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Inheritance of a Secondary Sexual Character in Drosophila Silvestris (Quantitative Genetics/Sexual Dimorphism/Evolution/Speciation/Hawaiian Drosophila) HAMPTON L

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Inheritance of a Secondary Sexual Character in Drosophila Silvestris (Quantitative Genetics/Sexual Dimorphism/Evolution/Speciation/Hawaiian Drosophila) HAMPTON L Proc. Natd. Acad. Sci. USA Vol. 81, pp. 6904-6907, November 1984 Population Biology Inheritance of a secondary sexual character in Drosophila silvestris (quantitative genetics/sexual dimorphism/evolution/speciation/Hawaiian Drosophila) HAMPTON L. CARSON* AND RUSSELL LANDEt *Department of Genetics, University of Hawaii, Honolulu, HI 96822; and tDepartment of Biology, University of Chicago, Chicago, IL 60637 Contributed by Hampton L. Carson, July 16, 1984 ABSTRACT Reciprocal crosses were carried out between cal genetic technique using mutations with known positions laboratory stock specimens obtained from two races of Dro- in the genome of one taxon to map the positions of genes sophila silvestris from the island of Hawaii that differ in a producing differences between taxa in the trait(s) of interest. quantitative secondary sexual character. The race from the This method has been applied recently by Coyne (13) to ana- Hilo side of the island has a novel attribute, consisting of an lyze three sibling species in the Drosophila melanogaster extra row of cilia on the tibia of males, which is used during group that differ morphologically only in the shape of the courtship. With regard to this character, sex-linked genes con- male genitalia. He showed that the species differences are tribute about 30% of the difference, and the remaining 70% of polygenic, with contributions from at least one gene on ev- the difference between the races is produced by genes on at ery chromosome or on each arm of the major chromosomes. least two autosomes. The novel character appears to have been The second method is purely biometrical and was devel- the outcome of altered sexual selection in the Hilo-side race. In oped originally by Wright (chapter 15 in ref. 14) to estimate an altered genetic environment, resulting from a founder event the effective (or minimum) number of freely segregating ge- or random genetic drift, sexual selection may take a new direc- netic factors contributing to an extreme difference in a quan- tion, Such a shift may serve as a model for incipient speciation. titative character between two inbred (homozygous) lines by assessing the amount of genetic variance segregating in F2 or Male secondary sexual characters are among the most rapid- backcross populations. It has since been extended to the ly evolving morphological traits of higher animals, and close- analysis of crosses between wild (or genetically variable) ly related species are often distinguished taxonomically by taxa (15). The biometrical method has been used to show differences in male morphology (1). In such taxa, morpho- that the major difference in head shape between the closely logical divergence and reproductive isolating barriers be- related Hawaiian Drosophila species D. heteroneura and D. tween species may often originate by sexual selection via silvestris is polygenic, with a minimum of about six to eight female mating preferences (2-6). This appears to apply to genes involved (15-17). In the absence of available mutant many of the several hundred species of large Hawaiian Dro- stocks or known genetic markers to distinguish all the chro- sophila, and sexual selection may have been an important mosomes in the two races, we have employed the biometri- factor in their proliferation (7, 8). Here we examine the ge- cal method to investigate the inheritance of the morphologi- netic basis for the origin of a novel secondary sexual charac- cal difference between the races of D. silvestris described ter by analyzing crosses between two races of Drosophila above. silvestris. Reciprocal crosses between two stocks collected from Ka- This species is endemic to the volcanic island of Hawaii, huku Ranch, South Kona District (isofemale line U26B9), which is geologically very young; it has no lava flows older and Kilauea Forest Reserve, Puna District (isofemale line than 0.5 million years (9). Males from populations on the U28T2), representing respectively the bare and hairy races south and west side of the island ("Kona side") have two of D. silvestris, were performed between 1978 and 1983 (see rows of long cilia on the margins of the tibia of the foreleg. Fig. 1). Methods of rearing specimens, mounting legs and These are lacking in females. Between the rows is a dorsal counting cilia are given in ref. 10. All counts treated here bare area having at most two cilia. In populations to the refer to the middle (dorsal) row of cilia only. During the peri- north and east ("Hilo side"), this bare area is occupied by an od of the experiment, the mean values of cilia counts within additional row of about 20-30 cilia (10). Reciprocal crosses the stocks changed very little. Substantial genetic variance between the Kona and Hilo races give fully viable and fertile within the hairy stock (see below) creates real differences progeny of both sexes (11). between families, which invalidates the application to family The extra cilia are not a trivial character; during a crucial data of conventional statistical tests for homogeneity of stage in courtship, they are used to brush vigorously on the means and variances. More conservative tests using within- dorsal surface of the female's abdomen (12). Related species family means and variances as data points failed to disclose in the same subgroup resemble the Kona-side (bare) race of significant differences between sets of families produced by D. silvestris, having only two rows of cilia. Accordingly, the the same crossing scheme at different times. Therefore, data extra cilia on Hilo-side (hairy) males represent a novel and collected at different times was pooled whenever appropri- very recent evolutionary embellishment of a secondary sex- ate for purposes of the analysis. ual character. This provides the special focus for the follow- Cytoplasmic Effects. There is a conspicuous difference in ing analysis of its genetic basis. the distributions of reciprocal F1 populations (Fig. 1), which in principle could be produced either by maternal (or cyto- plasmic) effects or by sex-linked genes, or both. To deter- METHODS AND RESULTS mine the amount of difference in reciprocal F1 populations There are two basic methods for analyzing the genetic basis caused by maternal or cytoplasmic effect, comparisons were of phenotypic differences between closely related taxa that made between the average values of families with different can be crossed to produce fertile hybrids. First is the classi- cytoplasms but the same expected composition of nuclear genotypes. There are three such tests: two of them are com- The publication costs of this article were defrayed in part by page charge parisons between averages of male progeny from F1 females payment. This article must therefore be hereby marked "advertisement" backcrossed to the same parental stock; and, on the assump- in accordance with 18 U.S.C. §1734 solely to indicate this fact. tion that the Y chromosome is genetically inert with respect 6904 Downloaded by guest on September 29, 2021 Population Biology: Carson and Lande Proc. Natl. Acad. Sci. USA 81 (1984) 6905 e difference in the effect of X chromosomes from the hairy 40 --, I~~pi P2 and bare races is 6.68 ± 0.71 cilia, which can be contrasted B, 20o 'qP2- F-1 1xPI d with a total difference of 22.70 ± 1.00 cilia between the pure parental stocks. Thus X-linked genes account for 29.4% ± 0 5 10 15 3.4% of the difference between the races. Transformation of Scale. For biometrical analysis of the B2 10l b effective number of autosomal factors contributing to the 10 15 20 25 30 (80) 0 5 difference between the Kahuku and Kilauea stocks, it is de- F2 20 sirable to choose a scale of measurement on which all of the Rou) - 0 5 10 15 20u 25 30 35 genetic variance is additive. Because some of the distribu- 0/0 tions in Fig. 1 are truncated by the lower limit for expression 40 , of the trait at zero cilia, a suitable criterion for additivity of F1 20 autosomal genes in the crosses is that the average B2 proge- Fl(402) 0k ny fathered by F1 males (from either reciprocal cross) should 0 10 15 20 5 be intermediate between the average of the P2 stock and the 80 average F1 progeny obtained from P2 females x P1 males. 60 Males from these three populations, with distributions that p are not truncated by the threshold at zero cilia, all have X 40 1 KAHUKU 2 KILAUEA (40) chromosomes from the hairy stock and differ only in the ge- 20 (40) netic composition of their autosomes. I. m 4j rm 5 10 15 20 25 30 35 Wright (chapter 10 in ref. 14) described a method of deter- mining a scale transformation for a set of populations that FIG. 1. Distributions of cilia counts for male progeny in crosses tends to equalize the variances of populations with different between stocks of the bare and hairy races of D. silvestris. Sample mean values; in many cases this transformation also pro- sizes are given in parentheses. Families containing 20 individuals duces approximate additivity of mean values in crosses be- were pooled to produce the distributions, except for the parental tween populations. Wright's method consists of linear re- stocks from which individuals were sampled at random. Backcross gression of the standard deviations of the populations on distributions (B1 = F1 x P1 and B2 = F1 x P2) are each composed of two families from F1 males and two families from F1 females, with their mean values. The intercept of the regression line on the parents from the appropriate reciprocal cross indicated by dashed or axis of mean values becomes the constant L in the scale solid lines. F2 families were produced by sib mating within F1 fam- transformation x' = log(x - L).
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