Hopeful monsters: The role of hybrids in adaptation : The impact of hybridisation and genetic diversity on adaptation to stressful and novel environments

Adaptation to novel environments can only occur if natural selection has the raw material to act upon. But small, endangered populations are often genetically depleted, and the acquisition of beneficial de novo mutations often takes too long when population face quick and extreme environmental change. An alternative source for new variation is hybridisation and the genomic reshuffling and structural chromosomal changes accompanying it. In this thesis, I use yeast, experimental evolution, and comparative genomics to investigate the impact of different sources of genetic variation in adaptation to stressful environments - standing genetic variation, de novo mutations, and hybridisation. In Chapter I, I investigate the role of aneuploidy in the adaptation of microbial eukaryotes and the genetic mechanisms causing erroneous chromosome segregation, using a meta-analysis. I found that smaller chromosomes are more often aneuploid and that the frequency of segregation errors during cell division is higher in genomes with higher initial ploidy. I also propose that the co-occurrence of hybridisation and aneuploidy may provide an adaptive advantage in stressful environments. Traditionally, microbial experimental evolution studies start with clonal populations, relying on adaptation from de novo mutations alone. In the wild, this is an unlikely scenario. In Chapter II, I evolved genetically diverse founder populations for up to 1000 generations in 4 distinct environments and tracked adaptation dynamics at the phenotypic and genomic level. Almost all populations rapidly increased in fitness but the underlying allele frequency changes were surprisingly diverse and environment-specific. While in some populations all ancestral variation went to fixation in < 30 generations, others maintained genetic diversity across hundreds of generations. I found stunning parallelism of de novo mutations at the gene and pathway level and detected potentially adaptive aneuploidies. Hybridisation drastically boosts the genetic diversity of populations, which can allow for transgressive hybrids (hopeful monsters) with selective advantages in novel environments. In Chapter III, I made hybrid crosses at increasing parental divergence (using divergently evolved populations from Chapter II) and measured how much heterosis and transgressive segregation occurred in F1 and F2 hybrids when exposing them to 50 new, stressful environments. I found that both heterosis and transgression increased as a function of parental divergence, confirming predictions of quantitative genetics theory. Some hybrids were even able to survive in arsenic concentrations lethal for both parents. Anthropogenic climate change drives up rates of hybridisation between natural populations, yet the potential benefits and risks of hybridisation for the long-term conservation of populations are often unknown. In Chapter IV, I compared the survivability of hybrid populations to their parents under deteriorating environmental conditions. I found that hybrids avoided extinction for a significantly longer time than their parents, at all levels of parental divergence. The more divergent the parents the more similar were the responses of replicate crosses, likely due to the erosion of standing genetic variation in the parental populations. In summary, my thesis provides a better understanding of the impact of different sources of genetic diversity in determining a population’s capacity to adapt to environmental change