Polymorphism in a metabolic gene involved in sexual selection shapes global gene expression profiles in the bulb mite males

Uncovering the genetic basis of sexually selected traits and traits involved in sexual conflict is a key to understand the association between sexual and non-sexual fitness. 6-phosphogluconate dehydrogenase (6Pgdh) is a metabolic gene associated with pentose phosphate pathway. It was shown to be involved in sexual selection and conflict in bulb mite, Rhizoglyphus robini. Two previously identified 6Pgdh genotypes are associated with variation in male reproductive fitness: the "winning" 6Pgdh allele (S) confers advantage in male reproductive success compared to the alternative F allele, but mating with S-bearing males decreases female fecundity. Physiological mechanisms of these differences remain a puzzle. We compare gene expression patterns between males from the S- and F-allele homozygous lines to identify which molecular pathways are affected by 6Pgdh polymorphism. Moreover, we test for linkage disequilibrium in gene-coding regions associated with genetic polymorphism in 6Pgdh and show that polymorphism in 6Pgdh is in linkage disequilibrium with nonsynonymous single nucleotide polymorphisms in five genes, four of which are located within the same chromosome. We show that male genotype in 6Pgdh is associated with differential expression of genes distributed throughout the whole genome. Among differentially expressed genes, we found overrepresentation of several categories associated with fructose metabolism, including an enzyme associated with both pentose phosphate metabolism and glycolysis. Differential expression in genes associated with a number of other general categories highlight the connection between sexual fitness and gene expression in a number of important pathways, potentially affecting performance of a whole organism.