Whittle, C. | bioRxiv Science

bioRxiv2023

Gene protein sequence evolution can predict the rapid divergence of ovariole numbers in Drosophila

Ovaries play key roles in fitness and evolution: they are essential female reproductive structures that develop and house the eggs in sexually reproducing animals. In Drosophila, the mature ovary contains multiple tubular egg-producing structures known as ovarioles. Ovarioles arise from somatic cellular structures in the larval ovary called terminal filaments, formed by terminal filament cells and subsequently enclosed by sheath cells. As in many other insects, ovariole number per female varies extensively in Drosophila. At present however, there is a striking gap of information on genetic mechanisms and evolutionary forces that shape the well-documented rapid interspecies divergence of ovariole numbers. To address this gap, here we studied genes associated with D. melanogaster ovariole number or functions based on recent experimental and transcriptional datasets from larval ovaries, including terminal filaments and sheath cells, and assessed their rates and patterns of molecular evolution in five closely related species of the melanogaster subgroup that exhibit species-specific differences in ovariole numbers. From comprehensive analyses of protein sequence evolution (dN/dS), branch-site positive selection, expression specificity (tau) and phylogenetic regressions (PGLS), we report evidence of 42 genes that showed signs of playing roles in the genetic basis of interspecies evolutionary change of Drosophila ovariole number. These included the signalling genes upd2 and Ilp5 and extracellular matrix genes vkg and Col4a1, whose dN/dS predicted ovariole numbers among species. Together, we propose a model whereby a set of ovariole-involved gene proteins have an enhanced evolvability, including adaptive evolution, facilitating rapid shifts in ovariole number among Drosophila species. Significance StatementOvaries in Drosophila, like in other insects, contain egg producing structures, known as ovarioles. The number of ovarioles per female varies among Drosophila species, but little is known about the genes and evolutionary dynamics that may shape interspecies changes in ovariole numbers. Here, used a priori experimental and transcriptome data from D. melanogaster to identify genes involved in ovariole formation and functions, and studied their molecular evolution among its closely related species within the melanogaster subgroup. Using a multi-layered analysis consisting of protein sequence divergence (dN/dS), adaptive evolution, expression breadth, and phylogenetic regressions, we identified 42 genes whose molecular evolution patterns were well linked to ovariole numbers divergence. Further, gene protein sequence divergence was often predictive of species ovariole numbers.

evolutionary biology↗

bioRxiv2020

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

BackgroundFor multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems. ResultsHere, we rigorously studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain, ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were largely shaped by selection, and their identities were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization. ConclusionsCollectively, the results strongly suggest that codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNAs abundances, as well as amino acid use, have been adapted for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

genomics↗