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

Josephine R. Paris (), James R. Whiting, Mitchel J. Daniel, Joan Ferrer Obiol, Paul J. Parsons, Mijke J. Zee, Christopher W. Wheat, Kimberly A. Hughes and Bonnie A. Fraser
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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
Mijke J. Zee: University of Exeter
Christopher W. Wheat: Stockholm University
Kimberly A. Hughes: Florida State University
Bonnie A. Fraser: University of Exeter

Nature Communications, 2022, vol. 13, issue 1, 1-15

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-28895-4

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