Quantitative evolutionary genomics: differential gene expression and male reproductive success inDrosophila melanogaster

Abstract

We combined traditional quantitative genetics and oligonucleotide microarrays to examine withinpopulation genetic variation in a trait closely related to fitness. The trait, male reproductive success under competitive conditions (MCRS), is of central importance to both life-history and sexual-selection theory. We identified 27 candidate genes whose expression levels were associated with within-population variation in MCRS. 'High' MCRS was associated with low expression of a cytochrome P450 that causes pesticide resistance, suggesting a fitness cost to resistance. Two groups of metabolic proteins (glutathione transferases and phosphatases) were significantly over-represented, and a large portion of the candidates are genes involved in oxidative stress resistance, energy acquisition or energy storage. Genes expressed in accessory glands and testes were not over-represented among differentially expressed genes, but testis-expressed genes were significantly more likely to be upregulated in high MCRS genotypes. Finally, nine candidate genes that we identified had no previous functional annotation, and this experiment suggests that they play a role in male reproductive success.

QUANTITATIVE TRAIT LOCUS ANALYSIS OF MALE MATING SUCCESS AND SPERM COMPETITION INDROSOPHILA MELANOGASTER

“…However, none of these genes was significantly associated with male reproductive success in the Ives population (Drnevich et al 2004).…”

“…Although expression differences may not be the causative factor underlying the QTL effects on this trait, these results suggest that the three genes listed in Table 4 warrant further investigation as candidate genes for variation in male reproductive fitness. Unfortunately, no functional annotation is currently available for any of these genes, although it is known that CG15200 is expressed in testes (Boutanaev et al 2002) and CG11699 is expressed in the male accessory glands, which produce seminal fluid (Drnevich et al 2004).…”

“…Finally, we compared our QTL results to previous investigations of male traits that used the same mapping population and to two studies of differential gene expression in adult males. One of the expression studies (Gibson et al 2004) compared mRNA expression in the parental lines used to create the RILs that we used for our mapping study; the other (Drnevich et al 2004) reported variation in gene expression that was significantly associated with male reproductive success within a randomly mating population (the Ives population).…”

“…Quantitative genetic analyses of a randomly mating population have supported similar conclusions: that genetic variation for first-male mating success is largely additive and that the amount of vari- Mackay et al (2005). 4 Tissue-specific expression: M, male accessory gland (Drnevich et al 2004); T, testis (Boutanaev et al (2002).…”

“…A second study of flies derived from a natural population found that single-nucleotide polymorphism (SNP) in six ACP genes was associated with variation in sperm competition or mating success (Fiumera et al 2005). Using a different approach (microarray analysis), Drnevich et al (2004) identified 27 candidate genes for male reproductive success in D. melan-ogaster. None of the genes identified by microarrays were ACPs, and genes expressed in male accessory glands or testes were not overrepresented among genes implicated in fitness variation.…”