Multicellularity makes somatic differentiation evolutionarily stable
Mary E. Wahl a,b,1 and Andrew W. Murray a,b,2
aDepartment of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138;
bFAS Center for Systems Biology, Harvard University, Cambridge, MA 02138
Contributed by Andrew W. Murray, June 15, 2016 (sent for review September 13, 2015; reviewed by Harmit S. Malik and Boris I. Shraiman)
Unicellular species lack the nonreproductive somatic cell types that characterize complex multicellular organisms. We consider two alternative explanations: first, that the costs of lost reproductive potential never exceed the benefits of somatic cells in unicellular organisms; and second, that somatic cells may profit a unicellular population but leave it vulnerable to invasion by common mutants. We test these hypotheses using engineered yeast strains that permit direct comparisons of fitness and evolutionary stability between lifestyles. We find that the benefits of somatic cell production can exceed the costs in unicellular strains. Multicellular, soma-producing strains resist invasion by nondifferentiating mutants that overtake unicellular populations, supporting the theory that somatic differentiation is stabilized by population structure imposed by multicellularity.
Many multicellular organisms produce two cell lineages: germ cells, whose descendants produce the next generation, and somatic cells, which support, protect, and disperse the germ cells. This germ-soma demarcation has evolved independently in dozens of multicellular taxa but is absent in unicellular species. A common explanation holds that in these organisms, inefficient intercellular nutrient exchange compels the fitness cost of producing nonreproductive somatic cells to outweigh any potential benefits. We propose instead that the absence of unicellular, soma-producing populations reflects their susceptibility to invasion by nondifferentiating mutants that ultimately eradicate the soma-producing lineage. We argue that multicellularity can prevent the victory of such mutants by giving germ cells preferential access to the benefits conferred by somatic cells. The absence of natural unicellular, soma-producing species previously prevented these hypotheses from being directly tested in vivo: to overcome this obstacle, we engineered strains of the budding yeast Saccharomyces cerevisiae that differ only in the presence or absence of multicellularity and somatic differentiation, permitting direct comparisons between organisms with different lifestyles. Our strains implement the essential features of irreversible conversion from germ line to soma, reproductive division of labor, and clonal multicellularity while maintaining sufficient generality to permit broad extension of our conclusions. Our somatic cells can provide fitness benefits that exceed the reproductive costs of their production, even in unicellular strains. We find that nondifferentiating mutants overtake unicellular populations but are outcompeted by multicellular, soma-producing strains, suggesting that multicellularity confers evolutionary stability to somatic differentiation.
evolution multicellularity differentiation synthetic biology yeast
1Present address: Microsoft New England Research and Development Center, Cambridge, MA 02142.
2To whom correspondence should be addressed. Email: firstname.lastname@example.org.
This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2014.
Author contributions: M.E.W. and A.W.M. designed research; M.E.W. performed research; M.E.W. analyzed data; and M.E.W. and A.W.M. wrote the paper.
Reviewers: H.S.M., Fred Hutchinson Cancer Research Center; and B.I.S., University of California, Santa Barbara.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1608278113/-/DCSupplemental.
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