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Inferences from Fungi on the Evolution of Anisogamy and Mating Types

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Biol. Rev. (2010), pp. 000–000. 1 doi: 10.1111/j.1469-185X.2010.00153.x Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types Sylvain Billiard1,∗,ManuelaLopez-Villavicencio´ 2, Benjamin Devier3,Michael E. Hood4,Cecile´ Fairhead5 and Tatiana Giraud3 1 Universit´e Lille Nord de France, USTL, GEPV, CNRS, FRE 3268, F-59650 Villeneuve d’Ascq, France 2 Origine, Structure, Evolution de la Biodiversit´e, UMR 7205 CNRS-MNHN, Mus´eum National d’Histoire Naturelle, CP39, 57 rue Cuvier, 75231 Paris Cedex 05, France 3 Ecologie, Syst´ematique et Evolution, Universit´e Paris-Sud, F-91405 Orsay cedex, France; CNRS F-91405 Orsay cedex, France 4 Department of Biology, McGuire Life Sciences Building, Amherst College, Amherst, MA 01002-5000, USA 5 Institut de G´en´etique et Microbiologie, Universit´e Paris-Sud, UMR CNRS 8621, F-91405 Orsay cedex, France (Received 3 November 2009; revised 15 July 2010; accepted 16 July 2010) ABSTRACT The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual repro- duction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zerotothousands,withmostoftenonlytwoclasses?Wereview here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the num- ber of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number. Key words: sexual reproduction, gametes, syngamy, mitochondrial inheritance, cytoplasmic genetic elements, gamete classes, mating types. CONTENTS I. Introduction ................................................................................................ 2 II. Models explaining the origin, number and loss of gamete classes ........................................... 3 (1) Origin of gamete classes ................................................................................ 3 (a) The ‘‘by-product’’ model ........................................................................... 3 (b) The ‘‘selfish element’’ model ........................................................................ 4 (c) The ‘‘inbreeding depression avoidance’’ model ..................................................... 4 (d) The ‘‘sex advantage enhancer’’ model .............................................................. 4 (e) The ‘‘ploidy’’ model ................................................................................ 4 (f ) The ‘‘organelle inheritance’’ model ................................................................. 4 (g) The ‘‘gamete size’’ model ........................................................................... 5 (h) The ‘‘anisogamy consequence’’ model .............................................................. 6 (2) The optimal number of gamete classes ................................................................. 6 * Address for correspondence: (E-mail: [email protected]). Biological Reviews (2010) 000–000 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society 2 Sylvain Billiard and others (a) The number of gamete classes depends on negative frequency-dependent selection and the effective size of the population ............................................................................... 6 (b) The number of gamete classes depends on their mechanism of origin .............................. 6 (c) The mating type number depends on the mating system ........................................... 6 (d) The mating type number depends on mating dynamics ............................................ 7 (e) The mating type number depends on genomic constraints ......................................... 7 (3) The loss or maintenance of gamete classes ............................................................. 7 (a) Gamete classes can be lost when population or ecological factors render universal compatibility advantageous ....................................................................................... 8 (b) Gamete classes can be maintained for the same reasons they appeared ............................. 8 III. Mating types, anisogamy and sex in fungi .................................................................. 8 (1) Anisogamy and mitochondrial inheritance in fungi .................................................... 8 (2) Mating types in fungi, homothallism and heterothallism ............................................... 9 IV. Origin, number and loss of gamete classes in fungi ......................................................... 10 (1) The origin and maintenance of gamete classes in fungi ................................................. 10 (a) The ‘‘organelle inheritance’’ model ................................................................. 14 (b) The ‘‘inbreeding depression avoidance’’ model ..................................................... 14 (c) The ‘‘sex advantage enhancer’’ model .............................................................. 14 (d)Othermodels ....................................................................................... 15 (e) An evolutionary scenario for the origin of gamete classes in fungi and in other taxa ................ 15 (2) The optimal number of gamete classes in fungi ........................................................ 16 (3) The loss and maintenance of gamete classes in fungi ................................................... 17 V. Conclusions ................................................................................................ 17 VI. Acknowledgements ......................................................................................... 18 VII. References .................................................................................................. 18 VIII. Supporting Information .................................................................................... 22 I. INTRODUCTION population evolve by natural selection? In the extreme, when there are two gamete classes, each gamete can only fuse with Sexual reproduction involves a variety of costs relative to one half of the potential gamete partners. How, then, can a asexual or clonal reproduction (e.g. energy, time, infection system with two gamete classes arise from a system with no risk, and the ‘‘cost of males’’ in anisogamous species), and restrictions? And why are there thousands of gamete classes many investigations have attempted to find evolutionary in some species while others have reverted to no size or benefits to sex that balance these costs (Otto, 2009). These mating type restrictions on syngamy? The most problematic investigations have mainly focused on the consequences of case, with the existence of two gamete classes, appears para- sex in terms of the genetic variation generated by recombi- doxically the most frequent among eukaryotes (male and female, or two mating types). Any new rare gamete class, natorial meiosis during the transition from the diploid to the being compatible with all other existing classes, should be haploid phase of the sexual life cycle. Syngamy, the counter- selected for, leading to an increase in the number of gamete part of meiosis that restores the diploid phase, has received classes. Both why gamete classes exist at all and what the much less attention, although the regulation of syngamy is forces are that act upon the number of classes need to be central to the evolution of sexual eukaryotes. Indeed, syn- understood from an evolutionary point of view. gamy is generally not random, occurring almost exclusively Broadly satisfying answers to the questions raised above through the combination of distinct and alternative gamete are still lacking, and groups such as fungi represent highly classes, such as small and large gametes (anisogamy, i.e. a suitable organisms to test various hypotheses that have been system regulating syngamy between different gamete classes put forward based upon theoretical grounds. Indeed, fungi that is dependent upon size) or gametes with different mating constitute a unique kingdom where all combinations of types (hereafter referring to a molecular mechanism of the gamete classes are represented, and with frequent transitions gamete allowing discrimination for syngamy, independent of between different numbers of mating types and/or gamete size dimorphism). We use the generic term ‘‘gamete classes’’ size dimorphism. Importantly, anisogamy is decoupled from to refer to forms of gametes that are intercompatible but that mating types in fungi, allowing separate consideration of cannot undergo syngamy within the same class, including the evolutionary forces acting on the two determinants of both anisogamy and mating types as properties that may gamete classes. Finally, data on the number of mating types, distinguish gamete classes (Fig. 1).
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