Tissue Specificity and Dynamics of Sex-Biased Gene Expression in a Common Frog Population with Differentiated, Yet Homomorphic, Sex Chromosomes

Ma, Wen‐Juan; Veltsos, Paris; Toups, Melissa A.; Rodrigues, Nicolas; Sermier, Roberto; Jeffries, Daniel L.; Perrin, Nicolas

doi:10.3390/genes9060294

Cited by 25 publications

(23 citation statements)

References 94 publications

(193 reference statements)

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“…Thus, we find no support for the canonical model of sex-chromosome evolution, which assigns a key role to sex-linked SA genes (Ma, Veltsos, Sermier, Parker, & Perrin, 2018a;Ma, Veltsos, Toups, et al, 2018b). These convergent results seem to suggest that sexual dimorphism in Rana temporaria essentially stems from the differential expression of genes regardless of their sex-linkage and not from the differential fixation of alleles at sexually antagonistic loci on X and Y chromosomes.…”

Section: Discussioncontrasting

confidence: 83%

No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

Veltsos

Rodrigues

Studer

et al. 2019

J of Evolutionary Biology

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The canonical model of sex‐chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (nonrecombinant Y haplotypes) coexist with both XY° males with proto‐Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex‐determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study finds no effect of sex‐chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs might result more from the differential expression of autosomal genes than from sex‐linked SA genes. Among‐male variance in sex‐chromosome differentiation seems better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X‐Y recombination in XY females), independent of sex‐linked SA genes.

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Section: Discussioncontrasting

confidence: 83%

No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

Veltsos

Rodrigues

Studer

et al. 2019

J of Evolutionary Biology

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“…It is also important to note that previous studies on genomic clusters of sex-biased genes were primarily conducted on primary sexual organs, such as ovaries and testes 35–40 . These tissues are highly complex, often express more sex-biased genes than secondary sexual traits and their evolution is considered to be under natural selection 1,45,52–54 . Moreover, analyzing gene expression in these adult tissues does not capture the sex differences that are established during development.…”

Section: Discussionmentioning

confidence: 99%

Impact of trait exaggeration on sex-biased gene expression and genome architecture in a water strider

Toubiana¹,

Armisén²,

Dechaud³

et al. 2020

Preprint

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Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of sex-specific phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the lack of a representative genome and transcriptomes to study the development of secondary sexual traits. Here we present the genome and developmental transcriptomes, focused on the legs of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs used as weapons. The quality of the genome assembly is such that over 90% of the sequence is captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in sex-biased genes, indicating a specific signature of gene expression in association with sex-specific trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. Interestingly, we found that female-biased genes that are expressed in the third legs only, but not male-biased genes, were over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed that they can arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Our findings shed light on how directional sexual selection drives sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

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“…) and a Y C population with differentiated sex chromosomes (Ammarnäs, northern Sweden; Ma et al. ), so that the SA model does not seem to apply either. No Y A population, however, has yet been investigated in this respect.…”

Section: Discussionmentioning

confidence: 99%

“…). In the case of R. temporaria, genomic studies of sex-biased gene expression have failed to identify signatures of SA genes on sex chromosomes both in a Y B population with proto-sex chromosomes (Tvedöra, southern Sweden;Ma et al 2018a) and a Y C population with differentiated sex chromosomes (Ammarnäs, northern Sweden;Ma et al 2018b), so that the SA model does not seem to apply either. No Y A population, however, has yet been investigated in this respect.…”

mentioning

confidence: 99%

Phylogeography, more than elevation, accounts for sex chromosome differentiation in Swiss populations of the common frog ( Rana temporaria )*

et al. 2019

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Sex chromosomes in vertebrates range from highly heteromorphic (as in most birds and mammals) to strictly homomorphic (as in many fishes, amphibians, and nonavian reptiles). Reasons for these contrasted evolutionary trajectories remain unclear, but species such as common frogs with polymorphism in the extent of sex chromosome differentiation may potentially deliver important clues. By investigating 92 common frog populations from a wide range of elevations throughout Switzerland, we show that sex chromosome differentiation strongly correlates with alleles at the candidate sex‐determining gene Dmrt1. Y‐specific Dmrt1 haplotypes cluster into two main haplogroups, YA and YB, with a phylogeographic signal that parallels mtDNA haplotypes: YA populations, with mostly well‐differentiated sex chromosomes, occur primarily south of the main alpine ridge that bisects Switzerland, whereas YB populations, with mostly undifferentiated (proto‐)sex chromosomes, occur north of this ridge. Elevation has only a marginal effect, opposing previous suggestions of a major role for climate on sex chromosome differentiation. The Y‐haplotype effect might result from differences in the penetrance of alleles at the sex‐determining locus (such that sex reversal and ensuing X‐Y recombination are more frequent in YB populations), and/or fixation of an inversion on YA (as supported by the empirical observation that YA haplotypes might not recombine in XYA females).

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Tissue Specificity and Dynamics of Sex-Biased Gene Expression in a Common Frog Population with Differentiated, Yet Homomorphic, Sex Chromosomes

Cited by 25 publications

References 94 publications

No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

Impact of trait exaggeration on sex-biased gene expression and genome architecture in a water strider

Phylogeography, more than elevation, accounts for sex chromosome differentiation in Swiss populations of the common frog ( Rana temporaria )*

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