Guppy Colour Genetics: Basics for Breeders

How guppy colour is inherited: Y- and X-linked male ornaments, autosomal recessives such as golden, blue and blond, why females carry hidden traits, and line versus outcross.

Overview

The guppy (Poecilia reticulata) has been a model for colour genetics since the 1920s, when Winge first analysed its male ornaments. Guppies have 23 pairs of chromosomes, one pair of which are sex chromosomes, and use an XY system in which males are XY and females XX. Wild-type females are grey, while males carry spots, splashes and stripes in many colours. These patterns are built from three to four pigment cell types: black melanophores, yellow-orange to reddish xanthophores, blue iridescent iridophores and possibly white leukophores.

Sex-linked colour: the Y and the X

In 1922 and 1927 Winge described 18 putative colour loci. Seventeen of them showed sex-linked inheritance and nine were strictly Y-linked. Later classical studies recorded at least 20 colour pattern alleles found only on the Y and at least 28 that recombine between X and Y. Pigment pattern loci can therefore be Y-linked, X-linked, XY-linked or autosomal. Because so much of the male pattern sits on the Y, early studies found a strong inheritance of male colour pattern down the father's line.

The sex-determining locus lies in a male-specific, non-recombining region at the end of the Y chromosome. Crossing over between X and Y is low but not zero: Winge and colleagues found up to 10% recombination between a sex-chromosome marker and the sex locus, and a later quantitative trait locus (QTL) study found 2.3%. Y chromosomes also differ between strains in heterochromatin content and even visible length. YY males are viable as long as the two Y chromosomes come from different strains, and no Y marker shared by all strains has been found.

Worked example: the variegated tail pattern

Khoo and colleagues (1999, Zoological Science) studied a variegated mosaic of black spots and patches on the tail. They concluded that a single gene, Var, sits on both the X and the Y, and that the dominant Var allele produces variegation while the recessive allele gives the plain wild type. Crossing variegated males with wild-type females gave an all-variegated F1. The F2 came out at roughly 2 variegated males : 1 variegated female : 1 wild-type female. In the reciprocal cross (wild-type males × variegated females) the F1 was again all variegated, but the F2 came out at roughly 1 variegated male : 1 wild-type male : 2 variegated females. Crossing over between Var and the sex-determining region was about 1.9 map units. The example shows how, for a gene on the sex chromosomes, the expected ratios change with the direction of the cross.

Autosomal recessive colours

Unlike the sex-specific ornaments, several autosomal colour factors behave as ordinary Mendelian recessives and show in both sexes. Two classic examples arose spontaneously. In golden guppies a mutation in kita on autosomal linkage group 4 cuts melanophore numbers: golden females have about half the normal number, and the fish look coarsely mottled. Blue guppies carry a mutation in csf1ra on linkage group 10 and lack nearly all orange xanthophores in the skin. Because the two genes lie on different autosomes, they recombine freely. The same golden mutation was found in several laboratory strains, which suggests breeders introduced it on purpose for its colour (Kottler et al. 2013, Genetics).

The blond phenotype comes from a spontaneous 2-base-pair deletion in adcy5, which is needed for melanophore development and for male orange markings (Kottler et al. 2015, Pigment Cell & Melanoma Research). Some domestic strains have red eyes, a sign of albinism. Early reports pointed to autosomal Mendelian inheritance for it, but the gene was not known. A 2024 genomic and transcriptomic study proposed OCA2 as the main candidate gene, which is not the same as a confirmed cause (Chang et al. 2024, International Journal of Molecular Sciences).

Autosomal genes also change how the Y-linked ornaments look. In backcrosses, blue males lacked every orange trait no matter which strain their Y came from, and golden males had their black ornaments reduced or shifted. The black dorsal-fin spot of the Maculatus strain is considered strictly Y-linked, yet it was reduced in golden males. Even a strictly Y-linked trait therefore depends on autosomal cofactors to show.

Tail shape and pattern

Fancy guppy strains differ in colour, pattern, and the shape and size of their fins; snakeskin and grass varieties are among the named types. Tail colour patterns such as variegation can be sex-linked, as described above. QTL analysis has confirmed that most male colour traits are controlled by several genes, including genes on the autosomes, each with a minor effect. The sources consulted for this guide give no inheritance mode for specific tail-shape types, so no ratios are given for them here.

Why females carry hidden traits

• Females carry X-linked and pseudoautosomal colour genes that they normally do not express. In some populations, females treated with testosterone develop spots and stripes.
• XY females of the Maculatus strain show the black dorsal-fin spot of Maculatus males, only fainter, but none of the other male pattern elements.
• Autosomal recessive alleles stay hidden in heterozygous carriers of either sex. One laboratory stock, for example, was made up of fish heterozygous for both golden and blue.
• Because a female's appearance reveals little of her colour genotype, the same female can produce very different sons depending on the male she is paired with.

Line breeding versus outcrossing

Selection changes guppy colour quickly. In feral guppies from Okinawa, Sato and Kawata (2020, BMC Research Notes) needed only three generations of artificial selection to make high and low lines differ significantly in male orange area. Realised heritability was 1.47 in the high line and 0.32 in the low line, and the low-line value was not significantly above zero. Closing a line in this way concentrates the wanted alleles. It also raises inbreeding: in guppies, full-sib matings significantly reduced survival to day 120 and salinity tolerance, while crosses between genetically different strains raised them (Nakadate et al. 2003, Aquaculture). The guide on line breeding and inbreeding depression covers these effects; the reproductive biology of livebearers is covered in the fish reproductive strategies guide.

An outcross to another strain brings in new X chromosomes and autosomes, and these can change a familiar Y-linked pattern. In one set of crosses, F1 and wild-type grandsons showed more complex black labyrinthine ornaments than their wild-derived grandfather. The researchers took this as a sign that cofactors from the other strain's autosomes or X chromosome modulate the trait.