encountered in the wild adults. nonrandom associations (reviewed in Levitan 1992) sug- All inversion frequency data were tested for heterogeneity gesting fitness interactions between arrangements on oppos- between sexes and life stages using likelihood ratio or G- ing chromosome arms. Even now, it remains impractical to tests (Sokal and Rohlf 1981) with Williams's correction (Wil- perform experiments with sap flux-reared larvae. liams 1976). Data for each chromosome arm were also tested The focus of the present study was to estimate karyotypic for Hardy-Weinberg equilibrium. Analyses of linkage dis- variation in a natural population of D. robusta and compare equilibrium of gene arrangements on the X and second chro- frequencies of wild caught adults and their offspring to detect mosomes at Mill Creek and four other Arkansas populations the effects of natural selection and possible karyotype related are presented in Levitan and Etges (1995) and so are not differences in male mating success. This study represents the presented here in detail. They found strong nonrandom as- first attempt to identify selection on particular components