Scientific Report
The overall aim was to test the sexually antagonistic polymorphism hypothesis, that male coloration polymorphisms that are beneficial only in males of the guppy, Poecilia reticulata, may have selected against recombination between the X and Y chromosomes of this species, especially in populations subject to high predation, where the survival of females expressing male coloration traits would be strongly reduced. The proposal was to use genetic mapping of molecular markers to test whether recombination differs between different wild populations of guppies in Trinidad. The results from the different goals, in combination, suggest that such polymorphisms are indeed likely to be present in the region most closely linked to the male-determining locus on the Y chromosome, but that recombination has not evolved in response to this, but instead that an ancestral low recombination rate allowed these polymorphisms to be established.
For goals 1 and 2, we mapped microsatellite markers and single nucleotide polymorphisms (SNPs), which revealed that, in males, genetic recombination occurs only in a small terminal “pseudo-autosomal region” (or PAR), but across the entire chromosome in females [1, 2]. Other guppy chromosomes (probably all 23 of them) show similar sex differences in recombination patterns. The lack of recombination in male meiosis did not evolve specifically on the XY chromosome pair, which was confirmed using analyses of GC content patterns across guppy chromosomes and those of related fish [3]. Our genetic maps confirm that the guppy recombination pattern did not evolve recently, as the PAR boundary is the same in families from different populations [2].
Goals 3, 4 and 6. The goal of estimating the age of the guppy sex chromosome system was not possible, because our population genomic analysis showed that, although most genes on this chromosome are closely linked to the fully sex-linked region, DNA sequence variants are incompletely associated with the male-determining factor. Due to occasional recombination, the Y is only slightly diverged from the X and has not lost genes that are carried on the X [1, 4]. Other results from close outgroup species that do have highly degenerated Y chromosomes [5] suggest that the guppy Y evolved in a recent sex chromosome turnover event in which a male-determining factor appeared on the ancestral X [6].
Goals 5 and 6: The comparison of the population genetic structure of male coloration phenotypes versus weakly selected molecular variants in natural populations rejected a model of neutral phenotypic divergence between populations, but did not support a simple picture of parallel evolution in relation to high versus low predation [7]. The rarity of recombination between the Y and X chromosomes precluded mapping the factors controlling male coloration phenotypes, which proved not to be located in the recombining PAR; thus we could not obtain the planned estimates of allele frequencies in natural populations with low and high predation rates.
However, detailed analysis of molecular variants indirectly suggested the presence of polymorphism(s) in a small region that is particularly closely linked to the male-determining factor. Specifically, although the region is limited to just a physically small part of the XY pair (within the rarely recombining region, but near the PAR boundary), association with the male-determining factor are observed across a much larger physical distance in the sex chromosome assembly than predicted; although the estimated recombination rate is low, it is probably not low enough to account for the results without the presence of a gene or genes under balancing selection [8]. The (indirectly inferred) polymorphism(s) might be factors controlling sexually dimorphic traits other than male coloration.
References
1. Bergero, R., et al., Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms. Proceedings of the National Academy of Sciences of the United States of America, 2019. 116(14): p. 6924-6931.
2. Charlesworth, D., et al., Locating the sex determining region of linkage group 12 of guppy (Poecilia reticulata). G3 (Bethesda), 2020. 10(10): p. 3639-3649.
3. Charlesworth, D., et al., Using GC content to compare recombination patterns on the sex chromosomes and autosomes of the guppy, Poecilia reticulata, and its close outgroup species. Molecular Biology and Evolution, 2020. 37(12): p. 3550–3562.
4. Fraser, B.A. et al., Improved reference genome uncovers novel sex-linked regions in the guppy (Poecilia reticulata). Genome Biology and Evolution, 2020. 12(10): p. 1789–1805.
5. Charlesworth, D., et al., PromethION sequencing and assembly of the genome of Micropoecilia picta, a fish with a highly degenerated Y chromosome. Genome Biology and Evolution, 2021: p. evab171.
6. Charlesworth, D., et al., How did the guppy Y chromosome evolve? PLoS Genetics, 2021.
7. Yong, L., et al., Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space. Molecular Ecology, 2021.
8. Qiu, S., et al., Partial sex linkage and linkage disequilibrium on the guppy sex chromosome. Molecular Ecology, 2022.
