Sex chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog

Ogata, Mitsuaki; Suzuki, Kazuo; Yuasa, Yoshiaki; Miura, Ikuo

doi:10.1098/rstb.2020.0105

Cited by 19 publications

(14 citation statements)

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“…And vice versa, that two taxa exhibit the same chromosome pair as sex chromosomes does not necessarily mean their sex determination systems are homologous: the same pair of autosomes can be independently co-opted for the function of sex chromosomes (e.g. [71,75,128]; for overview in amniotes see [34]), or there might be turnovers of sex determination systems by the emergence of a new sex-determining locus within the same sex chromosome pair [66,129] (cases 15, 18 and 20 in figure 2).…”

Section: Is the Sex Chromosome Differentiationmentioning

confidence: 99%

“…Even highly differentiated, cytogenetically detectable sex chromosomes can be replaced by poorly differentiated ones, as supported by results in basilisks and Paroedura geckos [130][131][132] (case 10 in figure 2). Ogata et al [66] revealed that the heteromorphic sex chromosome systems probably returned to homomorphy through hybridization in the Japanese wrinkled frog Glandirana rugosa. In some cases, a simple system of two sex chromosomes changed into derived systems of three homologous sex chromosomes present in a population, e.g.…”

Section: Is the Sex Chromosome Differentiationmentioning

confidence: 99%

“…Haldane's effects may lead to less introgression of loci linked to well-differentiated sex chromosomes across hybrid zones in comparison to autosomes. By contrast, undifferentiated sex chromosomes might be more susceptible to introgression and may contribute to the emergence of multi-locus systems [65] or other derived sex determination systems [66] (case 20 in figure 2). Hybrids of parental species with higher divergence may exhibit sex-specific distortions of gametogenesis typified by potential male sterility and frequently female clonality, often closely linked to polyploidization [67][68][69].…”

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confidence: 99%

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Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Kratochvíl

Stöck

Rovatsos

et al. 2021

Phil. Trans. R. Soc. B

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Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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Section: Is the Sex Chromosome Differentiationmentioning

confidence: 99%

Section: Is the Sex Chromosome Differentiationmentioning

confidence: 99%

mentioning

confidence: 99%

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Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Kratochvíl

Stöck

Rovatsos

et al. 2021

Phil. Trans. R. Soc. B

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“…The sex-associated region on chromosome 4 could be a precursor to homomorphic sex chromosomes as we found no evidence of heteromorphic sex chromosomes. The potential sexdetermining region on chromosome 4 is small as there were only 2 sex-associated variants out of 418; therefore, a small and young homomorphic sex chromosome system could be present (Ogata et al 2021). Studies on sex chromosome evolution have shown that sex chromosomes usually evolve from homomorphic to heteromorphic (Charlesworth et al 2005).…”

Section: Evidence Of a Sex-associated Region In Bluehead Suckersmentioning

confidence: 99%

Identification of sex-determining loci in hybridizing Catostomus fish species

Pyne

McFarlane

Mandeville

2022

Preprint

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Despite the near-universality of gonochorism (separate sexes) in eukaryotic organisms, the underlying mechanisms of sex determination are poorly understood and highly variable in some taxa. In hybridizing species, sex determination mechanisms may promote or impede reproductive isolation depending on whether mechanisms are similar between species. In Catostomus fishes, contemporary hybridization is variable and extensive. In the present study, we aim to describe the genetic basis of sex determination in bluehead (Catostomus discobolus) and white suckers (Catostomus commersonii) to understand the impact of sex determination on reproductive isolation. We used genotyping-by-sequencing genomic data from Catostomus species and their hybrids to identify regions of the genome associated with sex using a genome-wide association study and the identification of sex-specific loci. We found a genetic basis of sex determination in Catostomus fishes, with a region of the genome significantly associating with sex in bluehead suckers. This region is suggestive of a master sex-determining region in bluehead suckers but is not significant in white suckers, implying that either the sex-determining region of the genome differs in these two species that hybridize, or that sample size was insufficient to identify this genomic region in white suckers. By describing and comparing sex-determination systems across Catostomus fish species, we highlight the relationship between sex determining systems and hybridization in closely related fish species.

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“…The Japanese soil‐frog Glandirana rugosa (formerly Rana rugosa ) is particularly well suited to address the above questions as it is highly diversified in sex‐determination and sex chromosomes. Previous studies on this species allow us to divide it into six geographic groups, based on sex‐determination, sex chromosomes, and mitochondrial DNA (Figure 1) (Miura, 2017; Ogata et al, 2021). The three populations, named ZW (northwestern Japan), XY (eastern Central Japan), and Neo‐ZW (western Central Japan), all have a heteromorphic sex chromosome system of ZW or XY on chromosome 7 in 13 haploid complements.…”

Section: Introductionmentioning

confidence: 99%

Identification of ancestral sex chromosomes in the frog Glandirana rugosa bearing XX‐XY and ZZ‐ZW sex‐determining systems

et al. 2022

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Sex chromosomes constantly exist in a dynamic state of evolution: rapid turnover and change of heterogametic sex during homomorphic state, and often stepping out to a heteromorphic state followed by chromosomal decaying. However, the forces driving these different trajectories of sex chromosome evolution are still unclear. The Japanese frog Glandirana rugosa is one taxon well suited to the study on these driving forces. The species has two different heteromorphic sex chromosome systems, XX‐XY and ZZ‐ZW, which are separated in different geographic populations. Both XX‐XY and ZZ‐ZW sex chromosomes are represented by chromosome 7 (2n = 26). Phylogenetically, these two systems arose via hybridization between two ancestral lineages of West Japan and East Japan populations, of which sex chromosomes are homomorphic in both sexes and to date have not yet been identified. Identification of the sex chromosomes will give us important insight into the mechanisms of sex chromosome evolution in this species. Here, we used a high‐throughput genomic approach to identify the homomorphic XX‐XY sex chromosomes in both ancestral populations. Sex‐linked DNA markers of West Japan were aligned to chromosome 1, whereas those of East Japan were aligned to chromosome 3. These results reveal that at least two turnovers across three different sex chromosomes 1, 3 and 7 occurred during evolution of this species. This finding raises the possibility that cohabitation of the two different sex chromosomes from ancestral lineages induced turnover to another new one in their hybrids, involving transition of heterogametic sex and evolution from homomorphy to heteromorphy.

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Sex chromosome evolution from a heteromorphic to a homomorphic system by inter-population hybridization in a frog

Cited by 19 publications

References 36 publications

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Identification of sex-determining loci in hybridizing Catostomus fish species

Identification of ancestral sex chromosomes in the frog Glandirana rugosa bearing XX‐XY and ZZ‐ZW sex‐determining systems

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