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On the Evolution of Allorecognition and Somatic Fusion in Ascomycete Filamentous Fungi On the evolution of allorecognition and somatic fusion in ascomycete filamentous fungi Eric Bastiaans Thesis committee Promotor Prof. Dr B.J. Zwaan Professor of Genetics Wageningen University Co-promotors Dr D.K. Aanen Assistant professor, Laboratory of Genetics Wageningen University Dr A.J.M. Debets Associate professor, Laboratory of Genetics Wageningen University Other members Prof. Dr T.W. Kuyper, Wageningen University Prof. Dr H. Wösten, Utrecht University Prof. Dr N.P.R. Anten, Wageningen University Prof. Dr L. Sundström, University of Helsinki, Finland This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation On the evolution of allorecognition and somatic fusion in ascomycete filamentous fungi Eric Bastiaans Thesis submitted 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 Wednesday 27 May 2015 at 4 p.m. in the Aula. Eric Bastiaans On the evolution of allorecognition and somatic fusion in ascomycete filamentous fungi 128 pages. PhD thesis, Wageningen University, Wageningen, NL (2015) With references, with summaries in Dutch and English ISBN 978-94-6257-297-3 Contents Chapter 1 7 General introduction Chapter 2 19 Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition Chapter 3 35 High relatedness protects multicellular growth against somatic cheaters Chapter 4 53 Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects in Neurospora Chapter 5 67 Natural variation of heterokaryon incompatibility gene het-c in Podospora anserina reveals diversifying selection Chapter 6 97 General discussion References 103 Summary 111 Nederlandse samenvatting 115 Acknowledgments 121 Curriculum vitae 125 Education statement 127 6 Chapter 1 General introduction Eric Bastiaans 7 Chapter 1 The evolution of cooperation Cooperation can increase productivity or efficiency by exchange of goods and services with others. For example a house is built by a group of cooperating people. Each of these people is specialized and most productive in doing something different for example making a foundation, plumbing or roofing. By division of labour this house can be built much faster with less total work hours compared to when one person alone builds the same house. In nature, such division of labour can take extreme forms, such as in the social insects. Evolutionary theory predicts that individuals that can use available resources most efficiently for reproduction and survival in a certain environment will have the highest fitness, i.e. their genes will be transferred relatively more to the next generation. This will lead to selection of the best adjusted genotypes to that environment. By cooperating, individuals can potentially obtain a higher fitness than individuals that do not cooperate. Social insects like for example honeybees form colonies in which many sterile workers maintain the colony so that the queen of the colony can effectively reproduce. The workers themselves cannot reproduce which makes them true altruists that sacrifice their own reproduction for the benefit of the colony (Breed et al. 1982). Cooperation does not always involve division of labour as in the previous example, but cooperation can also be advantageous because a large group is simply more efficient to perform certain tasks than a single individual. For example, parasitic bacteria of the species Pseudomonas aeruginosa excrete siderophores, which are required for the uptake of iron (West and Buckling 2003). The excreted siderophores bind to insoluble iron after which the bacteria can take it up in their cells. Since the siderophores are excreted from the cell, they become a common good that all surrounding bacteria can use as well. If siderophores are produced by a large group this will be more efficient because relatively less siderophores will get lost by diffusion. Cooperation can be mutually beneficial, for example when there is a mechanism that enforces the receiver to cooperate as well. However, often cooperation is not mutually beneficial and gives a benefit for the receiver but is costly to the actor. This leads to a problem to explain the evolution of stable cooperation. Individuals that use the benefits provided by others, but do not contribute their fair share to cooperate, will have a selective advantage within a group of cooperating individuals. For example, in a group of siderophore producing bacteria it is advantageous not to invest costs in producing siderophores while using the siderophores produced by others. This way, every bacterium in the group has the same benefits from the common pool of siderophores but the non-producer has an advantage because it saves on the costs of producing siderophores. If this kind of selfish behaviour is a heritable mutation, it will be selected through natural selection, because of the relative advantage it provides to a carrier, until the social behaviour disappears completely. This theory, which predicts that cooperation is unstable because of its vulnerability to selfish or cheating individuals, is known as the tragedy of the commons (Hardin 1968) (figure 1-1, top panels). 8 General introduction Kin selection theory The most widely accepted theory to explain how cooperation within a species can evolve stably is Hamilton’s kin selection theory (Hamilton 1964a, b) also known as inclusive fitness theory. Essential in this theory is that cooperative behaviour or goods are directed with a higher probability to genetically related individuals, in such a way that the genes of the helper benefit more than the helping action costs. Hamilton’s rule summarizes this in the simple formulized condition that an allele for cooperation can be selected if rB > C. Where r is the average relatedness of the actor to the individuals receiving the benefit,B is the fitness benefit received from cooperating and C is the fitness cost for the cooperating individual. In other words the Benefit of cooperation should always be higher than the costs, but the difference between cost and benefit can be smaller if help is directed towards more related individuals. This principle has been used regularly to try to explain cooperation as observed in nature for example in the social insects (Foster et al. 2006). Kin selection on itself is not always sufficient to explain stable evolution and may require additional mechanisms (Bourke 2011). For example several social insect species require active policing against cheaters to compromise for a reduced relatedness between members of the colony (Ratnieks et al. 2006). The evolution of genetic kin recognition and Crozier’s paradox Kin selection requires a way to direct cooperation preferentially towards kin (genetically related individuals) rather than random individuals. One way is keeping kin together by population viscosity after propagation, as for example a bacterial colony on solid medium where bacteria stay next to each other after division. When individuals are more motile and are likely to meet non-kin, active kin discrimination is required for kin selection. Active kin discrimination can occur through the use of environmental or genetic cues (Grafen 1990). Whereas environmental cues, such as prior association or shared environment, are probably most important in higher organisms such as the social insects (Helanterä and Sundström 2007), kin discrimination in microorganisms usually involves genetic cues (West et al. 2007). Also in plants, some evidence for genetic kin recognition exists to regulate how roots of neighbouring plants interact, but little is known about possible mechanisms (Chen et al. 2012). Furthermore, kin recognition is also present in most multicellular organism to maintain relatedness among the cooperating cells within a multicellular individual (see next paragraph about multicellularity). Genetic kin recognition requires polymorphic recognition genes that have a higher probability to be shared between closely related individuals than between unrelated individuals. Crozier made a model based on colony forming marine invertebrates such as anemones, where neighbouring colonies can fuse if it they are clonally related, or actively compete by attacking each other if they are not closely related. This discrimination based on relatedness is genetically determined. Fusion between colonies is a cooperative process in which the individuals likely gain in fitness compared to actively competing with 9 Chapter 1 selection Cooperation: help is directed No cooperation towards each other, often in the form of a common good Non-cooperating individuals (cheaters) will destabilize cooperation. When cheaters occur together with cooperators A cooperative group has a higher fitness compared they will have a higher fitness because they do not have the to a group of non-cooperating individuals cost of helping, but receive the benefit of being helped. Crozier’s paradox selection Cooperation can be stabilized by genetic kin However Crozier (1986) predicted that genetic polymorphisms that recognition. Help is only directed towards restrict cooperation and cooperative fusion would disappear through related individuals based on similarity at positive frequency dependent selection. This will happen because on polymorphic recognition genes. This reduces
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