Female responses to experimental removal of sexual selection components in Drosophila melanogaster

Abstract

Background: Despite the common assumption that multiple mating should in general be favored in males, but not in females, to date there is no consensus on the general impact of multiple mating on female fitness. Notably, very little is known about the genetic and physiological features underlying the female response to sexual selection pressures. By combining an experimental evolution approach with genomic techniques, we investigated the effects of single and multiple matings on female fecundity and gene expression. We experimentally manipulated the opportunity for mating in replicate populations of Drosophila melanogaster by removing components of sexual selection, with the aim of testing differences in short term post-mating effects of females evolved under different mating strategies.

Results: We show that monogamous females suffer decreased fecundity, a decrease that was partially recovered by experimentally reversing the selection pressure back to the ancestral state. The post-mating gene expression profiles of monogamous females differ significantly from promiscuous females, involving 9% of the genes tested (approximately 6% of total genes in D. melanogaster). These transcripts are active in several tissues, mainly ovaries, neural tissues and midgut, and are involved in metabolic processes, reproduction and signaling pathways.

Conclusions: Our results demonstrate how the female post-mating response can evolve under different mating systems, and provide novel insights into the genes targeted by sexual selection in females, by identifying a list of candidate genes responsible for the decrease in female fecundity in the absence of promiscuity.

Figure 1

Overview of experiment . Experimental populations evolving under monogamous (M, in blue) and promiscuous (P, in red) mating systems were derived from the LH_M base population at generation GO, the reverse selection lines (MP, in black) occurred at G95. The intervals between each of the 5 female fecundity trials, as well as body size and microarray assays are also shown.

Figure 2

Female fecundity . Reproductive output of females evolved under monogamous and promiscuous selection regimes after mating once (panels B and C) or being continuously exposed to males (panels A and D), during the normal reproductive window (panel A and B; 14 individual females) or during a longer interval (4 days; panel C and D; 16 individual females). Closed circles represent median values, boxes limited to interquartile range, and whiskers at minimum and maximum values.

Figure 3

Reversed selection . Individual level reproductive output of females evolved under monogamous (M), monogamous then promiscuous (MP) and promiscuous (P) selection regimes. Results of the posthoc analysis are given above the plotting frame, letters not shared indicate treatments that show statistical significant differences (see Results for details). Closed circles represent median values, boxes limited to interquartile range, and whiskers at minimum and maximum values.

Figure 4

Association with post-mating response and female fitness . (A) Density distribution of significant up-regulated (blue) and down-regulated (red) transcripts in monogamous (versus promiscuous) females along all the tested genes, ranked according to their post-mating reaction (data from a previously published study on the same population; Innocenti and Morrow [44]). (B) Density distribution of the significant transcripts along all the tested genes, ranked by the t-value of their association with female fitness (data from a previously published study on the same population; Innocenti and Morrow [60]).

Figure 5

Transcriptional modules . Level-plot representing the matrix of pair-wise correlation for the expression of the 1141 significant transcripts across tissues of D. melanogaster data from [62]. The correlation matrix has been used to compute modules of correlated expression (separated by grey lines). The 7 modules containing more than 50 genes are labeled.