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Evolution of Reproductive Systems in Hermaphroditism and Other

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Evolution of Reproductive Systems in Hermaphroditism and Other Heredity 68 (1992) 537—546 Genetical Society of Great Britain Received 25 June 1997 Evolution of reproductive systems in filamentous ascomycetes. II. Evolution of hermaphroditism and other reproductive strategies M. J. NAUTA & R. F. HOEKSTRA Department of Genetics, Agricultural University, Dreyen/aan 2, 6703 I-/AWageningen,The Netherlands Theevolution of different reproductive systems in filamentous ascomycetes is studied in a popula- tion genetic model. These fungi differ essentially from higher plants and animals because mating types can exist in addition to male and female gametes, and the conidia serve as both male gametes and asexual spores; moreover, selfing is genetically equivalent to asexual reproduction in these haploid organisms. A variable fitness of ascospore production is predicted as the explanation for the evolution of two systems that abundantly exist in nature: hermaphroditism in heterothallic species and the formation of both asexual and sexual spores in homothallic species. Imperfect fungi will evolve if sexual spores do not show a remarkably higher fitness than asexual spores. Keywords:ascomycetes,dioecy, evolution, hermaphroditism, reproduction. family of Sordariaceae, which contains a number of Introduction well-studied species such as Neurospora crassa and Agreat variety of reproductive systems exist in fila- Sordaria fimicola; many ascomycete mating systems mentous ascomycetes. Compared with the reproduct- are represented. ive systems in higher plants, some specific differences All heterothallic Sordariaceae investigated to date attract attention. The first is the possible occurrence of have both conidia (male gametes) and ascogonia (struc- mating types in addition to the existence of both male tures holding the female gamete) and can therefore be and female gametes [discussed in a previous study considered to be hermaphrodite. No report on a Nauta & Hoekstra, 1992], where only crossings natural dioecious filamentous ascomycete (i.e. with between male and female with unlike mating types are seperate male and female individuals) is known to us. possible. The second is that both sexual and asexual This leads to the question why, in Sordariaceae, spores exist, while the asexual spores (conidia) can hermaphrodites with mating types do occur, whereas often also function as male gametes. Finally the fact separate males and females without mating types, do that the gamete-producing individual is haploid has not. special implications for selfing and inbreeding. It is also remarkable that in many homothallic species Mating systems such as monoecy, dioecy, gyno- (such as the homothallic Neurosporas and Sordaria dioecy and trioecy are known in plants. The evolu- fimicola) the comdia are absent and ascogoma no tionary forces that can account for these different types longer form trichogynes (small hyphae growing have been thoroughly studied (Charlesworth & towards fertilizing conidia). This means that no asexual Charlesworth, 1978a, b; Charesworth & Ganders, spores are formed and outcrossing is probably very 1979; Gregorius et al., 1982, 1983; Ross, 1982): for rare, being only possible after heterokaryosis. fungi, however, such studies appear to be lacking. Another phenomenon in fungi, incomparable with This paper is a theoretical analysis of the evolu- higher plants, is the existence of imperfect fungi, in tionary relations between a number of fungal repro- which no sexual stage is found. Although taxonomi- ductive strategies. Attention is mainly limited to the cally they are not classified as ascomycetes, most can 537 538 M. J. NAUTA & R. F. HOEKSTRA Homothallic Heterothallic Fig. 1 Overview of the evolutionary transitions considered. Conidia are symbolized by a dot above a stalk, ascogonia by a cup on a stalk (ready to capture airborne conidia). Strictly self- / ing ascogonia that are not fertilized by conidia are symbolized by a cup covered with a lid. Arrows indicate / possible transitions between 1 homo- + thallics and heterothallics (Nauta & Hoekstra, 1992), (2) hermaphrodite, male and female heterothallics (Section A), (3) different types of homothallics (Section B). be considered as such because they show all the survive, or (3) on a site which is already occupied by characteristics of ascomycetes except a sexual cycle another individual. In the last case a landing conidium (e.g. Ainsworth, 1973). These imperfect fungi can be can fertilize an ascogonium of that individual, whereas considered as pure male ascomycetes, which only form a landing ascospore will get lost. It is assumed that conidia and no ascogonia. As there are no more there are always sufficient conidia in the population to females to fertilize, the conidia have ceased to function fertilize all available ascogonia. as male gametes and are now specialized asexual The 'twofold disadvantage of sex' (Maynard Smith, spores. 1971) or 'cost of genome dilution' (Lewis, 1987) is A model is developed in this study in an attempt to manifested in the production of ascospores. In the find evolutionary pathways for all these different ascospores half of the genes are of paternal origin (the mating systems (as illustrated in Fig. 1). The important conidium) and half of maternal origin (the asco- fitness parameters are the differences between sexual gonium), while in an asexual spore all genes are from and asexual reproduction and between selfing and out- 'paternal' origin. Although half of its genome is lost, a breeding. conidium may profit by sexual reproduction, because the female parent provides the resources to produce Themodel several (normally eight) ascospores out of one coni- dium. The female parent, however, experiences a two- Themodel organism in this study is the idealized fold cost of sex, compared to a situation where she ascomycete described previously (Nauta & Hoekstra, would produce asexual spores or selfed ascospores. It 1992). It has a haploid life cycle and in principle can is essential, therefore, that ascospores, being more form both conidia and ascogonia. In the young ascus, resistant and capable of remaining viable for long karyogamy and meiosis take place and the ascospores periods, have a higher fitness than asexual spores are formed. The population size is assumed to be (Perkins & Turner, 1988). In addition, some kind of infinite and generations are separated. inbreeding depression must occur to explain outbreed- It is assumed that the conidia and ascospores formed ing. are dispersed randomly over the habitat of the popula- Several types of individual are considered. They tion. They can land on three different types of sub- differ in the production of male and female gametes strate: (1) on an appropriate site where they can and in the frequency of self-fertilization. An individual germinate, (2) on an unfit site where they cannot that produces only conidia (a 'male') forms N conidia, REPRODUCTIVE STRATEGIES IN ASCOMYCETES 539 and an individual that produces only ascogonia (a 'female') forms n ascogonia. A hermaphrodite forms a)Vconidia and fin ascogonia. As the energy required to form a conidium (just a small cell) must be much lower than that needed to form an ascogonium (the receptive structure) plus a fruiting body filled with ascospores, we assume n 4 N. If all individuals can use the same amount of energy for reproduction, then a +fi1 for all hermaphrodites. This is assumed in the model, so we may define a =zand fi= 1 —z,where z is the 'maleness' of the individual. The selfing rate for homothallic species is s. Out- bred and selfed progeny have a relative fitness of 1 and d respectively. M As elaborated in Appendix I, a general recursion Fig.2 Results for heterothallism with constant ascospore fit- equation can be derived from these assumptions. It is ness 0, as described in section Al, with 0 =4and z —0.75. shown that the differences in fitness between sexual Frequencies of males (M), females (F), and hermaphrodites and asexual spores can be summarized by a single (H) are given in a de Finetti diagram. Starting with different parameter U for the fitness of ascospore production. frequencies x1, stability is reached when x1 +zx2=0/0 — I), When a population contains different types of indi- given as a solid line in the diagram. Arrows indicate the viduals, where type j has a frequency x, a maleness z1 frequency every subsequent generation. and a selfing rate s1, this general recurrence relation is given by: (1—sk)(1—zk)xk (see Appendix II) it can be deduced that the population A is in equilibrium if = 1+ Wxx z1 ZX x1+zx2=01. (2) (1) + 6(1-z)[1 -s(1 _2d)]} It is easy to see that for 0 2a pure male population is stable. This implies that with 0 2the evolution of imperfect fungi is expected. For 6>2 polymorphism is where stable; the equilibrium values of x depend on the start- ing frequencies and are located on a straight line seg- ment (Fig. 2). Thus, in an infinite population, one W=(1 —O)xkzk+O1—(1—d)(1Zk)SkXk k k should expect to find trioecy: populations with her- maphrodites, males and females. Notethat the model covers both homo- and hetero- In a finite population random genetic drift may thallic populations, but not populations polymorphic cause the frequencies in the population to change along for this trait. the equilibrium line (2). As stated in Appendix II no In subsequent sections a number of specific models specific tendency towards dioecy of hermaphroditism are analysed. The different types of individual and the could be found, so in the long-term a finite population possible transitions between them are shown may either become dioecious (males and females) or schematically in Fig. 1. A constant and a variable asco- consist of hermaphrodites with either males or females. spore fitness parameter 0 are considered. A2Heterothallic population with males, AlHeterothallic population with males, females and hermaphrodites. Variable females and hermaphrodites. Constant ascospore fitness 0 ascopore fitness 0 Sexualspores are often formed under conditions of stress Considera population with three types j, j =1repre- alone. In the model this can be represented by a vary- senting males (z =1,s1 =0),]=2representing herma- ing 6.
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