Abstract
For most arthropod species, male genital size is relatively implastic in response to variation in developmental nutrition, such that the genitals in large well-fed males are similar in size to those in small poorly-fed males. In Drosophila melanogaster, reduced nutritional plasticity of the male genitalia is a consequence of low insulin sensitivity through a tissue-specific reduction in the expression of FOXO, a negative growth regulator . Despite an understanding of the proximate developmental mechanisms regulating organ size, the ultimate evolutionary mechanisms that may have led to reduced FOXO expression in the genitalia have not been fully elucidated. Here we show that restoring FOXO activity in the developing genitalia reduces the male genital size and decreases various aspects of male reproductive success. These data support the hypothesis that sexual selection has acted on the male genitalia to limit their nutritional plasticity through a reduction in FOXO expression, linking proximate with ultimate mechanisms of genital evolution.
Highlights
In most animals, body proportion stays relatively consistent across a range of body sizes in a population, such that both large and small individuals have the same shape
Perhaps the best studied hypoallometric traits are arthropod genitalia, and there are a number of alternative hypotheses to account for their low covariance with body size, most proposing reduced reproductive success in males with atypically sized genitalia [4,5,6]
While increasing FOXO expression in the posterior lobe restores nutritional sensitivity [10], it is unclear what impact this has on male mating success. We addressed this question by upregulating both FOXO and insulin-receptor (InR) activity in the posterior lobe of the genital arch alone, imposing changes in IIS to produce males with an expanded range of genital sizes beyond that found in wild-type populations, including very small genitalia
Summary
Body proportion stays relatively consistent across a range of body sizes in a population, such that both large and small individuals have the same shape. Perhaps the most obvious examples are of exaggerated secondary sexual characteristics used by males to compete for females, e.g. the horns of rhinoceros beetles and stalked eyes of diopsid flies [1,2]. These traits are disproportionally large in larger individuals and referred to as hyperallometric traits. Less charismatic but probably more prevalent are traits that show the opposite pattern and are disproportionally small in larger individuals, referred to as hypoallometric traits, e.g. brain size in mammals and genital size in male arthropods [3,4]. Because hypoallometric traits show relatively little variation in a population, testing the effects of their size on fitness is challenging
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