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Sexual Selection in Fungi

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Sexual Selection in Fungi Sexual selection in Fungi Bart P. S. Nieuwenhuis Thesis committee Thesis supervisor Prof. dr. R.F. Hoekstra Emeritus professor of Genetics (Population and Quantitative Genetics) Wageningen University Thesis co-supervisor Dr. D.K. Aanen Assistant professor at the Laboratory of Genetics Wageningen University Other members Prof. dr. J. B. Anderson, University of Toronto, Toronto, Canada Prof. dr. W. de Boer, NIOO, Wageningen and Wageningen University Prof. dr. P.G.L. Klinkhamer, Leiden University, Leiden Prof. dr. H.A.B. Wösten, Utrecht Univesity, Utrecht This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation (PE&RC) Sexual selection in Fungi Bart P. S. Nieuwenhuis Thesis submittted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Friday 21 September 2012 at 4 p.m. in the Aula. Bart P. S. Nieuwenhuis Sexual selection in Fungi Thesis, Wageningen University, Wageningen, NL (2012) With references, with summaries in Dutch and English ISBN 978-94-6173-358-0 Contents Chapter 1 7 General introduction Chapter 2 17 Why mating types are not sexes Chapter 3 31 On the asymmetry of mating in the mushroom fungus Schizophyllum commune Chapter 4 49 Sexual selection in mushroom-forming basidiomycetes Chapter 5 59 Fungal fidelity: Nuclear divorce from a dikaryon by mating or monokaryon regeneration Chapter 6 69 Fungal nuclear arms race: experimental evolution for increased masculinity in a mushroom Chapter 7 89 Sexual selection in the fungal kingdom Chapter 8 109 Discussion: male and female fitness Bibliography 121 Summary 133 Dutch summary 137 Dankwoord 147 Curriculum vitea 153 Education statement 155 6 Chapter 1 General introduction Bart P. S. Nieuwenhuis 7 8 General introduction Sexual selection The theory of natural selection tells us that the individuals best adapted to their environment will survive best and get most offspring. The genes that code for these characteristics will in- crease in frequency and as a result extremely well adapted species evolve: perfectly streamlined fish, octopuses with environment dependent camouflage, or plants that catch insects in nutrient poor soils. On the other hand, any trait that is maladaptive is expected to be selected against. Nevertheless, there are many species with traits that appear not well adapted to their environ- ment at all, and these traits are often present in only one of the two sexes. For instance, male Montezuma swordtail fish with large tails swim less well, than males with smaller tails, which reduces their chance to escape predators (Kruesi & Alcaraz, 2007) and male collared lizards with more conspicuous coloration have an increased predation risk (Husak et al., 2006). Even though these traits lead to reduced survivorship, long tails or colourful skins are very common in natural populations of these species. Darwin was puzzled by these traits that appear to be detrimental for survival but are nev- ertheless maintained. Already in ‘On the Origin of Species’ (Darwin, 1859) he documented that such traits might give an advantage for a different component of natural selection than survival, viz. the relative mating success. He expanded on this theory in ‘The Descent of Man’ (Darwin, 1871). Next to staying alive, an individual of an outcrossing sexually reproducing species needs to find a mating partner and successfully mate in order to reproduce. The traits that seem to be a burden might actually contribute to success in mating. This part of natural selection is known as sexual selection. In many species, males have the opportunity to mate with multiple females and produce offspring with all of them. Potentially, one male can have a large share of the total offspring in the population, while other males reproduce much less or not at all. The number of offspring mainly depends on the number of females he mates with and, if a female mates with multiple males, the proportion of offspring per female. Because females can only produce a limited number of offspring, they are usually limiting for reproduction. This results in an operational sex ratio that is effectively skewed towards the males and thus the males will be in competition for the females. The more partners a male can mate with, the larger his share of the next generation will be, and, therefore, the higher his fitness. A female only needs to mate enough to get all her eggs fertilized, and can suffice with a few or even a single mating, and mating more often will not increase her fitness (Bateman, 1948). The most successful male is the one that is most effective in competition for the females. Males actively fight over females, as for instance seen in stags that gather the greatest harem. Another common scenario is when males are in competition to be chosen by the female. Because there are effectively more males that compete for each female, the females can be choosy to take only that mate (or those mates) that are most beneficial for her fitness. Famous examples of female choice are birds in which the males are showing off their quality, by singing, beautiful plumage, or performing complicated dances. Even though in gen- eral the males are in competition with each other for the females, competition is not restricted to 9 Chapter 1 males. Females compete with each other for males that can supply them with the best territory, paternal help, or that increase offspring quality (Clutton-Brock, 2009). Also during and after copulation, competition for fertilization continues between the gametes (Parker, 1970). If a female has mated multiple times, sperm from different males com- pete to fertilize the eggs. Different traits to increase this post-copulation competitiveness have evolved. For instance, in many species the penis has a dual function; next to transferring sperm, it removes sperm from competing males that mated with that female earlier, thus reducing di- rect sperm competition (e.g. Waage, 1979). Still, the female can affect the outcome of post- copulatory competition through female cryptic choice (Eberhard, 1996). In response males try to manipulate the female to use their sperm, for instance by producing seminal fluid proteins (Chapman, 2001). In many seed beetles, the male have spines on the penis that brutally harm the female genitalia to discourage her from re-mating at all, thereby monopolizing the female and her gametes (Hotzy & Arnqvist, 2009). Even when manipulations by the male are harmful to the female, and reduce her fitness, selection might favour such adaptations if the male manipulation increases his fitness (Parker, 2006). Sexual selection is an interesting driver of evolution, because it can select for traits that are harmful for viability and the probability to survive. Since individuals are only in competition over mating with individuals of their own sex, traits that increase successful mating but reduce survival, will most likely only come to expression in the sex where it is beneficial. Sexual selec- tion can thus lead to dimorphism between males and females that are not primarily meant for reproduction. Sexual selection theory is mostly applied to animals (Andersson, 1994; Carranza, 2009). Recently, sexual selection has also been recognized in plants, where selection has led to impressive flowers for attracting pollinators (Andersson & Simmons, 2006), and male pollen are competing to fertilize the female ovules (Snow & Spira, 1991). In sharp contrast, in fungi, sexual selection has not been generally considered. The traits in fungi that might be under sexual selection are less obvious than those investigated in macro-organisms, and in fungi there is no separation into males and females. Even though sexual selection in fungi is not so easily observed, fungi are not fundamentally different from other organisms: for sexual reproduction mating has to occur, and during mating different individuals can compete to increase their number of matings. In this thesis, I aim to show that sexual selection is also acting in fungi and I argue that it shapes the evolution of traits involved in fungal mating. Fungi as model organisms Many fundamental questions on the evolution and maintenance of sex and the mechanisms of sexual reproduction remain to be answered, such as: What are the benefits of sexual reproduc- tion? How do sex chromosomes evolve? How does meiosis work? Many of these questions can be studied using fungi, because the fungal kingdom is very diverse. Many different mating systems (e.g. inbreeding, selfing) and breeding systems (e.g. sexual compatibility) are present 10 General introduction in fungi, which makes them very interesting to study (Billiard et al., 2012). Comparing related species with different systems (e.g. López-Villavicencio et al., 2010), or unrelated species that show convergent evolution (e.g. Billiard et al., 2011) can be used to answer questions on how and when sex occurs. Fungi have been used for many years to study sexual reproduction. In contrast to most animals and plants, most fungi are haploid for a large part of their life cycle. Whereas in a diploid organism the two different alleles at a locus both can influence a trait of interest, in a haploid organism there is only one copy and its effect can be seen immediately. Another very convenient factor is that fungi produce meiotic products that remain together. This gives the opportunity to investigate how crossing-over occurs during a single meiosis. The four haploid gametes can be grown separately and a trait or gene of interest can be followed through meiosis. Add to this that most fungi can be maintained in the laboratory practically indefinitely, that they can be multiplied clonally and genetically modified rather easily, and it is clear that fungi are great model organisms.
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