Novel evolutionary pathways of sex-determining mechanisms

    Research output: Contribution to journalArticle

    21 Citations (Scopus)

    Abstract

    Evolutionary transitions between sex-determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature-dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature-dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex-determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixedmechanism system that has not been revealed by previous approaches. This study solves two long-standing puzzles of the evolution of sex-determining mechanisms by illuminating the evolutionary pathways and endpoints.
    Original languageEnglish
    Pages (from-to)2544-2557
    Number of pages14
    JournalJournal of Evolutionary Biology
    Volume26
    Issue number12
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    sex determination
    gender
    sex reversal
    temperature
    chromosome
    incubation
    allele
    vertebrate
    viability
    genotype
    fitness
    mechanistic models
    sex chromosomes
    valley
    endpoints

    Cite this

    @article{916603ef77ea4941985424e8b79e097c,
    title = "Novel evolutionary pathways of sex-determining mechanisms",
    abstract = "Evolutionary transitions between sex-determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature-dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature-dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex-determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixedmechanism system that has not been revealed by previous approaches. This study solves two long-standing puzzles of the evolution of sex-determining mechanisms by illuminating the evolutionary pathways and endpoints.",
    keywords = "Amphibians, Charnov-Bull, Environmental sex determination, Fish, Genotypic sex determination, Reptiles, Sex-determining modes, Temperature-dependent sex determination",
    author = "Lisa Schwanz and Tariq EZAZ and Bernd GRUBER and Arthur GEORGES",
    year = "2013",
    doi = "10.1111/jeb.12258",
    language = "English",
    volume = "26",
    pages = "2544--2557",
    journal = "Journal of Evolutionary Biology",
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    publisher = "Wiley-Blackwell",
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    }

    Novel evolutionary pathways of sex-determining mechanisms. / Schwanz, Lisa; EZAZ, Tariq; GRUBER, Bernd; GEORGES, Arthur.

    In: Journal of Evolutionary Biology, Vol. 26, No. 12, 2013, p. 2544-2557.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Novel evolutionary pathways of sex-determining mechanisms

    AU - Schwanz, Lisa

    AU - EZAZ, Tariq

    AU - GRUBER, Bernd

    AU - GEORGES, Arthur

    PY - 2013

    Y1 - 2013

    N2 - Evolutionary transitions between sex-determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature-dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature-dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex-determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixedmechanism system that has not been revealed by previous approaches. This study solves two long-standing puzzles of the evolution of sex-determining mechanisms by illuminating the evolutionary pathways and endpoints.

    AB - Evolutionary transitions between sex-determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature-dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature-dependent sex reversal (e.g. XX male or XY female) was asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex reversal. We demonstrate that selection for TSD in a realistic sex-determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX/XY systems, sex reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixedmechanism system that has not been revealed by previous approaches. This study solves two long-standing puzzles of the evolution of sex-determining mechanisms by illuminating the evolutionary pathways and endpoints.

    KW - Amphibians

    KW - Charnov-Bull

    KW - Environmental sex determination

    KW - Fish

    KW - Genotypic sex determination

    KW - Reptiles

    KW - Sex-determining modes

    KW - Temperature-dependent sex determination

    U2 - 10.1111/jeb.12258

    DO - 10.1111/jeb.12258

    M3 - Article

    VL - 26

    SP - 2544

    EP - 2557

    JO - Journal of Evolutionary Biology

    JF - Journal of Evolutionary Biology

    SN - 1010-061X

    IS - 12

    ER -