A primary role of developmental instability in sexual selection

Abstract

In evolutionary biology, fluctuating asymmetry (FA) is thought to reveal developmental instability (DI, inability to buffer development against perturbations), but its adaptive and genetic bases are being debated. In other fields, such as human clinical genetics, DI is being assessed as incidence of minor morphological abnormalities (MMAs) and used to predict certain fitness outcomes. Here, for the first time, we combine these complementary measures of DI in sexual selection and quantitative genetic studies of a natural population. Comprehensive multivariate analyses demonstrate that FA and MMAs in a conditiondependent sexual ornament, the male Drosophila bipectinata sex comb used in courtship, are sole significant targets of selection favouring their reduced expression in New Caledonia. Comb FA and MMAs are positively correlated, confirming that each are linked to a common buffering system. Ornament size and DI (as FA and MMAs) are positively correlated, genetically and phenotypically, contrary to theoretical expectation of negative size-FA scaling under the assumption that FA reveals overall genetic quality. There exists significant additive genetic variance for MMAs, demonstrating their evolutionary potential. Ornament DI in New Caledonia is markedly elevated compared with populations where such selection was not detected, suggesting that the increased population-level DI is capacitating adaptive evolution.

Fluctuating Asymmetry: Methods, Theory, and Applications

“…Moreover, fluctuating asymmetry and phenodeviants in Drosophila bipectinata share a common buffering system [176]. Understanding the underlying basis of developmental instability is critically important to the future development of the field [105].…”

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

“…However, a lack of condition dependence is not the case for the sex comb in D. bipectinata. In fact sex comb size is both heritable and condition dependent, and therefore not surprisingly, also under sexual selection in some populations [35,36]. Condition dependence of the sex comb has been demonstrated in a previous study, in which increased temperature applied during larval development decreased sex comb size [28].…”

“…These negative relationships suggest that FA is influenced by a multitude of loci throughout the genome, as body size in Drosophila and other organisms is a complex, multifactorial trait related to fitness [51][52][53][54]. Interestingly, in a field study in New Caledonia, where FA was strongly and consistently shown to be the target of sexual selection, it was FA1, not FA2 or comb size, that predicted male mating success [36]. These differential effects on mating success further support the view that FA and comb size tap distinct properties of the genome.…”

“…Sex comb size is heritable [28,35,36] and found to be the target sexual selection [35], suggesting that the likely cause of this pronounced inter-population differentiation is sexual selection, although other micro-evolutionary factors, such as genetic drift, may be involved. In addition to significant differences in trait size, we also found significant differences in FA among the populations, with mean FA being greatest in the Hiva Oa population.…”

“…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.…”