The Genetic Architecture of Ovariole Number in Drosophila melanogaster: Genes with Major, Quantitative, and Pleiotropic Effects

Abstract

Ovariole number has a direct role in the number of eggs produced by an insect, suggesting that it is a key morphological fitness trait. Many studies have documented the variability of ovariole number and its relationship to other fitness and life-history traits in natural populations of Drosophila However, the genes contributing to this variability are largely unknown. Here, we conducted a genome-wide association study of ovariole number in a natural population of flies. Using mutations and RNAi-mediated knockdown, we confirmed the effects of 24 candidate genes on ovariole number, including a novel gene, anneboleyn (formerly CG32000), that impacts both ovariole morphology and numbers of offspring produced. We also identified pleiotropic genes between ovariole number traits and sleep and activity behavior. While few polymorphisms overlapped between sleep parameters and ovariole number, 39 candidate genes were nevertheless in common. We verified the effects of seven genes on both ovariole number and sleep: bin3, blot, CG42389, kirre, slim, VAChT, and zfh1 Linkage disequilibrium among the polymorphisms in these common genes was low, suggesting that these polymorphisms may evolve independently.

Keywords: Drosophila melanogaster; genome-wide association study; ovariole number; sleep.

Figure 1

Variation in ovariole number in the DGRP. Histogram of (A) ovariole number and (B) ovariole number CV_E line means. Mean and SE of (C) ovariole number and (D) ovariole number CV_E.

Figure 2

Variation in ovariole asymmetry in the DGRP. Histogram of (A) ovariole asymmetry and (B) ovariole asymmetry CV_E line means. Mean and SE of (C) ovariole asymmetry and (D) ovariole asymmetry CV_E.

Figure 3

Partitioning of variance components for ovariole phenotypes.

Figure 4

Impact of major effect genes on ovary morphology and female fecundity. (A) anneboleyn mutant, and (B) zfh1 knockdown ovary morphology; (C) anneboleyn mutant, and (D) zfh1 knockdown offspring production.