Evolutionary dynamics of sex-biased genes expressed in cricket brains and gonads

Abstract

<jats:title>Abstract</jats:title><jats:sec><jats:title>Background</jats:title><jats:p>Sex-biased gene expression, particularly male-biased expression in the gonad, has often been linked to rapid protein sequence evolution (dN/dS) in animals. This evolutionary trend may arise from one or both of sexual selection pressures during mating or 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 is central to the mating process, and provides neurological foundation for mating behaviors, such as courtship, intrasex competition and mate choice. However, there is a striking paucity of research on sex-biased expression of genes in the brain and the rate of protein sequence evolution in such genes.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>Here, we studied sex-biased gene expression in a hemimetabolous insect, the cricket <jats:italic>Gryllus bimaculatus</jats:italic>. We generated novel 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 genes and seminal fluid proteins (SFPs) genes, as compared to ovary-biased and unbiased genes in this cricket model, which includes 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 exceptionally 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. Moreover, the sex-biased brain genes exhibited remarkably low cross-tissue expression breadth, or pleiotropy. We speculate that this feature may permit relaxed purifying selection, and allow the freedom for adaptive protein functional changes in these brain-expressed genes.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>Our results demonstrate that sex-biased expression in the male gonad, and sex-biased gene expression in the brain, especially the female brain, are associated with 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 potential role of the dynamic mating biology of this cricket model in shaping these patterns.</jats:p></jats:sec>

Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

“…Moreover, the low Fop observed in the brain (Fig. 2) suggests that Hill-Robertson effects may be greatest in this tissue type, a notion that is consistent with recent observations of a rapid rate of protein sequence evolution of sex-biased brain genes in this species [64]. It is worth noting that the finding that the degree of optimal codon use is particularly pronounced for genes transcribed in the gonads in Fig.…”

“…Gene expression was assessed using RNA-seq data from four adult male and female tissue types, the gonad (testis for males, ovaries for females), somatic reproductive system (for males this includes the pooled vasa deferentia, seminal vesicle and ejaculatory duct and for females includes the spermathecae, common oviduct, and bursa), brain and ventral nerve cord (Additional file 1: Table S1; [64]). The male accessory glands were included for study, but were separated from the other male reproductive system to prevent overwhelming, or skewing, the types of transcripts detected in the former tissues [64]. The trimmed reads in Additional file 1: Table S1 were mapped to the 15,539 annotated G. bimaculatus genes independently for each of the nine tissue types under study and the expression level, or FPKM, was determined per gene.…”

“…Gene expression level was determined for all 15,539 G. bimaculatus protein-coding genes (CDS, longest CDS per gene) [65] that had a start codon and were >150bp. RNA-seq was obtained for four adult male and female tissue types, the gonad (testis for males, ovaries for females), somatic reproductive system, brain and ventral nerve cord and for the male accessory glands (Additional file 1: Table S1) as described previously [64]. The expression level of each G.…”

“…Within insects, Gryllus is a hemimetabolous genus (Order Orthoptera) and has highly diverged from the widely studied model insect genus Drosophila (Order Diptera) [57,58]. G. bimaculatus comprises a model for investigations in genetics [59,60], germ line formation and development [61][62][63] and for molecular evolutionary biology [10,64]. In the present study, we rigorously assess codon and amino acid use in highly transcribed genes of G. bimaculatus using its recently available annotated genome [65] and large-scale RNA-seq data from tissues of the male and female reproductive and nervous systems [64].…”

“…G. bimaculatus comprises a model for investigations in genetics [59,60], germ line formation and development [61][62][63] and for molecular evolutionary biology [10,64]. In the present study, we rigorously assess codon and amino acid use in highly transcribed genes of G. bimaculatus using its recently available annotated genome [65] and large-scale RNA-seq data from tissues of the male and female reproductive and nervous systems [64]. From our analyses, we demonstrate that optimal codons, those preferentially used in highly expressed genes, occur in this organism, are largely shaped by selection pressures, and are nearly identical across tissues.…”