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Sex chromosome polymorphism in guppies

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Abstract

Sex chromosomes differ from autosomes by dissimilar gene content and, at a more advanced stage of their evolution, also in structure and size. This is driven by the divergence of the Y or W from their counterparts, X and Z, due to reduced recombination and the resulting degeneration as well as the accumulation of sex-specific and sexually antagonistic genes. A paradigmatic example for Y-chromosome evolution is found in guppies. In these fishes, conflicting data exist for a morphological and molecular differentiation of sex chromosomes. Using molecular probes and the previously established linkage map, we performed a cytogenetic analysis of sex chromosomes. We show that the Y chromosome has a very large pseudoautosomal region, which is followed by a heterochromatin block (HCY) separating the subtelomeric male-specific region from the rest of the chromosome. Interestingly, the size of the HCY is highly variable between individuals from different population. The largest HCY was found in one population of Poecilia wingei, making the Y almost double the size of the X and the largest chromosome of the complement. Comparative analysis revealed that the Y chromosomes of different guppy species are homologous and share the same structure and organization. The observed size differences are explained by an expansion of the HCY, which is due to increased amounts of repetitive DNA. In one population, we observed also a polymorphism of the X chromosome. We suggest that sex chromosome-linked color patterns and other sexually selected genes are important for maintaining the observed structural polymorphism of sex chromosomes.

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Acknowledgments

We thank Georg Schneider, Hugo Schwind, and Petra Weber for expert fish keeping, Monika Niklaus-Ruiz for the support in the preparation of this manuscript, and Dr. Indar Ramnarine (St. Augustine, Trinidad) for the help in obtaining a research and collection permit (AMJ/pj 18/02/2008). We are grateful to Prof. Dr. Johannes-Horst Schröder (Mariastein), Fred N Poeser (Amsterdam), and Felix Breden for the founder fish and Emil Linke (Euerbach) for the XX males from the Ca population of P. wingei. This work was supported by Deutsche Forschungsgemeinschaft.

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Authors and Affiliations

  1. Biocenter, Institute for Human Genetics, Am Hubland, 97074, Würzburg, Germany

    Indrajit Nanda, Thomas Haaf & Michael Schmid

  2. Biocenter, Physiological Chemistry, Am Hubland, 97074, Würzburg, Germany

    Susanne Schories & Manfred Schartl

  3. Max Planck Institute for Developmental Biology, Spemannstraße 37-39, 72076, Tübingen, Germany

    Namita Tripathi & Christine Dreyer

  4. Comprehensive Cancer Center, University Clinic Würzburg, Josef Schneider Straße 6, 97080, Würzburg, Germany

    Manfred Schartl

Authors
  1. Indrajit Nanda
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  2. Susanne Schories
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  3. Namita Tripathi
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  4. Christine Dreyer
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  5. Thomas Haaf
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  6. Michael Schmid
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  7. Manfred Schartl
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Corresponding author

Correspondence to Manfred Schartl.

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Supplementary Figure 1

Comparison of the length of sex chromosomes and the largest autosome in different guppies. Measurements of X, Y, and the largest autosome were made from the same metaphases. Note that the Y chromosome is the largest chromosome in the karyotype of the EnCCFR and LP strains of P. wingei. FISH Probes; EnCCFR, LP, RS: BAC 36H23(green)-BAC 05C08 (red); Gr: BAC 34K02(green)-BAC 04G05(red) (JPEG 39.2 kb)

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Suppl. Table 1

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Nanda, I., Schories, S., Tripathi, N. et al. Sex chromosome polymorphism in guppies. Chromosoma 123, 373–383 (2014). https://doi.org/10.1007/s00412-014-0455-z

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  • DOI: https://doi.org/10.1007/s00412-014-0455-z

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