Role of Sex-Concordant Gene Expression in the Coevolution of Exaggerated Male and Female Genitalia in a Beetle Group

Abstract

Some sexual traits, including genitalia, have undergone coevolutionary diversification toward exaggerated states in both sexes among closely related species, but the underlying genetic mechanisms that allow correlated character evolution between the sexes are poorly understood. Here, we studied interspecific differences in gene expression timing profiles involved in the correlated evolution of corresponding male and female genital parts in three species of ground beetle in Carabus (Ohomopterus). The male and female genital parts maintain morphological matching, whereas large interspecific variation in genital part size has occurred in the genital coevolution between the sexes toward exaggeration. We analyzed differences in gene expression involved in the interspecific differences in genital morphology using whole transcriptome data from genital tissues during genital morphogenesis. We found that the gene expression variance attributed to sex was negligible for the majority of differentially expressed genes, thus exhibiting sex-concordant expression, although large variances were attributed to stage and species differences. For each sex, we obtained co-expression gene networks and hub genes from differentially expressed genes between species that might be involved in interspecific differences in genital morphology. These gene networks were common to both sexes, and both sex-discordant and sex-concordant gene expression were likely involved in species-specific genital morphology. In particular, the gene expression related to exaggerated genital size showed no significant intersexual differences, implying that the genital sizes in both sexes are controlled by the same gene network with sex-concordant expression patterns, thereby facilitating the coevolution of exaggerated genitalia between the sexes while maintaining intersexual matching.

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

“…iwawakianus , and C . uenoi ), as seen in a previous study [ 24 ] (see Table S 5 ). In FLP1, we focused on dimm (TF), Fhos (involved in imaginal disc development), and Cpr56F (involved in cuticle development), which showed different expression profiles between species with different vaginal appendix lengths.…”

“…iwawakianus , and C . uenoi ) with different genital sizes and morphologies, as seen in our previous study [ 24 ] (see Table S 4 ). In MPL4, bun (TF) and CG14073 , Usp8 , and cmb (genes involved in imaginal disc development) were differentially expressed between Ar and Ko and between Ar and Es.…”

“…Obst-A is involved in chitin-based cuticle development [ 28 ]. Genes involved in cuticle development may affect the morphology of species-specific copulatory pieces in other Ohomopterus species [ 15 , 24 ], and obst-A may underlie the interspecific differences in copulatory piece length seen in our study species. Although MED24 and obst-A are not known for their effects on genital morphology in Drosophila [ 29 ], these genes may be involved in differences in copulatory piece length between species with long (Ar and In) and short (Ko and Es) copulatory pieces.…”

“…iwawakianus , and C . uenoi , which occur in the western part of the range of the iwawakianus - insulicola group [ 14 , 15 , 23 , 24 ]. Fujisawa et al [ 15 ] performed a genomic comparison with QTL mapping analyses and detected six genomic regions and 21 genes that might control male and female genital size in C .…”

“…maiyasanus . Nomura et al [ 24 ] compared gene expression profiles in genital morphogenesis among the three species and suggested that different sets of genes showing sex-discordant expression changes were important for the evolution of genital size in C . maiyasanus and C .…”