Genomic data reveal conserved female heterogamety in giant salamanders with gigantic nuclear genomes

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16 Scopus citations

Abstract

Systems of genetic sex determination and the homology of sex chromosomes in different taxa vary greatly across vertebrates. Much progress remains to be made in understanding systems of genetic sex determination in non-model organisms, especially those with homomorphic sex chromosomes and/or large genomes. We used reduced representation genome sequencing to investigate genetic sex determination systems in the salamander family Cryptobranchidae (genera Cryptobranchus and Andrias), which typifies both of these inherent difficulties. We tested hypotheses of male- or female-heterogamety by sequencing hundreds of thousands of anonymous genomic regions in a panel of known-sex cryptobranchids and characterized patterns of presence/absence, inferred zygosity, and depth of coverage to identify sex-linked regions of these 56 gigabase genomes. Our results strongly support the hypothesis that all cryptobranchid species possess homologous systems of female heterogamety, despite maintenance of homomorphic sex chromosomes over nearly 60 million years. Additionally, we report a robust, non-invasive genetic assay for sex diagnosis in Cryptobranchus and Andrias which may have great utility for conservation efforts with these endangered salamanders. Co-amplification of these W-linked markers in both cryptobranchid genera provides evidence for long-term sex chromosome stasis in one of the most divergent salamander lineages. These findings inform hypotheses about the ancestral mode of sex determination in salamanders, but suggest that comparative data from other salamander families are needed. Our results further demonstrate that massive genomes are not necessarily a barrier to effective genome-wide sequencing and that the resulting data can be highly informative about sex determination systems in taxa with homomorphic sex chromosomes.

Original languageEnglish
Pages (from-to)3467-3476
Number of pages10
JournalG3: Genes, Genomes, Genetics
Volume9
Issue number10
DOIs
StatePublished - Oct 1 2019

Bibliographical note

Publisher Copyright:
Copyright © 2019 Hime et al.

Funding

We thank the Saint Louis Zoo (M. Duncan, J. Ettling, R. Junge, J. Merkle, S. O'Brien, A. Salb, C. Schuette, M. Wanner, and M. Weber), R. Williams at Purdue University, F. Dunker at the California Academy of Sciences, K. Hope at the National Zoo, the late M. Sieggreen at the Detroit Zoo, D. Barber at the Fort Worth Zoo, and K. Irwin at the Arkansas Game and Fish Commission for invaluable access to tissue samples and/or necropsy reports. We also thank the Missouri Department of Conservation and the Indiana Department of Natural Resources for permission to utilize samples. We are grateful to S. Nunziata for assistance with ddRAD library preparation. We thank the University of Kentucky Department of Information Technology and Center for Computational Sciences for processor time on the Lipscomb High Performance Computing Cluster. We also thank R. Glor and three anonymous reviewers for constructive comments on this manuscript. This work was supported by funding from the Cryptobranchid Interest Group, Fresno Chaffee Zoo, the Saint Louis Zoo WildCare Institute, the University of Kentucky G.F. Ribble Fund, and by the National Science Foundation (DEB-0949532 to D.W.W. and DGE-3048109801 to P.M.H.). Any opinion, 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 authors declare no competing financial interests. We thank the Saint Louis Zoo (M. Duncan, J. Ettling, R. Junge, J. Merkle, S. O’Brien, A. Salb, C. Schuette, M. Wanner, and M. Weber), R. Williams at Purdue University, F. Dunker at the California Academy of Sciences, K. Hope at the National Zoo, the late M. Sieggreen at the Detroit Zoo, D. Barber at the Fort Worth Zoo, and K. Irwin at the Arkansas Game and Fish Commission for invaluable access to tissue samples and/or necropsy reports. We also thank the Missouri Department of Conservation and the Indiana Department of Natural Resources for permission to utilize samples. We are grateful to S. Nunziata for assistance with ddRAD library preparation. We thank the University of Kentucky Department of Information Technology and Center for Computational Sciences for processor time on the Lipscomb High Performance Computing Cluster. We also thank R. Glor and three anonymous reviewers for constructive comments on this manuscript. This work was supported by funding from the Cryptobranchid Interest Group, Fresno Chaffee Zoo, the Saint Louis Zoo WildCare Institute, the University of Kentucky G.F. Ribble Fund, and by the National Science Foundation (DEB-0949532 to D.W.W. and DGE-3048109801 to P.M.H.). Any opinion, 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 authors declare no competing financial interests.

FundersFunder number
Purdue Climate Change Research Center, Purdue University
University of Kentucky Information Technology Department and Center for Computational Sciences
California Academy of Sciences
Saint Louis Zoo WildCare Institute
Cryptobranchid Interest Group
University of Kentucky G.F. Ribble Fund
Indiana Department of Natural Resources
Saint Louis Zoo
Arkansas Game and Fish Commission
Missouri Department of Conservation
National Science Foundation Arctic Social Science Program0949532, DEB-0949532, DGE-3048109801

    Keywords

    • Amphibian
    • Andrias
    • Cryptobranchus
    • DdRADseq
    • Genetics of Sex
    • W chromosome

    ASJC Scopus subject areas

    • Molecular Biology
    • Genetics
    • Genetics(clinical)

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