Abstract
BackgroundSpermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates. Although Hymenopterans share many characteristics with other organisms, their complex haplodiploid reproduction system is still relatively unknown. However, they serve as a complementary insect model to Drosophila for studying functional male fertility. In this study, we used a comparative method combining taxonomic, phenotypic data and gene expression to identify candidate genes that could play a significant role in spermatogenesis in hymenopterans.ResultsOf the 546 mouse genes predominantly or exclusively expressed in the mouse testes, 36% had at least one ortholog in the fruit fly. Of these genes, 68% had at least one ortholog in one of the six hymenopteran species we examined. Based on their gene expression profiles in fruit fly testes, 71 of these genes were hypothesized to play a marked role in testis function. Forty-three of these 71 genes had an ortholog in at least one of the six hymenopteran species examined, and their enriched GO terms were related to the G2/M transition or to cilium organization, assembly, or movement. Second, of the 379 genes putatively involved in male fertility in Drosophila, 224 had at least one ortholog in each of the six Hymenoptera species. Finally, we showed that 199 of these genes were expressed in early pupal testis in Nasonia vitripennis; 86 exhibited a high level of expression, and 54 displayed modulated expression during meiosis.ConclusionsIn this study combining phylogenetic and experimental approaches, we highlighted genes that may have a major role in gametogenesis in hymenopterans; an essential prerequisite for further research on functional importance of these genes.
Highlights
Spermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates
We performed a phylogenetic metaanalysis of functional data from the fruit fly (Drosophila melanogaster) to identify genes with high expression levels in vertebrates, and we found that the expression of these genes was highly conserved in the testis (81%) [22]
We focused on genes that are predominantly expressed in the mouse testis, based on the hypothesis that high expression levels may reveal functional relevance; we subsequently searched for orthologs in the fruit fly (D. melanogaster) and in six hymenopterans (Apis mellifera, Atta cephalotes, Bombus terrestris, Bombus impatiens, Nasonia vitripennis, and Solenopsis invicta) (Figs. 2 and 3)
Summary
Spermatogenesis appears to be a relatively well-conserved process even among distantly related animal taxa such as invertebrates and vertebrates. Hymenopterans share many characteristics with other organisms, their complex haplodiploid reproduction system is still relatively unknown. They serve as a complementary insect model to Drosophila for studying functional male fertility. The insect order Hymenoptera contains more than 150,000 described species and potentially around 850,000 undescribed species [1, 2] This taxon includes all wasps, bees, and ants and represents approximately 8% of all described species [3]. It is important to understand how haploid males produce sperm and to identify the genes involved in this process in order to study functional male fertility in hymenopterans, a group containing many species of agricultural significance
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