Variation and Evolution of Male Sex Combs in Drosophila: Nature of Selection Response and Theories of Genetic Variation for Sexual Traits

Abstract

We investigated the genetic architecture of variation in male sex comb bristle number, a rapidly evolving secondary sexual character of Drosophila. Twenty-four generations of divergent artificial selection for sex comb bristle number in a heterogeneous population of Drosophila melanogaster resulted in a significant response that was more pronounced in the direction of low bristle numbers. We observed a strong positive correlated response to selection in the corresponding female transverse bristle row. The correlated response in male abdominal and sternopleural bristle numbers, on the other hand, did not follow the same pattern as sex comb bristle number differences between selection lines. Relaxation-of-selection experiments along with mate choice and fecundity assays using the selection lines developed demonstrated the action of stabilizing selection on sex comb bristle number. Our results show (1) substantial genetic variation underlying sex comb bristle number variation; (2) a weak relationship between the sex comb and developmentally related, non-sex bristle systems; and (3) that sexual selection may be a driving force in sex comb evolution, indicating the potential of sex combs to diversify rapidly during population differentiation and speciation. We discuss the implications of these results for theories of genetic variation in display and nondisplay male sex traits.

Evolution of Drosophila sex comb length illustrates the inextricable interplay between selection and variation

“…S1). In artificial selection experiments in D. melanogaster, small sex combs occurred more rapidly than longer sex combs (24). Based on these experiments, we would predict that small rotating sex combs can be produced faster than long rotating sex combs in evolution.…”

“…Lines for high and low numbers of sex comb teeth were developed by artificial selection for 24 generations following the protocol described by ref. 24. The line artificially selected for high number of bristles in the sex comb and distal TR were developed through the introgression of the High line into the scd mutant for six generations.…”

“…For image acquisition, adult legs were dissected, and mounted on cover slips 22X22 mm No 1 (VWR), viewed with an Olympus BX41M and imaged with a Cool Snap camera U-CMAD (Photometrics) following protocols previously described (12,24). Angles were measured using the angle tool of Image J software (http://rsb.info.nih.gov/ij).…”

“…S1) (Any mention in this paper regarding sex comb length strictly refers to bristle number per comb). Similar to the butterfly, B. anynana (10,11), artificial selection experiments have demonstrated segregating variation for modifying sex comb tooth number in D. melanogaster (24). After short-term selection, ∼20 generations, it is possible to increase the number of sex comb teeth from 9 to 11 teeth up to 18 teeth (24).…”

Consistent Positive Co-Variation between Fluctuating Asymmetry and Sexual Trait Size: A Challenge to the Developmental Instability-Sexual Selection Hypothesis

“…D. bipectinata is a member of the ananasssae subgroup of the melanogaster species group [32], and is widely distributed in the Australian and Oriental biogeographic zones [32]. The trait under study is the male sex comb, a heritable and condition dependent secondary sexual trait [33][34][35][36] undergoing incipient diversification throughout its geographic range [35,37,38]. The sex comb consists of two major components (referred to as C1 and C2), each comprised of a row stout black bristles, or "teeth", arranged obliquely along the foretarsus of each of the front legs of males ( Figure 1); females do not possess sex combs.…”