Sex, Outcrossing and Mating Types: Unsolved Questions in Fungi and Beyond
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doi: 10.1111/j.1420-9101.2012.02495.x REVIEW Sex, outcrossing and mating types: unsolved questions in fungi and beyond S. BILLIARD*, M. LO´ PEZ-VILLAVICENCIO ,M.E.HOODà &T.GIRAUD§– *Laboratoire de Ge´ne´tique et Evolution des Populations Ve´ge´tales, UMR CNRS 8016, Universite´ des Sciences et Technologies de Lille – Lille1, Villeneuve d’Ascq Cedex, France Origine, Structure, Evolution de la Biodiversite´, UMR 7205 CNRS-MNHN, Muse´um National d’Histoire Naturelle, Paris Cedex, France àDepartment of Biology, McGuire Life Sciences Building, Amherst College, Amherst, MA, USA §Ecologie, Syste´matique et Evolution, Universite´ Paris-Sud, Orsay cedex, France –Ecologie, Syste´matique et Evolution, CNRS, Orsay cedex, France Keywords: Abstract ascomycete; Variability in the way organisms reproduce raises numerous, and still asexual reproduction; unsolved, questions in evolutionary biology. In this study, we emphasize that basidiomycete; fungi deserve a much greater emphasis in efforts to address these questions breeding systems; because of their multiple advantages as model eukaryotes. A tremendous diploid selfing; diversity of reproductive modes and mating systems can be found in fungi, gametophytic selfing; with many evolutionary transitions among closely related species. In addition, haploid selfing; fungi show some peculiarities in their mating systems that have received little mating systems; attention so far, despite the potential for providing insights into important oomycetes; evolutionary questions. In particular, selfing can occur at the haploid stage in sexual reproduction. addition to the diploid stage in many fungi, which is generally not possible in animals and plants but has a dramatic influence upon the structure of genetic systems. Fungi also present several advantages that make them tractable models for studies in experimental evolution. Here, we briefly review the unsolved questions and extant hypotheses about the evolution and mainte- nance of asexual vs. sexual reproduction and of selfing vs. outcrossing, focusing on fungal life cycles. We then propose how fungi can be used to address these long-standing questions and advance our understanding of sexual reproduction and mating systems across all eukaryotes. fields of biotechnology, breeding and artificial selection Introduction (Whitton et al., 2008), conservation biology (e.g. Fre´ville The process of reproduction is one of the most variable et al., 2007), species invasion (Barrett, 2011) and path- traits in the living world, with organisms giving rise to ogen evolution and control (Shea et al., 2000; Zuk, progeny either clonally or sexually, and in the latter case 2009). by selfing or outcrossing (see the Glossary for defini- The prevalence of sexual or asexual reproduction is tions). Understanding what factors shape an organism’s highly variable among eukaryotes, with the vast majority reproductive mode is of fundamental importance because of taxa being able to perform sexual reproduction either patterns of inheritance drastically affect major evolution- exclusively (e.g. mammals) or alternatively with clonality ary and ecological processes (adaptation, e.g. Charles- (e.g. aphids, ciliates, many angiosperms and fungi). worth & Charlesworth, 1995; Otto, 2009; colonization, Sexual reproduction implies the succession of haploid e.g. Busch, 2011; Richards, 2003), as well as the applied and diploid phases, transitions occurring by meiosis, where recombination and chromosomal segregation Correspondence: Sylvain Billiard, Laboratoire de Ge´ne´tique et Evolution des occur, and syngamy, where two haploids fuse. The Populations Ve´ge´tales, UMR CNRS 8016, Universite´ des Sciences et long-term persistence of eukaryotes relying exclusively Technologies de Lille – Lille1, F-59655 Villeneuve d’Ascq Cedex, France. Tel.: (+33)3 20 33 59 23; fax: (+33)3 20 43 69 79; on asexual reproduction is rare and is thought to include e-mail: [email protected] the famous bdelloid rotifers (Welch et al., 2000), ª 2012 THE AUTHORS. J. EVOL. BIOL. JOURNAL OF EVOLUTIONARY BIOLOGY ª 2012 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 S. BILLIARD ET AL. Fig. 1 Synthetic view of the different possible modes of reproduction in homothallic vs. heterothallic fungi and oomycetes. *Some diploid selfing may be possible for heterothallic oomycetes but only when in presence of a different mating partner, i.e. when also performing outcrossing. Glomeromycota fungi (Kuhn et al., 2001), some insects extended haploid life stage such as ascomycete fungi, and some plants (Judson & Normark, 1996). Even in mosses, ferns and some algae, selfing is sometimes these textbook examples of asexuality, however, recent possible through the fusion of two mitotic descendants studies have suggested the occurrence of cryptic sex, in of the same haploid cell, which is called intrahaploid particular, because all the genes required for the meiotic mating, intragametophytic selfing (Hedrick, 1987), same- machinery are maintained in the genomes (Schurko clone mating (Perrin, 2012), gametophytic selfing (Epinat et al., 2009; Halary et al., 2011). & Lenormand, 2009) or haploid selfing (Billiard et al., Mating systems, governing which haploids fuse at 2011). Diploid selfing and haploid selfing can have syngamy, are also highly variable: most species under- very different consequences for genetic structure, and go predominantly selfing or outcrossing, whereas a few care should be taken in the application of different species show a mixed-mating system in both animals terms to describe their occurrence in eukaryotes. and plants (e.g. Jarne & Auld, 2006; Igic & Kohn, The proximate mechanisms controlling mating systems 2006). Outcrossing results from the syngamy between are also highly diverse (sometimes called ‘breeding haploid cells produced by separate diploid individuals, systems’, Neal & Anderson, 2005); obligate outcrossing whereas selfing results from the syngamy between can result, for instance, from the existence of (i) separate haploid cells produced by the same diploid individual sexes (even though outcrossing may not be the main (Figs 1 and 2). Selfing occurs in plants and animals force responsible for the evolution of separate sexes), through the fusion of gametes produced from meioses (ii) sexual morphs (e.g. heterostyly in angiosperms, of a single diploid individual, referred to as diploid where two morphs with different stigma and pistil selfing. In some eukaryotes, in particular those with an lengths coexist in populations, mating being only possible ª 2012 THE AUTHORS. J. EVOL. BIOL. JOURNAL OF EVOLUTIONARY BIOLOGY ª 2012 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Sexy fungi 3 Fig. 2 Illustration of the different modes of reproduction and mating systems in fungi. between individuals of different morphs), (iii) molecular Evolutionary biologists attempt to explain the deriva- recognition mechanisms (e.g. self-incompatibility sys- tion of particular reproductive modes in terms of fitness tems in angiosperms), or (iv) asynchrony in the produc- benefits and costs. Sexual reproduction can induce tion of male and female gametes in an individual (see fitness costs through energetic, genetic transmission Barrett, 2010 for a review). The tendency for selfing can and demographic constraints compared to asexual repro- result, for instance, from nonopening hermaphroditic duction (see Otto, 2009; Lehtonen et al., 2012, for flowers (cleistogamy) or developmental proximity be- reviews). When sex requires males that contribute only tween gametes from the same individual (Giraud et al., with their genes and do not directly produce offspring, a 2008). mutation allowing females to reproduce independently Biologists have struggled for more than a century to of males, either asexually or through various forms of identify factors responsible for the evolution of such self-fertilization, is expected to invade because its prog- preference for outcrossing vs. selfing or for sexual vs. eny grows at twice the rate of the ancestral lineage (the asexual reproduction. Sexual reproduction has appar- famous ‘two-fold cost of males’; Maynard Smith, 1978). ently been lost independently in diverse eukaryotes Recombination can furthermore break locally adapted (reviewed in fungi, Billiard et al., 2011; Lobuglio et al., combinations of alleles at multiple loci, which is called 1993; Lo´ pez-Villavicencio et al., 2010; Kuhn et al., 2001; the recombination load. Even in organisms without in microsporidia, Ironside, 2007; in animals, Simon et al., either separate sexes or outcrossing, however, meiosis 2003; and in plants, Whitton et al., 2008). However, itself can be costly because it takes more time and energy there is growing evidence that some species long thought than mitotic cell divisions. Other costs of sex may apply to be asexual undergo cryptic sex (Burt et al., 1996; in specific systems: cost of finding and courting a mate, Schurko et al., 2009; Lee et al., 2010). Nevertheless, risk of predation or contracting sexually transmitted anciently asexual lineages undoubtedly exist in many diseases or parasitic genetic elements. On the other hand, different taxonomic groups, as revealed, for instance, by sex is considered to provide benefits, both proximate (e.g. the Meselson effect, in which the divergence between DNA repair) and ultimate, by limiting the accumulation alleles in the two nuclei of each cell is so great that it can of deleterious mutations and by creating novel and only be explained by a long divergence without recom- advantageous genetic combinations,