Abstract
A common misconception is that evolution is a linear 'march of progress', where each organism along a line of descent is more fit than all those that came before it. Rejecting this misconception implies that evolution is nontransitive: a series of adaptive events will, on occasion, produce organisms that are less fit compared to a distant ancestor. Here we identify a nontransitive evolutionary sequence in a 1000-generation yeast evolution experiment. We show that nontransitivity arises due to adaptation in the yeast nuclear genome combined with the stepwise deterioration of an intracellular virus, which provides an advantage over viral competitors within host cells. Extending our analysis, we find that nearly half of our ~140 populations experience multilevel selection, fixing adaptive mutations in both the nuclear and viral genomes. Our results provide a mechanistic case-study for the adaptive evolution of nontransitivity due to multilevel selection in a 1000-generation host/virus evolution experiment.
Highlights
Adaptive evolution is a process in which selective events result in the replacement of less-fit genotypes with a more fit ones
The Intermediate clone was isolated following a selective sweep that fixes three nuclear mutations including a beneficial mutation in YUR1
The Late clone was isolated following three more selective sweeps that fix an additional 10 nuclear mutations including a beneficial mutation in STE4
Summary
Adaptive evolution is a process in which selective events result in the replacement of less-fit genotypes with a more fit ones. What is unknown is whether nontransitive interactions arise for direct descendants along a line of genealogical succession This is the crux of Gould’s paradox and has broad implications for our understanding of evolutionary processes. When Buskirk et al pitted these yeast against their distant ancestors, the new generation were destroyed by the toxins the older generation produced These findings provide the first experimental evidence for nontransitivity along a line of descent. By expanding our study of host-virus genome evolution to over 100 additional yeast populations, we find that multilevel selection, and the potential for the evolution of nontransitive interactions, is a common occurrence given the conditions of our evolution experiment
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