The fungal individual: an evolutionary perspective

The history of life has been driven by evolutionary transitions in individuality, i.e., the aggregation of autonomous individuals to form a new, higher-level individual. Theoretical expectations for such transitions are well defined. First, grouping has to yield benefits, arising for example from cooperation amongst members of the lower level of the group. On the other hand, conflicts between members of the group may arise and should be minimized, which can be achieved for example by ensuring genetic homogeneity, since intraorganismal diversity would mean that selfish variants, deleterious to the group-level, could evolve. In fungi, the concept of individuality is challenging. This is due to the fact that a fungal mycelium can contain millions of genetically diverse nuclei, each capable of giving rise to new mycelia. Furthermore, the fungal kingdom provides examples of transitions in individuality from homo- to heterokaryosis. In my research-group, we have studied the interaction between nuclei and mycelia in several fungal systems, but have focused much of our recent effort to understand individuality in the filamentous ascomycete Neurospora tetrasperma. This species has recently (approximately 1 MYA) evolved a mating system (pseudohomothallism) in which mating-type heterokaryosis is dominant throughout the life cycle. In N. tetrasperma, selection can act at different levels: while nuclei can compete in their replication and transmission into short-lived asexual spores, at the level of the heterokaryotic individual cooperation between nuclear types is required to produce the long-lived sexual spores. I will outline recent results on conflicts and cooperation among nuclei in heterokaryons of N. tetrasperma, and generalize our findings to shed light on evolutionary transitions in individuality.