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

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

doi:10.1038/s41467-022-28895-4

Cited by 8 publications

(5 citation statements)

References 139 publications

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“…Similarly, we do not find support for a large haplotype on LG1, which has been previously been indirectly implicated in guppy color variation in another population ( 50 ). Instead, our results suggest a far more complicated genetic architecture for color pattern.…”

Section: Discussioncontrasting

confidence: 99%

Deep learning reveals the role of copy number variation in the genetic architecture of a highly polymorphic sexual trait

van der Bijl,

Shu,

Goberdhan

et al. 2023

Preprint

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The extraordinary variation in male guppy coloration has been a powerful model for studying the interplay of natural and sexual selection. Many guppy populations exhibit substantial Y-linkage of color traits, and this has hampered the identification of the genetic architecture underlying male guppy color, as well as clouded our understanding of how this exceptional level of diversity is maintained. Here we used a population with low levels of Y-linkage for color variation to identify the heritability and genetic basis of male color variation using convolutional neural networks for high-resolution phenotyping coupled with selection experiments and controlled pedigrees and whole-genome resequencing for Genome Wide Association Study (GWAS) of colour. Our phenotypic and genomic results converge to show that color patterning in guppies is a combination of many heritable features, each with a partially overlapping genetic architecture. Unusually, our GWAS results suggest that copy number variation (CNV) is responsible for much of the variation in colour in guppies, providing a potential mechanism for the maintenance of variation of this classic model trait.

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Section: Discussioncontrasting

confidence: 99%

Deep learning reveals the role of copy number variation in the genetic architecture of a highly polymorphic sexual trait

van der Bijl,

Shu,

Goberdhan

et al. 2023

Preprint

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show abstract

“…An important avenue by which the Y chromosome can affect male phenotypes is by modulating gene expression throughout the genome, an effect described in D. melanogaster ( Lemos et al 2008 ) and for the SRY locus in mammals ( Berta et al 1990 ; Goodfellow and Lovell-Badge 1993 ). In line with such a mechanism, Y-autosome epistatic effects have also been associated with sexually antagonistic coloration in guppies ( Paris et al 2022 ). Callosobruchus maculatus Y shows significant enrichment for DNA binding molecular function, a category that SRY also falls into ( supplementary fig.…”

Section: Discussionmentioning

confidence: 93%

Y-Linked Copy Number Polymorphism of Target of Rapamycin Is Associated with Sexual Size Dimorphism in Seed Beetles

Kaufmann

Wiberg

Papachristos

et al. 2023

Molecular Biology and Evolution

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The Y chromosome is theorized to facilitate evolution of sexual dimorphism by accumulating sexually antagonistic loci, but empirical support is scarce. Due to the lack of recombination Y chromosomes are prone to degenerative processes, which poses a constraint on their adaptive potential. Yet, in the seed beetle Callosobruchus maculatus segregating Y linked variation affects male body size and thereby sexual size dimorphism (SSD). Here we assemble C. maculatus sex chromosome sequences and identify molecular differences associated with Y-linked SSD variation. The assembled Y chromosome is largely euchromatic and contains over 400 genes, many of which are ampliconic with a mixed autosomal and X chromosome ancestry. Functional annotation suggests that the Y chromosome plays important roles in males beyond primary reproductive functions. Crucially, we find that, besides an autosomal copy of the gene target of rapamycin (TOR), males carry an additional TOR copy on the Y chromosome. TOR is a conserved regulator of growth across taxa, and our results suggest that a Y-linked TOR provides a male specific opportunity to alter body size. A comparison of Y haplotypes associated with male size difference uncovers a copy number variation for TOR, where the haplotype associated with decreased male size, and thereby increased sexual dimorphism, has two additional TOR copies. This suggests that sexual conflict over growth has been mitigated by autosome to Y translocation of TOR followed by gene duplications. Our results reveal that despite of suppressed recombination, the Y chromosome can harbour adaptive potential as a male-limited supergene.

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“…An important avenue by which the Y chromosome can affect male phenotypes is by modulating gene expression throughout the genome, an effect described in D. melanogaster 58 and for the SRY locus in mammals 59,60 . In line with such a mechanism, Yautosome epistatic effects have also been associated with sexually antagonistic coloration in guppies 61 . C. maculatus Y shows significant enrichment for DNA binding molecular function, a category that SRY also falls into (Fig.…”

Section: Gene Content On the Ymentioning

confidence: 86%

Y-linked copy number polymorphism of target of rapamycin (TOR) is associated with sexual size dimorphism in seed beetles

Kaufmann

Wiberg

Papachristos

et al. 2023

Preprint

View full text Add to dashboard Cite

The Y chromosome is theorized to facilitate evolution of sexual dimorphism by accumulating sexually antagonistic loci, but empirical support is scarce. Due to the lack of recombination Y chromosomes are prone to degenerative processes, which poses a constraint on their adaptive potential. Yet, in the seed beetleCallosobruchus maculatussegregating Y linked variation affects male body size and thereby sexual size dimorphism (SSD). Here we assembleC. maculatussex chromosome sequences and identify molecular differences associated with Y-linked SSD variation. The assembled Y chromosome is largely euchromatic and contains over 400 genes, many of which are ampliconic with a mixed autosomal and X chromosome ancestry. Functional annotation suggests that the Y chromosome plays important roles in males beyond primary reproductive functions. Crucially, we find that, besides an autosomal copy of the genetarget of rapamycin(TOR), males carry an additionalTORcopy on the Y chromosome.TORis a conserved regulator of growth across taxa, and our results suggest that a Y-linkedTORprovides a male specific opportunity to alter body size. A comparison of Y haplotypes associated with male size difference uncovers a copy number variation forTOR, where the haplotype associated with decreased male size, and thereby increased sexual dimorphism, has two additionalTORcopies. This suggests that sexual conflict over growth has been mitigated by autosome to Y translocation ofTORfollowed by gene duplications. Our results reveal that despite of suppressed recombination, the Y chromosome can harbour adaptive potential as a male-limited supergene.

show abstract

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

Cited by 8 publications

References 139 publications

Deep learning reveals the role of copy number variation in the genetic architecture of a highly polymorphic sexual trait

Deep learning reveals the role of copy number variation in the genetic architecture of a highly polymorphic sexual trait

Y-Linked Copy Number Polymorphism of Target of Rapamycin Is Associated with Sexual Size Dimorphism in Seed Beetles

Y-linked copy number polymorphism of target of rapamycin (TOR) is associated with sexual size dimorphism in seed beetles

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