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.

Figure 1.—

Response to artificial selection for male sex comb bristle number in D. melanogaster. Mean sex comb bristle numbers in high (square), low (circle), and control (triangle) lines over 24 generations in (A) replicate 1 and (B) replicate 2. Solid lines with solid symbols indicate artificial selection lines and dashed lines with open symbols indicate relaxed sublines. Error bars represent standard deviation.

Figure 2.—

Forelegs of males (showing sex comb) and females (showing TBRs) from high, control, and low lines of D. melanogaster after 24 generations of artificial selection. Bristle number of the foreleg is indicated at the bottom left.

Figure 3.—

Correlated responses to divergent selection for sex comb bristle number. Mean sex comb bristle numbers are plotted against (A) mean female distal TBR bristle numbers, (B) mean male abdominal bristle numbers, and (C) mean male sternopleural bristle numbers of high (square), low (circle), and control (triangle) lines at generation 24 in replicate 1 (open) and replicate 2 (solid). Error bars represent standard deviation.

Figure 4.—

Numbers of high-scoring (h) and low-scoring (l) males that were successful in mating trials conducted within each selection line. Mean (±SE) and range of sex comb bristle numbers of all (30) males from each class are indicated above bars.

Figure 5.—

Mean number of progeny (±SE) sired by high-scoring (h) and low-scoring (l) males from within each selection line. Mean (±SE) and range of sex comb bristle numbers of all (30) males from each class are indicated above bars.