The Effect of Genetic and Environmental Variation on Genital Size in Male Drosophila: Canalized but Developmentally Unstable

Abstract

The genitalia of most male arthropods scale hypoallometrically with body size, that is they are more or less the same size across large and small individuals in a population. Such scaling is expected to arise when genital traits show less variation than somatic traits in response to factors that generate size variation among individuals in a population. Nevertheless, there have been few studies directly examining the relative sensitivity of genital and somatic traits to factors that affect their size. Such studies are key to understanding genital evolution and the evolution of morphological scaling relationships more generally. Previous studies indicate that the size of genital traits in male Drosophila melanogaster show a relatively low response to variation in environmental factors that affect trait size. Here we show that the size of genital traits in male fruit flies also exhibit a relatively low response to variation in genetic factors that affect trait size. Importantly, however, this low response is only to genetic factors that affect body and organ size systemically, not those that affect organ size autonomously. Further, we show that the genital traits do not show low levels of developmental instability, which is the response to stochastic developmental errors that also influence organ size autonomously. We discuss these results in the context of current hypotheses on the proximate and ultimate mechanisms that generate genital hypoallometry.

Plastic flies

“…On the other hand, male genital size shows low levels of variability in response to both sources of environmental variation and also in response to genetic variation, supporting a common mechanism. 13 To muddy the waters further, wing size is more developmentally stable, and shows lower levels of fluctuating asymmetry, than genital size. 13 The ambiguity of our data concerning the existence of a universal buffering mechanism reflects the wider literature, with some studies supporting the hypothesis 9,11,14 and others rejecting it.…”

“…13 To muddy the waters further, wing size is more developmentally stable, and shows lower levels of fluctuating asymmetry, than genital size. 13 The ambiguity of our data concerning the existence of a universal buffering mechanism reflects the wider literature, with some studies supporting the hypothesis 9,11,14 and others rejecting it. 7,8,15 These studies (ours included) are essentially correlative, comparing and contrasting variability in different traits in response to different environmental and genetic perturbations.…”

“…12 They also show reduced variability in response to genetic variation, relative to other organs. 13 Importantly, this reduction in variability is only in response to genetic variation that acts systemically, that is variation that affects the size of all organs in the body in a coordinated manner. 13 Such variation may result from, for example, allelic variation in the IIS pathway.…”

“…13 Importantly, this reduction in variability is only in response to genetic variation that acts systemically, that is variation that affects the size of all organs in the body in a coordinated manner. 13 Such variation may result from, for example, allelic variation in the IIS pathway. In contrast, the genitals do not show reduced variability in response to genetic factors that affect organ size autonomously, that is variation that is not correlated with variation in the size of any other organ.…”

“…In contrast, the genitals do not show reduced variability in response to genetic factors that affect organ size autonomously, that is variation that is not correlated with variation in the size of any other organ. 13 Such variation may result from, for example, allelic variation in the genes that pattern specific organs. The genitalia also do not show reduced levels of developmental instability.…”