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Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida

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Abstract

The sex chromosomes in Sauropsida (reptiles and birds) have evolved independently many times. They show astonishing diversity in morphology ranging from cryptic to highly differentiated sex chromosomes with male (XX/XY) and female heterogamety (ZZ/ZW). Comparing such diverse sex chromosome systems thus provides unparalleled opportunities to capture evolution of morphologically differentiated sex chromosomes in action. Here, we describe chromosomal mapping of 18 microsatellite repeat motifs in eight species of Sauropsida. More than two microsatellite repeat motifs were amplified on the sex-specific chromosome, W or Y, in five species (Bassiana duperreyi, Aprasia parapulchella, Notechis scutatus, Chelodina longicollis, and Gallus gallus) of which the sex-specific chromosomes were heteromorphic and heterochromatic. Motifs (AAGG)n and (ATCC)n were amplified on the W chromosome of Pogona vitticeps and the Y chromosome of Emydura macquarii, respectively. By contrast, no motifs were amplified on the W chromosome of Christinus marmoratus, which is not much differentiated from the Z chromosome. Taken together with previously published studies, our results suggest that the amplification of microsatellite repeats is tightly associated with the differentiation and heterochromatinization of sex-specific chromosomes in sauropsids as well as in other taxa. Although some motifs were common between the sex-specific chromosomes of multiple species, no correlation was observed between this commonality and the species phylogeny. Furthermore, comparative analysis of sex chromosome homology and chromosomal distribution of microsatellite repeats between two closely related chelid turtles, C. longicollis and E. macquarii, identified different ancestry and differentiation history. These suggest multiple evolutions of sex chromosomes in the Sauropsida.

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Acknowledgments

We thank David Wong and Theresa Knopp for providing tissues of pink-tailed worm-lizards, Bruno Ferronato for providing tissues of eastern long-necked turtle, and Tony Gamble for collecting marbled geckos. We are grateful to Alistair Zealey, Jacqui Richardson, and Wendy Ruscoe for caring for the animals, and Clare Holleley for valuable discussions.

Funding

This work was supported by an Australian Research Council Discovery Grant (ARC DP110102262) awarded to TE, SS, AG, JG, and YM. TE was supported by an ARC Future Fellowship (FT110100733).

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

Animal collection, handling, sampling, and all other relevant procedures were performed following the guidelines of the Australian Capital Territory Animal Welfare Act 1992 (Section 40) under permits and licenses issued by Environment ACT, the New South Wales State, and Northern Territory governments (LT2012587, LI2008321, S12364, and 26791, respectively), and with the approval of the Australian National University Animal Experimentation Ethics Committee (Proposal R.CG.07.3b/04/07) and CEAE 11/07 and 11/12 (the Committee for Ethics in Animal Experimentation at the University of Canberra).

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Author notes

  1. Kazumi Matsubara

    Present address: Laboratory of Animal Genetics, Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

Authors and Affiliations

  1. Institute for Applied Ecology, University of Canberra, Bruce, Australian Capital Territory, 2601, Australia

    Kazumi Matsubara, Denis O’Meally, Bhumika Azad, Arthur Georges, Stephen D. Sarre, Jennifer A. Marshall Graves & Tariq Ezaz

  2. The John Curtin School of Medical Research, The Australian National University, Garran Road, Acton, Australian Capital Territory, 2601, Australia

    Bhumika Azad

  3. School of Life Sciences, La Trobe University, Melbourne, 3086, Victoria, Australia

    Jennifer A. Marshall Graves

  4. Laboratory of Animal Genetics, Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Yoichi Matsuda

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  1. Kazumi Matsubara
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Correspondence to Kazumi Matsubara or Tariq Ezaz.

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ESM 1

Figure S1 Examples of dot plot analyses with chicken repetitive sequences. Dot plot showed presence of copies of EcoRI- (Accession no. X57344), XhoI- (X06548) and SspI-family (AB074190) repetitive sequences on chicken unlocalized scaffolds, AADN03017196, AADN03022444, and AADN03019847, respectively (a–c). Two complete copies of SspI-family repetitive sequences were clearly identified on single scaffolds, AADN03019847 (c). (PDF 4069 kb)

ESM 2

Table S1. Frequencies of (AG)n and (AGG)n microsatellite loci on released genome sequences of chicken chromosomes. (XLSX 48 kb)

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Matsubara, K., O’Meally, D., Azad, B. et al. Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida. Chromosoma 125, 111–123 (2016). https://doi.org/10.1007/s00412-015-0531-z

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