RT Journal Article
SR Electronic
T1 Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2020.07.07.192039
DO 10.1101/2020.07.07.192039
A1 Carrie A. Whittle
A1 Arpita Kulkarni
A1 Cassandra G. Extavour
YR 2021
UL http://biorxiv.org/content/early/2021/04/26/2020.07.07.192039.abstract
AB Sex-biased gene expression, particularly male-biased expression in the gonad, has often been linked to rapid protein sequence evolution (nonsynonymous to synonymous substitutions, dN/dS) in animals. This evolutionary trend may arise from adaptive evolution and/or from relaxed purifying selection due to low pleiotropy. In insects, research on sex-biased transcription and dN/dS remains largely focused on a few holometabolous species, with variable findings on male and female gonadal effects. The brain provides the neurological foundation for male and female mating behaviors. However, little is known about sex-biased expression of brain genes and their rates of protein sequence evolution. Here, we studied sex-biased gene expression in a hemimetabolous insect, the cricket Gryllus bimaculatus. We generated novel male and female RNA-seq data for two sexual tissue types, the gonad and somatic reproductive system, and for two core components of the nervous system, the brain and ventral nerve cord. From a genome-wide analysis of genes expressed in these tissues, we report the accelerated evolution of testis-biased gene, as compared to ovary-biased and unbiased genes, which was associated with an elevated frequency of positive selection events. With respect to the brain, while sex-biased brain genes were much less common than for the gonads, they exhibited a striking tendency for rapid evolution, an effect that was stronger for the female than for the male brain. Certain sex-biased brain genes were predicted to be involved in mating or sex-related functions, which we suggest may cause exposure to sexual selection. A tendency for narrow cross-tissue expression breadth, suggesting low pleiotropy, was observed for sex-biased brain genes. We speculate that this feature may permit relaxed purifying selection, which in turn, may allow enhanced freedom for adaptive protein functional changes in these sex-biased genes. Our results demonstrate that sex-biased expression in the male gonad, and sex-biased expression in the brain, especially the female brain, are associated with a propensity for rapid protein sequence evolution in a cricket model system. We discuss the results with respect to our findings on pleiotropy and positive selection, and consider the plausible roles of the mating biology of this cricket in shaping the observed patterns.Competing Interest StatementThe authors have declared no competing interest.