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Sex Determination: Why So Many Ways of Doing It?

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Sex Determination: Why So Many Ways of Doing It? Essay Sex Determination: Why So Many Ways of Doing It? Doris Bachtrog1*, Judith E. Mank2, Catherine L. Peichel3, Mark Kirkpatrick4, Sarah P. Otto5, Tia-Lynn Ashman6, Matthew W. Hahn7, Jun Kitano8, Itay Mayrose9, Ray Ming10, Nicolas Perrin11, Laura Ross12, Nicole Valenzuela13, Jana C. Vamosi14, The Tree of Sex Consortium" 1 University of California, Berkeley, Department of Integrative Biology, Berkeley, California, United States of America, 2 University College London, Department of Genetics, Evolution and Environment, London, United Kingdom, 3 Fred Hutchinson Cancer Research Center, Divisions of Human Biology and Basic Sciences, Seattle, Washington, United States of America, 4 University of Texas, Department of Integrative Biology, Austin, Texas, United States of America, 5 University of British Columbia, Department of Zoology, Vancouver, British Columbia, Canada, 6 University of Pittsburgh, Department of Biological Sciences, Pittsburgh, Pennsylvania, United States of America, 7 Indiana University, Department of Biology, Bloomington Indiana, United States of America, 8 National Institute of Genetics, Ecological Genetics Laboratory, Mishima, Shizuoka, Japan, 9 Tel Aviv University, Department of Molecular Biology and Ecology of Plants, Tel Aviv, Israel, 10 University of Illinois, Department of Plant Biology, Urbana- Champaign, Illinois, United States of America, 11 University of Lausanne, Department of Ecology and Evolution, Lausanne, Switzerland, 12 University of Oxford, Department of Zoology, Oxford, United Kingdom, 13 Iowa State University, Department of Ecology, Evolution and Organismal Biology, Ames, Iowa, United States of America, 14 University of Calgary, Department of Biological Sciences, Calgary, Alberta, Canada Abstract: Sexual reproduction is variance that is otherwise hidden [2]. or female depends on the presence of a an ancient feature of life on earth, While many unicellular organisms pro- single master sex-determining locus, the Sry and the familiar X and Y chromo- duce gametes of equal size (isogamy, see gene, on the male-limited Y chromosome. somes in humans and other model Box 1), sexual reproduction in most Expression of Sry early in embryonic species have led to the impression multicellular organisms has led to the development initiates testis differentiation that sex determination mecha- evolution of female and male gametes by activating male-specific developmental nisms are old and conserved. In differing in size (anisogamy), and often to networks, while in its absence, ovaries fact, males and females are deter- the evolution of two separate sexes. Even develop. The first visible signs of sexual mined by diverse mechanisms that though the outcome of sex determina- differentiation of the ovary and testis occur evolve rapidly in many taxa. Yet tion—whether an individual produces by the sixth week of gestation in humans this diversity in primary sex-deter- relatively few large ova or many small [6], and sex hormones initiate further sexual mining signals is coupled with sperm—is strongly conserved, a bewilder- differentiation in nongonadal tissues and conserved molecular pathways that ing number of underlying mechanisms can organs [7]. When this developmental pro- trigger male or female develop- trigger development as either a male or cess goes awry, the effects can be cata- ment. Conflicting selection on dif- female [3,4]. strophic, causing everything from ambigu- ferent parts of the genome and on In humans, sex is determined by sex ous external genitalia (which occurs in up to the two sexes may drive many of chromosomes (XX females, XY males). The one in 4,500 infants) to sterility (which is these transitions, but few systems X and Y chromosomes harbor dramatically more cryptic and difficult to diagnose but with rapid turnover of sex determi- different numbers and sets of genes (about may be far more common). nation mechanisms have been rig- orously studied. Here we survey 1,000 genes on the X and only a few dozen Like humans and most mammals, other our current understanding of how genes on the Y), yet they originated from genetic model systems, such as Drosophila and why sex determination evolves ordinary autosomes during the early evolu- melanogaster flies and Caenorhabditis elegans in animals and plants and identify tion of mammals (Figure 1). Restriction of nematodes, harbor sex chromosomes, and important gaps in our knowledge recombination followed by gene loss on the their commonalities have led to general that present exciting research op- Y has resulted in the morphological differ- assumptions about the conservation of sex portunities to characterize the evo- entiation of sex chromosomes (for a review determination mechanisms. However, lutionary forces and molecular of the molecular and evolutionary processes these model organisms present a false pathways underlying the evolution involved in Y degeneration, see [4,5]). The impression of stability in how sex is of sex determination. vast majority of genes on the sex chromo- determined, and their commonalities somes are not directly involved in sex mask the diversity and turnover in sex determination, and development as a male determination mechanisms that is readily Introduction Citation: Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, et al. (2014) Sex Determination: Why So Many Sex—the mixing of genomes via meiosis Ways of Doing It? PLoS Biol 12(7): e1001899. doi:10.1371/journal.pbio.1001899 and fusion of gametes—is nearly universal Published July 1, 2014 to eukaryotic life and encompasses a Copyright: ß 2014 Bachtrog et al. This is an open-access article distributed under the terms of the Creative diverse array of systems and mechanisms Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, [1]. One major role of sex is to bring provided the original author and source are credited. together alleles carried by different Funding: The Tree of Sex Consortium was funded by NESCent. The funders had no role in study design, data individuals, revealing beneficial genetic collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Essays articulate a specific perspective on a topic of broad interest to scientists. * E-mail: [email protected] " Membership of the Tree of Sex Consortium is provided in the Acknowledgments. PLOS Biology | www.plosbiology.org 1 July 2014 | Volume 12 | Issue 7 | e1001899 apparent when taking a broader taxonom- [18]). Thus, sex chromosomes that are separation of male and female gonads in ic view. In this article, we address three morphologically similar (homomorphic) the same individual, as in monoecious common myths about sex determination must be evolutionarily young, and in time plants with separate male and female and then deconstruct them based on a they too will degenerate. flowers (e.g., maize) and in most hermaph- broad taxonomic survey of animals and roditic animals. Alternatively, male and plants. The Myths Deconstructed female function can be separated in time within an individual, as found in many Myths of Sex Determination These myths do not survive a survey of plants (‘‘dichogamy,’’ [23]) and some sex determination systems across the tree animals (‘‘sequential hermaphroditism,’’ Myth 1: Sex is typically determined of life. To deconstruct these myths, we first by X and Y chromosomes [24]); slipper shells, for example, are born provide background on the evolution of male and become female later in life. Many biologists are habituated to think- separate sexes. We then summarize the Finally, male and female reproductive ing about sex determination through the diversity of sex-determining mechanisms organs can be segregated into different familiar examples of mammals and D. found among animals and plants and individuals, as in some plants (such as melanogaster, and assume that sex determi- discuss the evolutionary forces that drive papaya and cannabis) and most animals. nation by sex chromosomes is the norm, transitions among systems (Myth 1 revis- that males are XY and females are XX, Separate sexes have evolved indepen- ited). This is followed by a summary of dently many times among plants and and that sex chromosomes are a stable more recent findings on the underlying component of the genome. While biolo- animals, which suggests that there must molecular genetics of sex determination be an evolutionary cost to hermaphrodit- gists are generally aware of other modes of (Myth 2 revisited) and a deconstruction of ism, at least in some groups. Two major sex determination (such as female hetero- common misconceptions of sex chromo- hypotheses have been proposed to explain gamety in birds, temperature-dependent some evolution in humans and other the evolution of separate sexes. The first sex determination in reptiles, or develop- species (Myth 3 revisited). We conclude hypothesis is that there are trade-offs ment of males from unfertilized eggs in with an outlook for future research that between male and female function, such bees), these alternatives are often viewed as might improve our understanding of how as when mating displays enhance male strange and aberrant [8]. and why sex determination evolves so fitness but decrease female fitness. In this rapidly in many animals and plants. case, individuals can gain reproductive Myth 2: Sex is controlled by one advantages by specializing as a male or master-switch gene The Evolution of Separate Sexes female
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