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A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy

Author

Listed:
  • Josephine R. Paris

    (University of Exeter)

  • James R. Whiting

    (University of Exeter)

  • Mitchel J. Daniel

    (Florida State University)

  • Joan Ferrer Obiol

    (Genètica i Estadística and Institut de Recerca de la Biodiversitat, Universitat de Barcelona)

  • Paul J. Parsons

    (University of Exeter
    NERC Environmental Omics Facility, School of Biosciences, University of Sheffield)

  • Mijke J. Zee

    (University of Exeter)

  • Christopher W. Wheat

    (Stockholm University)

  • Kimberly A. Hughes

    (Florida State University)

  • Bonnie A. Fraser

    (University of Exeter)

Abstract

Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are typified by extreme variation governed by both natural and sexual selection. Since guppy colour patterns are often inherited faithfully from fathers to sons, it has been hypothesised that many of the colour trait genes must be physically linked to sex determining loci as a ‘supergene’ on the sex chromosome. Here, we phenotype and genotype four guppy ‘Iso-Y lines’, where colour was inherited along the patriline for 40 generations. Using an unbiased phenotyping method, we confirm the breeding design was successful in creating four distinct colour patterns. We find that genetic differentiation among the Iso-Y lines is repeatedly associated with a diverse haplotype on an autosome (LG1), not the sex chromosome (LG12). Moreover, the LG1 haplotype exhibits elevated linkage disequilibrium and evidence of sex-specific diversity in the natural source population. We hypothesise that colour pattern polymorphism is driven by Y-autosome epistasis.

Suggested Citation

  • Josephine R. Paris & James R. Whiting & Mitchel J. Daniel & Joan Ferrer Obiol & Paul J. Parsons & Mijke J. Zee & Christopher W. Wheat & Kimberly A. Hughes & Bonnie A. Fraser, 2022. "A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28895-4
    DOI: 10.1038/s41467-022-28895-4
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    1. Alison E. Wright & Iulia Darolti & Natasha I. Bloch & Vicencio Oostra & Ben Sandkam & Severine D. Buechel & Niclas Kolm & Felix Breden & Beatriz Vicoso & Judith E. Mank, 2017. "Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    2. Killick, Rebecca & Eckley, Idris A., 2014. "changepoint: An R Package for Changepoint Analysis," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 58(i03).
    3. Kimberly A. Hughes & Anne E. Houde & Anna C. Price & F. Helen Rodd, 2013. "Mating advantage for rare males in wild guppy populations," Nature, Nature, vol. 503(7474), pages 108-110, November.
    4. S. Kmoch & J. Majewski & V. Ramamurthy & S. Cao & S. Fahiminiya & H. Ren & I. M. MacDonald & I. Lopez & V. Sun & V. Keser & A. Khan & V. Stránecký & H. Hartmannová & A. Přistoupilová & K. Hodaňová & L, 2015. "Mutations in PNPLA6 are linked to photoreceptor degeneration and various forms of childhood blindness," Nature Communications, Nature, vol. 6(1), pages 1-10, May.
    5. Robert Olendorf & F. Helen Rodd & David Punzalan & Anne E. Houde & Carla Hurt & David N. Reznick & Kimberly A. Hughes, 2006. "Frequency-dependent survival in natural guppy populations," Nature, Nature, vol. 441(7093), pages 633-636, June.
    6. Shin, Ji-Hyung & Blay, Sigal & McNeney, Brad & Graham, Jinko, 2006. "LDheatmap: An R Function for Graphical Display of Pairwise Linkage Disequilibria Between Single Nucleotide Polymorphisms," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 16(c03).
    7. Kang-Wook Kim & Benjamin C. Jackson & Hanyuan Zhang & David P. L. Toews & Scott A. Taylor & Emma I. Greig & Irby J. Lovette & Mengning M. Liu & Angus Davison & Simon C. Griffith & Kai Zeng & Terry Bur, 2019. "Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    8. Jean-Guy J. Godin & Heather E. McDonough, 2003. "Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait," Behavioral Ecology, International Society for Behavioral Ecology, vol. 14(2), pages 194-200, March.
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