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.

Figure 1. Genetic variation, allometric coefficient and fluctuating asymmetry of somatic and genital traits in male Drosophila melanogaster.

(A) Genital traits had low levels of total genetic variation (light gray bars, CV_T) but not low levels of organ-autonomous genetic variation (dark gray bars, CV_I). The difference between total genetic variation and organ-autonomous variance is an estimate of genetic variation that is correlated with variation in other traits (‘systemic’ genetic variation). Columns with the same letter are not significantly different for total genetic variation (CV_T) using Tukey's HSD (P>0.05). Traits do not differ for organ-autonomous genetic variation (CV_I) using Tukey's HSD (P>0.05 for all) (B) The low systemic genetic variance of the genital traits reflected their low multivariate allometric coefficient compared to most somatic traits, although these differences are not significant for multiple comparisons (Tukey's HSD, P>0.05 for all). Grey horizontal line is isometry. (C) Genital traits did not show low levels of fluctuating asymmetry. Light grey bars, line 303, white bars, line 324, dark grey bars, line 335. Within a line, columns with the same letter are not significantly different for FA using Tukey's HSD (P 0.05). All error bars are 95% confidence intervals.

Figure 2. Model of a selection regime that alters the slope of the genital-body scaling relationship while maintaining genital-autonomous genetic variation.

Selection is for proportionally smaller genitalia in large males and proportionally larger genitalia in small males (black arrows). Implicit to such a regime is that there is selection or constraint maintaining variation in body size (gray arrows).