Abstract:Sex-antagonistic (SA) genes are widely considered to be crucial players in the evolution of sex chromosomes, being instrumental in the arrest of recombination and degeneration of Y chromosomes, as well as important drivers of sex-chromosome turnovers. To test such claims, one needs to focus on systems at the early stages of differentiation, ideally with a high turnover rate. Here, I review recent work on two families of amphibians, Ranidae (true frogs) and Hylidae (tree frogs), to show that results gathered so… Show more
“…In addition, selection can favour the location of a sex-determining gene in a region enriched by genes with sexually antagonistic effects [176]. However, as argued by Perrin [109], there is little role for sexual antagonism in the evolution of sex chromosomes in ranids and it is thus unlikely that the nonrandom co-option observed in this group would reflect the sexually antagonistic selection. Likewise, Lichilín et al [75] did not find evidence that sex-linked genes contribute exceptionally to sexual dimorphism in a clade of cichlid fish.…”
Section: Is the Sex Chromosome Differentiationmentioning
confidence: 95%
“…Thus the question remains, are sex chromosomes indeed hotspots for the resolution of sexual conflict in the genome? Perrin [ 109 ] concludes that there is little support for a significant role of sexual antagonism in the evolutionary dynamics of sex chromosomes in ranid and hylid frogs. Comparative genomic studies demonstrate an extensive variability in the gene content of sex chromosomes across independently evolved sex determination systems, which are not particularly enriched with genes controlling sexual dimorphism.…”
Section: Which Mechanisms Are Responsible For the Reduction Of Recombination In Sex Chromosomes?mentioning
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)’.
“…In addition, selection can favour the location of a sex-determining gene in a region enriched by genes with sexually antagonistic effects [176]. However, as argued by Perrin [109], there is little role for sexual antagonism in the evolution of sex chromosomes in ranids and it is thus unlikely that the nonrandom co-option observed in this group would reflect the sexually antagonistic selection. Likewise, Lichilín et al [75] did not find evidence that sex-linked genes contribute exceptionally to sexual dimorphism in a clade of cichlid fish.…”
Section: Is the Sex Chromosome Differentiationmentioning
confidence: 95%
“…Thus the question remains, are sex chromosomes indeed hotspots for the resolution of sexual conflict in the genome? Perrin [ 109 ] concludes that there is little support for a significant role of sexual antagonism in the evolutionary dynamics of sex chromosomes in ranid and hylid frogs. Comparative genomic studies demonstrate an extensive variability in the gene content of sex chromosomes across independently evolved sex determination systems, which are not particularly enriched with genes controlling sexual dimorphism.…”
Section: Which Mechanisms Are Responsible For the Reduction Of Recombination In Sex Chromosomes?mentioning
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)’.
“…alleles advantageous for males and detrimental for females will be maintained in the population with higher frequency than those with the opposite effect [ 140 ]. However, the results gathered so far, especially in ranid frogs, provided no support for the theoretical role of sexually antagonistic genes in the evolutionary dynamics of sex chromosomes [ 141 , 142 ]. Alternatively, different genes involved in the sex-determining pathway can take over the role of the MSD gene and give rise to new sex chromosomes [ 47 , 143 , 144 ].…”
Section: Evolutionary Pathways Of Teleost Multiple Sex Chromosomes: Current State Of Knowledge and Further Research Directionsmentioning
Despite decades of cytogenetic and genomic research of dynamic sex chromosome evolution in teleost fishes, multiple sex chromosomes have been largely neglected. In this review, we compiled available data on teleost multiple sex chromosomes, identified major trends in their evolution and suggest further trajectories in their investigation. In a compiled dataset of 440 verified records of fish sex chromosomes, we counted 75 multiple sex chromosome systems with 60 estimated independent origins. We showed that male-heterogametic systems created by Y-autosome fusion predominate and that multiple sex chromosomes are over-represented in the order Perciformes. We documented a striking difference in patterns of differentiation of sex chromosomes between male and female heterogamety and hypothesize that faster W sex chromosome differentiation may constrain sex chromosome turnover in female-heterogametic systems. We also found no significant association between the mechanism of multiple sex chromosome formation and percentage of uni-armed chromosomes in teleost karyotypes. Last but not least, we hypothesized that interaction between fish populations, which differ in their sex chromosomes, can drive the evolution of multiple sex chromosomes in fishes. This underlines the importance of broader inter-population sampling in studies of fish sex chromosomes.
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)’.
“…To date, the studies by Christiansen [ 172 , 275 ] appear the most comprehensive ones to include sex chromosome information and sex determination in water frogs. Nevertheless, knowledge on master sex-determining genes, potential intraspecific variation (as observed in other ranid frogs [ 276 ]) and on their molecular genetic interactions in the hybrids is lacking. Figure 4 Inferred inheritance of male heterogametic (XY) sex determination loci in three hybridogenetic population systems of Western Palearctic water frogs ( Pelophylax esculentus complex).…”
Section: Examples Of Sex Chromosomes In Hybrid Clonal Hemiclonal Meroclonal (‘Asexual’) and Meiotic Allopolyploid Vertebratesmentioning
We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in ‘the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal (‘asexual’) hybrid vertebrates, where ‘asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of ‘asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5–22% based on mtDNA). These ‘asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid ‘asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, ‘asexuality' and polyploidy.
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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