Causes and consequences of evolutionary innovation: An experimental approach to evaluating assumptions and predictions in macroevolutionary theory

Abstract

It has long been noted that there are some adaptations that appear to have played a disproportionate role in determining the evolutionary trajectories of the clades in which they arose. These adaptations, often termed evolutionary innovations, are often associated with increases in diversity and expansions into new niche spaces. The historic nature of evolutionary innovations, however, largely limit our ability to draw conclusions about causes and consequences, leaving broad-scale explanations constrained to theory. Using the power of experimental evolution, this work aims to explore empircally theories concerning the origins and evolutionary consequences of innovations. I used one proposed innovation, multicellularity, a trait that reliably arises in brewers’ yeast (Saccharomyces cerevisiae) under certain selective conditions. Using genomic tools, I show that despite their disruptive nature, loss-of-function mutations in largely “non-regulatory genes” are the major causal genetic changes underpinning convergent evolution of experimental yeast populations toward multicellularity. I further show that one of these mutations is also associated with major transcriptional and physiological effects one of which, increased apoptosis, has been previously described as a multicellular adaptation. Data presented here suggests this is less likely a direct effect of loss of gene activity than of microenvironmental shifts associated with a multicellular lifestyle. Finally, I present research that suggests that adaptive responses to environmental challenges often associated with complex multicellularity, such as division of labor, may not represent optimal fitness solutions but rather reflect a balance between the costs and benefits of retained multicellularity. In sum, my results reveal that current theories regarding multicellularity as well as other innovations may, at best, be incomplete and that generalizations about causes and consequences of evolutionary innovations may prove more difficult to come by than many have suggested.