The role of tradeoffs among life-history traits in a filamentous fungus

Life history theory explains how an organism’s reproductive success is driven by trade-offs among life-history traits. Organisms can have contrasting life-history strategies. For example, Chinook salmons reproduce once and then they die (semelparity), whereas Atlantic salmons reproduce several times in their lifetime (iteroparity). What is an optimal life-history strategy for a filamentous fungus? Theory predicts that based on the quality and quantity of resources and the presence of competition, a fungus can be semelparous or iteroparous.

In the first part of this thesis, adaptive constraints experienced by fifteen natural isolates of A. nidulans during evolution in their natural environment have been tested. No significant correlation between growth rate and asexual spore yield was observed. Instead, there was a clear dependence of the two traits on sugar concentration and nutrient richness. Further, six natural isolates were selected for a short evolution experiment in one environment where the isolates showed most variation in growth and asexual reproduction. A negative correlation between growth rate and spore density was observed among independently evolved replicate populations that approached significance, but not between growth rate and spore yield. All changes occurred in an antagonistic fashion: increases in growth rate were associated with decreases in spore yield/density, and vice versa, indicating short-term adaptive constraints from a growth-reproduction trade-off.

In the remainder of the thesis, the scope and mechanisms of adaptation in an Aspergillus Short-term Evolution eXperiment (ASEX) were tested including the role of trade-offs between growth rate and asexual reproduction. Surprisingly, asexual spore yield consistently decreased in all the populations and changes in growth rate and spore yield approached significance.  The competitive fitness of the evolved populations relative to their ancestor had not improved either. However, fitness measurements for two populations using more recent predecessors as competitors suggested that non-transitive fitness interactions explained the lack of fitness increases relative to the ancestor. Upon closer inspection, all populations had evolved morphological diversity as early as in week 20.

Competition experiments between the two morphotypes ancestor-like (AL) and fluffy-like (FL) in head-to-head competitions at low and high frequencies showed that the two types were engaged in negative frequency-dependent fitness interactions. The two types engaged in resource competition in which FL was a superior competitor for the limiting nutrient (glucose).

The genomic basis of adaptation of the ASEX populations, based on genome-sequence analysis of clones from both morphotypes of all populations at week 10 and 52 of the experiment, showed that genes that were mutated in two or more populations, occurred more frequently than expected by chance, indicating that they were under positive selection. Except in one population, in all other tested populations, the two morphs from the final time point derived from unrelated genetic backgrounds, suggesting their frequent extinction and re-emergence.

In conclusion, there was little evidence for adaptive constraints from a trade-off between growth and reproduction in A. nidulans. In both laboratory evolution studies, I found a reduction in asexual spore yield and variable changes in mycelial growth rate, questioning their general role during adaptation in this filamentous fungus. Fungi occupy a wide range of niches and are essential players in recycling carbon and nitrogen in the biosphere. It is crucial to understand which components of fitness contribute to adaptation to these different ecological conditions. For this, we need to study the adaptive role of fitness components in fungal isolates from different niches and develop fungal-specific life-history models.