A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

Stöck

Rovatsos

et al. 2021

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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)’.

Section: Is There Variation In Sex Chromosome Differentiation Between Male (Xx/xy) and Female (Zz/zw) Heterogamety?mentioning

confidence: 99%

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

Stöck

Rovatsos

et al. 2021

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“…old, poorly differentiated sex chromosomes with little degeneration for a long evolutionary time [12,13].…”

Section: Why Should the Emergence Of Sex Chromosomes Be Non-random?mentioning

confidence: 99%

Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?

Gamble

Rovatsos

2021

Sex chromosomes are a great example of a convergent evolution at the genomic level, having evolved dozens of times just within amniotes. An intriguing question is whether this repeated evolution was random, or whether some ancestral syntenic blocks have significantly higher chance to be co-opted for the role of sex chromosomes owing to their gene content related to gonad development. Here, we summarize current knowledge on the evolutionary history of sex determination and sex chromosomes in amniotes and evaluate the hypothesis of non-random emergence of sex chromosomes. The current data on the origin of sex chromosomes in amniotes suggest that their evolution is indeed non-random. However, this non-random pattern is not very strong, and many syntenic blocks representing putatively independently evolved sex chromosomes are unique. Still, repeatedly co-opted chromosomes are an excellent model system, as independent co-option of the same genomic region for the role of sex chromosome offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and gene identity. Future studies should use these systems more to explore the convergent/divergent evolution of 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)’.

“…Using chromosome-scale assemblies and pool-sequencing, an approximately 16 kb female-specific sequence from sterlet ( Acipenser ruthenus ) was detected by Kuhl et al . [ 84 ]. A polymerase chain reaction-genotyping test, yielding female-specific products in six sturgeon species, spanning the entire phylogeny with the most divergent extant lineages ( Acipenser sturio, Acipenser oxyrinchus versus Acipenser ruthenus, Huso huso ), stemming from an ancient tetraploidization.…”

Section: Overview Of Current Knowledge About Sex Evolution Across the Vertebrate Phylogenymentioning

confidence: 99%

“…Similar results were obtained in two octoploid species ( Acipenser gueldenstaedtii, Acipenser baerii ). Phylogenetic conservation during 180 Myr of sturgeon evolution and across at least one polyploidization event revealed the oldest known vertebrate system with undifferentiated sex chromosomes, based presumably on a ZZ/ZW-mode of sex determination [ 84 ].…”

Section: Overview Of Current Knowledge About Sex Evolution Across the Vertebrate Phylogenymentioning

confidence: 99%

A brief review of vertebrate sex evolution with a pledge for integrative research: towards ‘sexomics’

Stöck

Kuhl

et al. 2021

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Triggers and biological processes controlling male or female gonadal differentiation vary in vertebrates, with sex determination (SD) governed by environmental factors or simple to complex genetic mechanisms that evolved repeatedly and independently in various groups. Here, we review sex evolution across major clades of vertebrates with information on SD, sexual development and reproductive modes. We offer an up-to-date review of divergence times, species diversity, genomic resources, genome size, occurrence and nature of polyploids, SD systems, sex chromosomes, SD genes, dosage compensation and sex-biased gene expression. Advances in sequencing technologies now enable us to study the evolution of SD at broader evolutionary scales, and we now hope to pursue a sexomics integrative research initiative across vertebrates. The vertebrate sexome comprises interdisciplinary and integrated information on sexual differentiation, development and reproduction at all biological levels, from genomes, transcriptomes and proteomes, to the organs involved in sexual and sex-specific processes, including gonads, secondary sex organs and those with transcriptional sex-bias. The sexome also includes ontogenetic and behavioural aspects of sexual differentiation, including malfunction and impairment of SD, sexual differentiation and fertility. Starting from data generated by high-throughput approaches, we encourage others to contribute expertise to building understanding of the sexomes of many key vertebrate species. 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 I)’.