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

Joan Ferrer Obiol,Josephine R Paris,Paul J Parsons,Bonnie A Fraser,James R Whiting,Mijke J Van Der Zee,Kimberly A Hughes,Mitchel J Daniel,Christopher W Wheat

doi:10.1038/s41467-022-28895-4

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.

Highlights

Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are typified by extreme variation governed by both natural and sexual selection
We used geometric morphometrics to correct for individual differences in body size and shape among fish so that colour patterns could be measured as though they existed on identical male bodies
Using extensive whole-genome sequencing (WGS) from the source population, we further highlight just one of these regions (Region 2-NP: 11.1–15.9 Mb), as having strong linkage and significant local ancestry, finding that a large and variable haplotype is maintained in nature

Summary

Introduction

Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are typified by extreme variation governed by both natural and sexual selection. Despite this great diversity in colour patterns, and our understanding of the evolutionary processes maintaining it, the underlying genetic architecture remains largely unknown It has long-been hypothesised that colour patterning genes and the sex determining locus (SDL) form a Y-linked ‘supergene’ in the guppy[23,24]. A QTL mapping study found that only 13% of colour trait loci mapped to the sex chromosome (LG12)[28] and a pedigree analysis of colour pattern inheritance showed that ornaments are not completely Y-linked, hypothesising a potential role for Y-autosome epistasis[29]. The distal end of LG12 has been found to be highly diverse among males with many segregating male-specific variants, indicative of multiple Y haplotypes, as would be predicted under NFDS for Y-linked colour traits[31,35] Within this candidate region, no gene associated with colour or sex has been found. This genetic architecture could help to explain how high levels of Y-linked diversity is maintained in guppy colour patterns

Methods

Results

Conclusion