Comparative Transcriptomics in Two Bivalve Species Offers Different Perspectives on the Evolution of Sex-Biased Genes

Abstract

Comparative genomics has become a central tool for evolutionary biology, and a better knowledge of understudied taxa represents the foundation for future work. In this study, we characterized the transcriptome of male and female mature gonads in the European clam Ruditapes decussatus, compared with that in the Manila clam Ruditapes philippinarum providing, for the first time in bivalves, information about transcription dynamics and sequence evolution of sex-biased genes. In both the species, we found a relatively low number of sex-biased genes (1,284, corresponding to 41.3% of the orthologous genes between the two species), probably due to the absence of sexual dimorphism, and the transcriptional bias is maintained in only 33% of the orthologs. The dN/dS is generally low, indicating purifying selection, with genes where the female-biased transcription is maintained between the two species showing a significantly higher dN/dS. Genes involved in embryo development, cell proliferation, and maintenance of genome stability show a faster sequence evolution. Finally, we report a lack of clear correlation between transcription level and evolutionary rate in these species, in contrast with studies that reported a negative correlation. We discuss such discrepancy and call into question some methodological approaches and rationales generally used in this type of comparative studies.

The dynamics of mito-nuclear coevolution: A perspective from bivalve species with two different mechanisms of mitochondrial inheritance

“…Similar results were obtained by Havird and Sloan (2016) who analyzed 84 eukaryotic taxa and concluded that transcript abundance cannot be responsible for dN/dS. Moreover, Ghiselli et al (2018)-who analyzed sequence evolution and transcription level in sex-biased nuclear genes-already discussed the need to be careful in searching for a causal correlation between these two variables, and here, we confirm no evidence for E-R correlation. Also, our results show that transcription level of both nuclear and mitochondrial subunits is highly variable, and it is not uniform even across samples within species-despite using the same tissue at the same stage of life cycle.…”

“…Transcriptome data of mature gonads from 12 individuals (six females and six males) of R. decussatus and 12 individuals (six females and six males) of R. philippinarum were retrieved from Ghiselli et al. (). Raw reads and transcriptome assembly from both experiments are available on NCBI, under BioProjects PRJNA68513 ( R. philippinarum ) and PRJNA170478 ( R. decussatus ); further data are available on figshare: https://doi.org/10.6084/m9.figshare.5398618.v1.…”

“…Both transcriptomes of R. decussatus and R. philippinarum were previously annotated in Ghiselli et al. (). In order to identify genes involved in mitochondrial processes, we used AmiGO2 (Balsa‐Canto, Henriques, Gábor, & Banga, ) to select loci annotated with the GO term “Mitochondrion” and every associated child term in both transcriptomes.…”

“…Transcriptome data of mature gonads from 12 individuals (six females and six males) of R. decussatus and 12 individuals (six females and six males) of R. philippinarum were retrieved from Ghiselli et al (2018). The clams were collected from the Northern Adriatic Sea, in the river Po delta region (Sacca di Goro, approximate GPS coordinates: 44º50′06″N, 12º17′55″E).…”

“…Filtered reads were assembled with Trinity-v2.4.0. For technical details about transcriptome de novo assembly refer to Ghiselli et al (2018).…”