Abstract
The evolution of multicellular life requires cooperation among cells, which can be undermined by intra-group selection for selfishness. Theory predicts that selection to avoid non-cooperators limits social interactions among non-relatives, yet previous evolution experiments suggest that intra-group conflict is an outcome, rather than a driver, of incipient multicellular life cycles. Here we report the evolution of multicellularity via two distinct mechanisms of group formation in the unicellular budding yeast Kluyveromyces lactis. Cells remain permanently attached following mitosis, giving rise to clonal clusters (staying together); clusters then reversibly assemble into social groups (coming together). Coming together amplifies the benefits of multicellularity and allows social clusters to collectively outperform solitary clusters. However, cooperation among non-relatives also permits fast-growing unicellular lineages to ‘free-ride’ during selection for increased size. Cooperation and competition for the benefits of multicellularity promote the stable coexistence of unicellular and multicellular genotypes, underscoring the importance of social and ecological context during the transition to multicellularity.
Highlights
The evolution of multicellular life requires cooperation among cells, which can be undermined by intra-group selection for selfishness
We present evidence that multicellularity in K. lactis involves an interaction between two distinct mechanisms of group formation, providing an explanation for instances of divergence with S. cerevisiae
We observed evolution in populations derived from the unicellular dairy yeast K. lactis maintained under conditions previously shown to favour the evolution of multicellularity in S. cerevisiae[24]
Summary
The evolution of multicellular life requires cooperation among cells, which can be undermined by intra-group selection for selfishness. The origin and maintenance of cooperation among formerly free-living unicells is often viewed as a barrier for the evolution of complex multicellular life[1,9,10] This major evolutionary transition has occurred several times in disparate lineages, showing that solutions to evolving cooperation have evolved multiple times[11]. Evolutionary models suggest that cooperation depends on high relatedness among cells within a multicellular group; genetic diversity promotes competition, which favours selfish lineages that benefit from cooperation without reciprocating (cheaters[12]). All of the largest and most complex multicellular organisms rely on ST following cellular mitosis[22] This striking disparity is widely viewed as a reflection of the divergent opportunities for intra-group genetic conflict: ST results in clonal groups, whereas groups formed by CT may harbour multiple lineages, including cheaters. Systematic comparisons among these disparate outcomes remain difficult due to major differences in the features of unicellular ancestors and experimental conditions, including selection for multicellularity
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