Switches, stability and reversals: the evolutionary history of sexual systems in fish

Quirante, Susanna Pla; Benvenuto, Chiara; Capellini, Isabella; Piferrer, Francesc

doi:10.1101/2021.01.25.428070

Cited by 4 publications

(4 citation statements)

References 318 publications

(182 reference statements)

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“…For example, they allow for selfing-avoidance and efficient specialization of an individual in a given time to a sex-specific function. Indeed, this might explain why simultaneous hermaphroditism is so rare among vertebrates [ 29 ]. However, it is less clear why some lineages rely on sex chromosomes while others do not.…”

Section: What Was the Situation Prior To The Origins Of Sex Chromosomes Under The Canonical Model? Why Are Sex Chromosomes Absent In Somementioning

confidence: 99%

“…In angiosperms, gonochorism evolved mostly from the ancestral simultaneous hermaphroditism [10], while in vertebrates, simultaneous hermaphroditism is extremely rare and very likely a derived condition. Likewise, sequential hermaphroditism, which occurs in teleost fishes, is also likely a derived condition [28,29] and tends to return to gonochorism [29]. Ohno [2] suspected that GSD (and thus sex chromosomes) evolved in amniotes multiple times independently from ancestral ESD.…”

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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: What Was the Situation Prior To The Origins Of Sex Chromosomes Under The Canonical Model? Why Are Sex Chromosomes Absent In Somementioning

confidence: 99%

mentioning

confidence: 99%

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 studies differ in relation with fluctuations in water temperature and population density in which the fish were kept, which demonstrates that the distinctions in animal management alter the labile period for sex differentiation during aquaculture. However, when not intentionally performed for aquaculture, sex reversal and the presence of intersex in gonochorist species is indeed worrying, as it promotes an imbalance between male:female sex ratios; for gonochorist species, it is natural for it to be 1:1, and variations may have harmful effects on the genetic variability of these species (Pla et al, 2021).…”

Section: Eleven Months-one Year Of Age: Sexual Maturitymentioning

confidence: 99%

Female sex inversion as a reason for an unbalanced sex ratio in the neotropical species Brycon orbignyanus

Quirino

Delgado

Gomes‐Silva

et al. 2021

Aquaculture Research

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The objective of this study was to temporally identify sex differentiation to morphologically characterize the formation of female and male germinal epithelium and verify the occurrence of the sex disproportion reported for this species in aquaculture. Specimens of Brycon orbignyanus cultivated in water recirculation systems with a constant temperature of 27 ± 0.5°C were used. Monthly samplings of B. orbignyanus (n = 15) were performed from two months of age until 1 year of age, and posteriorly isolated sampling was performed on specimens of two and three years of age. The gonads of the specimens were removed and processed for light microscopy. In the beginning, the undifferentiated gonads develop into ovaries (females; at three months of age) and functional testicles (primary males; at five months of age); however, some of the females go through a sex inversion process creating intersex individuals and posteriorly secondary males (at five months of age). Due to the processes of sex inversion and gonadal remodelling, the population sex proportion fluctuates until it is finally established at 1♀:2♂. Females above 15 cm are differentiated, while in males (primary and secondary), differentiation will only occur after the animal reaches 20 cm. At the end of the first year of age, primary males and secondary males reach sexual maturity, while female sexual maturity is only observed at three years of age.

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“…Looking across fish families and genera, the genetic basis of tSD can be profoundly different, and can also be determined entirely by external factors, e.g. social structure or attainment of a critical age (Pla et al 2021). Importantly, it should be noted that for most fish species it is unknown how sex is genetically determined and what the genetic architecture is (e.g.…”

Section: Introductionmentioning

confidence: 99%

The genome of New Zealand trevally (Carangidae: Pseudocaranx georgianus) uncovers a XY sex determination locus

Ruigrok

Catanach

Bowatte

et al. 2021

Preprint

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Background: The genetic control of sex determinism in teleost species is poorly understood. This is partly because of the diversity of sex determining mechanisms in this large group, including constitutive genes linked to sex chromosomes, polygenic constitutive mechanisms, environmental factors, hermaphroditism, and unisexuality. Here we use a de novo genome assembly of New Zealand silver trevally (Pseudocaranx georgianus) together with whole genome sequencing to detect sexually divergent regions, identify candidate genes and develop molecular makers. Results: The de novo assembly of an unsexed trevally (Trevally_v1) resulted in an assembly of 579.4 Mb in length, with a N50 of 25.2 Mb. Of the assembled scaffolds, 24 were of chromosome scale, ranging from 11 to 31 Mb. A total of 28416 genes were annotated after 12.8% of the assembly was masked with repetitive elements. Whole genome re-sequencing of 13 sexed trevally (7 males, 6 females) identified sexually divergent regions located on two scaffolds, including a 6 kb region at the proximal end of chromosome 21. Blast analyses revealed similarity between one region and the aromatase genes cyp19 (a1a/b). Males contained higher numbers of heterozygous variants in both regions, while females showed regions of very low read-depth, indicative of deletions. Molecular markers tested on 96 histologically-sexed fish (42 males, 54 females). Three markers amplified in absolute correspondence with sex. Conclusions: The higher number of heterozygous variants in males combined with deletions in females support a XY sex-determination model, indicating the trevally_v1 genome assembly was based on a male. This sex system contrasts with the ZW-type sex system documented in closely related species. Our results indicate a likely sex-determining function of the cyp19b-like gene, suggesting the molecular pathway of sex determination is somewhat conserved in this family. Our genomic resources will facilitate future comparative genomics works in teleost species, and enable improved insights into the varied sex determination pathways in this group of vertebrates. The sex marker will be a valuable resource for aquaculture breeding programmes, and for determining sex ratios and sex-specific impacts in wild fisheries stocks of this species.

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Switches, stability and reversals: the evolutionary history of sexual systems in fish

Cited by 4 publications

References 318 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

Female sex inversion as a reason for an unbalanced sex ratio in the neotropical species Brycon orbignyanus

The genome of New Zealand trevally (Carangidae: Pseudocaranx georgianus) uncovers a XY sex determination locus

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