Immunogenic males: a genome‐wide analysis of reproduction and the cost of mating in Drosophila melanogaster females

Abstract

In Drosophila melanogaster, mating radically transforms female physiology and behaviour. Post‐mating responses include an increase in the oviposition rate, a reduction in female receptivity and an activation of the immune system. The fitness consequences of mating are similarly dramatic – females must mate once in order to produce fertile eggs, but additional matings have a clear negative effect. Previously, microarrays have been used to examine gene expression of females differing in their reproductive status with the aim of identifying genes influenced by mating. However, as only virgin and single mated females were compared, transcriptional changes associated with reproduction (under natural selection) and male‐induced effects (possibly under sexually antagonistic selection) cannot be disentangled. We partitioned these fundamentally different effects by instead examining the expression profiles of virgin, single mated and double mated females. We found substantial effects relating to reproduction and further effects that are only attributable to mating itself. Immune response genes dominate this male‐induced effect indicating that the cost of mating may be due partly to this system’s activation. We propose that both sexually antagonistic and natural selection have been important in the evolution of the innate immunity genes, thereby contributing to the sexual dimorphism and rapid evolution at these loci.

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

“…Hollis et al [67] examined expression profiles from unmated male and female flies and found a general pattern of feminization of the sex-biased genes in monogamous populations, consistent with predictions from sexual 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]).…”

“…We compared the expression profile of these transcripts with the female post-mating response characteristic to the ancestral population [44], and found that the expression level of 728 genes is altered in monogamous females to a lesser extent after mating, compared to promiscuous females (hereafter 'virgin-like', see Methods), while the post-mating reaction of the remaining 413 genes is altered to a higher extent in monogamous females compared to promiscuous females (hereafter 'mated-like'), and their proportion is higher than expected by chance (Binomial test: ratio = 0.64, P < 0.0001). In general, genes that are down-regulated in monogamous vs. promiscuous mated females tend to be switched on (up-regulated) by mating (two-tailed MR-GSE test: P < 0.0001, Figure 4A) and genes that are up-regulated in monogamous vs. promiscuous mated females tend to be switched off (downregulated) by mating (two-tailed MR-GSE test: P < 0.0001, Figure 4A).…”

“…In recent years, considerable quantities of data have been collected on the female physiological changes associated with the shifts in female mating status. Molecular and genomics techniques have been employed to investigate the effects of mating in D. melanogaster [40][41][42][43][44]. In particular, several detailed studies have focused on seminal fluid components on female post-mating physiology, leading to the identification of several seminal fluid proteins (SFP) and to the isolation of their effect in females reviewed in [45,46], including the characterization of sex-peptide and its receptor [47,48].…”

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

“…Less is known about the responses to mating in males, although they are predicted to primarily involve the replenishment of sperm and seminal fluid storage (Sirot, Buehner, Fiumera, & Wolfner, 2009). Several studies using Drosophila melanogaster have aimed to uncover the gene products that respond to mating, although these studies have examined males and females separately (Dalton et al., 2010; Ellis & Carney, 2010; Innocenti & Morrow, 2009; Lawniczak & Begun, 2004). …”

The genomic response to courtship song stimulation in femaleDrosophila melanogaster

“…Recent studies of female Drosophila have identified male-induced molecular changes associated with a response to sperm and accessory gland proteins, many of which appear to be under antagonistic sexual selection [10,11]. Do changes start to occur during courtship, in anticipation of mating?…”