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

Abstract

Sex‐biased gene expression, particularly sex‐biased expression in the gonad, has been linked to rates of protein sequence evolution (nonsynonymous to synonymous substitutions, dN/dS) in animals. However, in insects, sex‐biased expression studies remain centred on a few holometabolous species. Moreover, other major tissue types such as the brain remain underexplored. Here, we studied sex‐biased gene expression and protein evolution 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, we report several core findings. Firstly, testis‐biased genes had accelerated evolution, as compared to ovary‐biased and unbiased genes, which was associated with positive selection events. Secondly, although sex‐biased brain genes were much less common than for the gonad, they exhibited a striking tendency for rapid protein sequence evolution, an effect that was stronger for the female than male brain. Further, some sex‐biased brain genes were linked to sexual functions and mating behaviours, which we suggest may have accelerated their evolution via sexual selection. Thirdly, a tendency for narrow cross‐tissue expression breadth, suggesting low pleiotropy, was observed for sex‐biased brain genes, suggesting relaxed purifying selection, which we speculate may allow enhanced freedom to evolve adaptive protein functional changes. The findings of rapid evolution of testis‐biased genes and male and female‐biased brain genes are discussed with respect to pleiotropy, positive selection and the mating biology of this cricket.

Dissecting cricket genomes for the advancement of entomology and entomophagy

“…Studies on CpG depletion, considered a reliable indicator of DNA methylation, have revealed that DNA methylated genes tend to perform housekeeping functions across insects including holometabolous and hemimetabolous ones (Ylla et al 2021). In addition to the epigenomics described above, the genome and transcriptome in crickets have been used for studying the sex-biased gene expression regulation, which is linked to protein sequence evolution (Whittle et al 2021a) and the relationship between codon usage frequency and expression level in different tissues and sexes (Whittle et al 2021b).…”

oskaracts with the transcription factor Creb to regulate long-term memory in crickets

“…To check the expression of G. bimaculatus genes in nervous systems in wild-type animals, previously generated mRNA-seq libraries were used 37 and the complete CDS for genes of interest were obtained from the recently published genome 33 . Reads were trimmed with Cutadapt v3.4 64 , and mapped to the full G. bimaculatus CDS using Geneious Read Mapper 70 .…”

“…Table S4 . Gene expression levels for osk , piwi, vasa , and CrebA/B (in FPKM per tissue) from brain and ventral cord transcriptomes of male and female adult Gryllus bimaculatus 37 . Gene IDs as per the annotated cricket genome 36 .…”

PlantTribes2: Tools for comparative gene family analysis in plant genomics

“…Finally, protein multiple sequence alignments of orthogroups are estimated and trimmed using MAFFT ( Katoh and Standley, 2013 ) and trimAL ( Capella-Gutiérrez et al., 2009 ) respectively, to aid in identifying targeted assembled transcripts that are orthologous to the scaffold reference gene models based on the global sequence alignment coverage. A list of AssemblyPostProcessor use cases include: (1) processing de novo transcriptome assemblies to improve transcript qualities for downstream analyses ( Honaas et al., 2016 ; Yang et al., 2019 ; Whittle et al., 2021 ; and example in section 3.2.1); (2) generating matching coding sequences (CDSs) and peptide sequences in genomes with only mRNA sequences (e.g., the Malus domestica GDDH13 annotation provided only mRNA sequences but not CDSs, Daccord et al., 2017 ) and gene information gathered from databases lacking a uniformed naming system and processing protocols - for instance, the numbers of CDSs and peptides do not match in the Pyrus pyrifolia ‘Cuiguan’ genome, and the peptides are named differently from the CDSs ( Gao et al., 2021 ). The AssemblyPostProcessor -generated matching CDS and peptide sequences from the aforementioned Malus and Pyrus genomes among others provided a good starting point for the comparative genomic analyses described in section 3.2.2 and 3.2.3.…”