Unusual Mammalian Sex Determination Systems: A Cabinet of Curiosities

Saunders, Paul A.; Veyrunes, Frédéric

doi:10.3390/genes12111770

Cited by 23 publications

(20 citation statements)

References 184 publications

(262 reference statements)

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“…In natura , only few rodent species display atypical sex determination system with loss of the Y chromosome in males, or females carrying a Y chromosome (Saunders & Veyrunes, 2021). Among them, the African pygmy mouse, Mus minutoides , is peculiarly interesting as its evolution led to a third feminizing sex chromosome, X*, and three distinct female genotypes, XX, XX* and X*Y, while all males are XY (Veyrunes et al, 2010a).…”

Section: Introductionmentioning

confidence: 99%

Genotypic sex shapes maternal care in the African Pygmy mouse,Mus minutoides

Heitzmann

Challe

Pérez

et al. 2022

Preprint

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Parental care, one of the most sexually dimorphic behaviour in mammals, was long thought to be driven mostly, if not exclusively, by gonadal hormones. Over the past two decades, very few studies have challenged this view, highlighting the direct influence of the sex chromosome complement (XX vs XY). The African pygmy mouse, Mus minutoides , is a wild mouse species with a naturally occurring sex reversal due to a third, feminizing X* chromosome, leading to three female genotypes: XX, XX* and X*Y. Here, we show that the sex reversal in X*Y females shapes a divergent maternal care strategy from both XX and XX* females, rather than altering care quality. In addition, the sex reversal is likely to impact the dopaminergic system in the anteroventral periventricular nucleus of the hypothalamus, consistent with one component of maternal care: pup retrieval. Combining neurobiology and behavioural ecology in a wild mouse species subject to natural selection, we evaluate here the neural basis of maternal behaviours and strengthen the underestimated role of the sex chromosome in shaping sex differences in brain and behaviours. Furthermore, we highlight the emergence of a third sexual phenotype, challenging the binary view of sexes.

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Section: Introductionmentioning

confidence: 99%

Genotypic sex shapes maternal care in the African Pygmy mouse,Mus minutoides

Heitzmann

Challe

Pérez

et al. 2022

Preprint

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“…Other taxa have much more diversity in terms of sex chromosome identity and some likely tolerate a lack of Y chromosome much better than most Drosophila species. For instance, the Y is often required for fertility in the vast majority of mammals, except the mole vole ( Ellobius lutescens ), Tokudaia genus rodents, and the creeping vole ( Microtus Oregoni , with XO female sex-determining system) with natural XO male sex-determining system (reviewed by (Saunders and Veyrunes, 2021)). In addition, some groups such as Coleoptera and Diptera, have multiple independent losses of the Y chromosome (Blackmon and Demuth, 2014), and certain Lepidoptera insects lost the W chromosome and became a ZO sex-determining system (Traut et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Hoisted with his own petard: how sex-ratio meiotic drive in Drosophila affinis creates resistance alleles that limit its spread

Patch

Knoles

et al. 2022

Preprint

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Meiotic drivers are selfish genetic elements that tinker with gametogenesis to bias their own transmission into the next generation of offspring. Such tinkering can have significant consequences on gametogenesis and end up hampering the spread of the driver. In Drosophila affinis, sex-ratio meiotic drive is caused by an X-linked complex that, when in males with a susceptible Y chromosome, results in broods that are more than 95% female. Interestingly, D. affinis males lacking a Y chromosome (XO) are fertile and males with the meiotic drive X and no Y produce only sons - effectively reversing the sex-ratio effect. Here, we show that meiotic drive dramatically increases the rate of nondisjunction of the Y chromosome (at least 50X), meaning that the driver is creating resistant alleles through the process of driving. We then model how the O might influence the spread, dynamics and equilibrium of the sex-ratio X chromosome. We find that the O can prevent the spread or reduce the equilibrium frequency of the sex-ratio X chromosome and it can even lead to oscillations in frequency. Finally, with reasonable parameters, the O is unlikely to lead to the loss of the Y chromosome, but we discuss how it might lead to sex-chromosome turnover indirectly.

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“…Persistent Y chromosomes, and those with achiasmatic meiotic pairing, are stable with no observation of being lost (green ovals). In a few unusual rodents (e.g., Lasiopodomys mandarinus , Dicrostonyx torquatus , Myopus schistocolor , Mus minutoides ; Gil-Fernández et al 2021 ; Saunders and Veyrunes 2021 ), persistent Ys have gained achiasmatic meiotic pairing. In a few other unusual rodent groups (e.g., Ellobius and Ryukyu spiny rats; Arakawa et al 2002 ; Matveevsky et al 2017 ) executioner protection has been removed, resulting once more in a wimpy and fragile Y, permitting its loss in some species (orange ovals).…”

Section: Theories Of Y Chromosome Evolutionmentioning

confidence: 99%

Fragile, unfaithful and persistent Ys—on how meiosis can shape sex chromosome evolution

Ruiz‐Herrera

Waters

2022

Heredity

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Sex-linked inheritance is a stark exception to Mendel’s Laws of Heredity. Here we discuss how the evolution of heteromorphic sex chromosomes (mainly the Y) has been shaped by the intricacies of the meiotic programme. We propose that persistence of Y chromosomes in distantly related mammalian phylogroups can be explained in the context of pseudoautosomal region (PAR) size, meiotic pairing strategies, and the presence of Y-borne executioner genes that regulate meiotic sex chromosome inactivation. We hypothesise that variation in PAR size can be an important driver for the evolution of recombination frequencies genome wide, imposing constraints on Y fate. If small PAR size compromises XY segregation during male meiosis, the stress of producing aneuploid gametes could drive function away from the Y (i.e., a fragile Y). The Y chromosome can avoid fragility either by acquiring an achiasmatic meiotic XY pairing strategy to reduce aneuploid gamete production, or gain meiotic executioner protection (a persistent Y). Persistent Ys will then be under strong pressure to maintain high recombination rates in the PAR (and subsequently genome wide), as improper segregation has fatal consequences for germ cells. In the event that executioner protection is lost, the Y chromosome can be maintained in the population by either PAR rejuvenation (extension by addition of autosome material) or gaining achiasmatic meiotic pairing, the alternative is Y loss. Under this dynamic cyclic evolutionary scenario, understanding the meiotic programme in vertebrate and invertebrate species will be crucial to further understand the plasticity of the rise and fall of heteromorphic sex chromosomes.

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Unusual Mammalian Sex Determination Systems: A Cabinet of Curiosities

Cited by 23 publications

References 184 publications

Genotypic sex shapes maternal care in the African Pygmy mouse,Mus minutoides

Genotypic sex shapes maternal care in the African Pygmy mouse,Mus minutoides

Hoisted with his own petard: how sex-ratio meiotic drive in Drosophila affinis creates resistance alleles that limit its spread

Fragile, unfaithful and persistent Ys—on how meiosis can shape sex chromosome evolution

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