Evolutionary changes in gene expression profiles associated with the coevolution of male and female genital parts among closely related ground beetle species

Abstract

Background: The coevolutionary dynamics of corresponding male and female sexual traits, including genitalia, may be driven by complex genetic mechanisms. Carabus (Ohomopterus) ground beetles show correlated evolution in the size of their functionary corresponding male and female genital parts. To reveal the genetic mechanisms involved in the evolution of size, we investigated interspecific differences in gene expression profiles in four closely related species (two species each with long and short genital parts) using transcriptome data from genital tissues in the early and late pupal stages. Results: We detected 1536 and 1306 differentially expressed genes (DEGs) among the species in males and 546 and 1959 DEGs in females in the two pupal stages, respectively. The DEGs were clustered by species-specific expression profiles for each stage and sex to identify candidate gene clusters for genital size based on the expression patterns among the species and gene ontology. We identified one and two gene clusters in females and males, respectively, all from the late pupal stage; one cluster of each sex showed similar expression profiles in species with similar genital size, which implies a common genetic control mechanism in each sex. However, the remaining male cluster showed different expression profiles between species with long genital parts, which implies species-specific genetic mechanisms. These clusters did not show sex-concordant expression profiles for genital size differences. Conclusion: Our study demonstrates that sex-independent and partly species-specific genetic mechanisms underlie the correlated evolution of male and female genital size. These results may reflect the complex evolutionary history of male and female genitalia.