A shared XY sex chromosome system with variable recombination rates
Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals
Recommendation: posted 13 December 2023, validated 14 December 2023
Schwander, T. (2023) A shared XY sex chromosome system with variable recombination rates. Peer Community in Evolutionary Biology, 100656. 10.24072/pci.evolbiol.100656
Many species with separate sexes have evolved sex chromosomes, with the sex-limited chromosomes (i.e. the Y or W chromosomes) exhibiting a wide range of genetic divergences from their homologous X or Z chromosomes (Bachtrog et al., 2014). Variable divergences can result from the cessation of recombination between sex chromosomes that occurred at different time points, with the mechanisms of initiation and expansion of recombination suppression along sex chromosomes remaining poorly understood (Charlesworth, 2017).
The study by Castel et al (2023) describes the serendipitous discovery of a shared XY sex chromosome system in three closely related hydrothermal vent gastropods. The X and Y chromosomes appear to still recombine but at variable rates across the three species. This variation makes the gastropod system a very promising focus for future research on sex chromosome evolution.
An additional intriguing finding is that some females in one of three gastropod species contain male reproductive tissue in their gonads, providing a fascinating case of a mixed or transitory sexual system. Overall, the study by Castel et al (2023) offers the first insights into the reproduction and sex chromosome system of animals living in deep marine vents, which have remained poorly studied and open outstanding research perspectives on these creatures.
Bachtrog, D., J.E.Mank, C.L.Peichel, M.Kirkpatrick, S.P.Otto, T.L. Ashman, M.W.Hahn, J.Kitano, I.Mayrose, R.Ming, et al. 2014.Sex determination: why so many ways of doing it? PLoSBiol. 12:e1001899. https://doi.org/10.1371/journal.pbio.1001899
Charlesworth, D. Young sex chromosomes in plants and animals. 2019. New Phytologist 224: 1095–1107. https://doi.org/10.1111/nph.16002
Castel J, Pradillon F, Cueff V, Leger G, Daguin-Thiébaut C, Ruault S, Mary J, Hourdez S, Jollivet D, and Broquet T 2023. Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.04.11.536409
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
French Oceanographic Fleet program and the ANR CERBERUS (ANR-17-CE02-0003)
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2023.04.11.536409
Version of the preprint: 1
Author's Reply, 08 Nov 2023
Decision by Tanja Schwander, posted 27 May 2023, validated 30 May 2023
Thank you for submitting your preprint "Genetic sex determination in three closely related hydrothermal vent gastropods, one of which has intersex individuals" for evaluation by PCI Evol Biol.
Your manuscript has now been peer reviewed by three reviewers. As you will see, the reviewers all find your manuscript interesting, but make a number of constructive suggestions that will help you to improve and/or clarify the manuscript. I would particularly encourage you to focus the discussion more on the sexual and sex determination systems rather than the finding that sex linkage generates more structure in the dataset than geography. The current phrasing makes the bulk of the discussion rather taxon specific and largely a repetition of the results. Integrating the relevant discussion paragraphs directly into the results and mostly discussing the sexual systems and potential transition from gonochorism to hermaphroditism will make the discussion more appealing to a general audience.
Furthermore, I think that the analyses and discussion related to the sex-linked regions (and notably the size of the sex-linked regions) could be significantly improved by including an analysis of male-specific regions. Since your analyses are based on a de-novo assembly of RAD loci, the most strongly differentiated regions on the sex chromosomes will assemble as separate loci in males and females. All these loci are filtered out since only loci genotyped in at least 80% of inds are included (and sex-ratios are about 50:50). By adding another set of analyses with sex specific filtering (eg. retain loci genotyped in 80% of males, 80% of females, and looking for overlap vs sex-specific loci), one could assess variation in X-Y divergence across the three species as well as the size of the male-specific genome region.
Finally, for genetic variance and structure analyses, I recommend using a single SNP per RAD locus (as SNPs on the same locus are physically very close and thus in very strong LD, i.e., not independent estimates). This would also affect the simulations, which will consider too many independent SNPs.
I invite you to revise the manuscript by addressing the comments provided.