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

Extreme colour pattern variation in male Trinidadian guppies are influenced by natural selection and sexual selection. Here, the authors phenotype and genotype four guppy lineages finding that colour pattern is associated with a diverse haplotype on an autosome. 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.

Automated summary

Extreme colour pattern variation in male Trinidadian guppies is influenced by both natural selection and sexual selection. This study found that colour pattern is associated with genetic diversity on an autosome, rather than a 'supergene' on the sex chromosome.