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Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod

Abstract

Sex chromosomes are highly variable in some taxonomic groups, but the evolutionary mechanisms underlying this diversity are not well understood. In terrestrial isopod crustaceans, evolutionary turnovers in sex chromosomes are frequent, possibly caused by Wolbachia, a vertically-transmitted endosymbiont causing male-to-female sex reversal. Here, we use surgical manipulations and genetic crosses, plus genome sequencing, to examine sex chromosomes in the terrestrial isopod Trachelipus rathkei. Although an earlier cytogenetics study suggested a ZZ/ZW sex chromosome system in this species, we surprisingly find multiple lines of evidence that in our study population, sex is determined by an XX/XY system. Consistent with a recent evolutionary origin for this XX/XY system, the putative male-specific region of the genome is small. The genome shows evidence of Y-linked duplications of the gene encoding the androgenic gland hormone, a major component of male sexual differentiation in isopods. Our analyses also uncover sequences horizontally acquired from past Wolbachia infections, consistent with the hypothesis that Wolbachia may have interfered with the evolution of sex determination in T. rathkei. Overall, these results provide evidence for the co-occurrence of multiple sex chromosome systems within T. rathkei, further highlighting the relevance of terrestrial isopods as models for the study of sex chromosome evolution.

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Fig. 1
Fig. 2: Phylogenetic tree showing the relationship of candidate horizontally transferred Wolbachia segments in the T. rathkei genome to other Wolbachia isolates.
Fig. 3: Distribution of sequencing depth for single-copy BUSCO genes in male and female Illumina sequencing datasets (M-pool and F-pool).
Fig. 4: Possible duplicates of the androgenic gland hormone gene in the T. rathkei genome, including male-specific duplicates (on the right).
Fig. 5: Phylogenetic tree showing relationships among AGH sequences from terrestrial isopods.

Data availability

Data can be accessed at NCBI under the following Accession ID: PRJNA633105.

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Acknowledgements

We thank the editor and three anonymous reviewers for constructive comments on earlier drafts of this manuscript. We also appreciate the computing time and assistance provided by the National Center for Genome Analysis Support at Indiana University, especially Tom Doak and Sheri Sanders. This research was funded by National Science Foundation grant NSF-DEB 1453298 to CHC. It was also supported in part by Lilly Endowment, Inc., through its support for the Indiana University Pervasive Technology Institute. This research is based upon work supported by the National Science Foundation under Grant Nos. DBI-1062432 2011, ABI-1458641 2015, and ABI-1759906 2018 to Indiana University. Any opinions, findings, and conclusions, or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation, the National Center for Genome Analysis Support, or Indiana University.

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Correspondence to Christopher H. Chandler.

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Russell, A., Borrelli, S., Fontana, R. et al. Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod. Heredity 127, 266–277 (2021). https://doi.org/10.1038/s41437-021-00457-2

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