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      Experimental evolution of an alternating uni- and multicellular life cycle in Chlamydomonas reinhardtii

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          Abstract

          The transition to multicellularity enabled the evolution of large, complex organisms, but early steps in this transition remain poorly understood. Here we show that multicellular complexity, including development from a single cell, can evolve rapidly in a unicellular organism that has never had a multicellular ancestor. We subject the alga Chlamydomonas reinhardtii to conditions that favour multicellularity, resulting in the evolution of a multicellular life cycle in which clusters reproduce via motile unicellular propagules. While a single-cell genetic bottleneck during ontogeny is widely regarded as an adaptation to limit among-cell conflict, its appearance very early in this transition suggests that it did not evolve for this purpose. Instead, we find that unicellular propagules are adaptive even in the absence of intercellular conflict, maximizing cluster-level fecundity. These results demonstrate that the unicellular bottleneck, a trait essential for evolving multicellular complexity, can arise rapidly via co-option of the ancestral unicellular form.

          Abstract

          The early steps in the evolution of multicellularity are poorly understood. Here, Ratcliff et al. show that multicellularity can rapidly evolve in the green alga Chlamydomonas reinhardtii, demonstrating that single-cell developmental bottlenecks may evolve rapidly via co-option of the ancestral phenotype.

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          Most cited references30

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          Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli.

          The role of historical contingency in evolution has been much debated, but rarely tested. Twelve initially identical populations of Escherichia coli were founded in 1988 to investigate this issue. They have since evolved in a glucose-limited medium that also contains citrate, which E. coli cannot use as a carbon source under oxic conditions. No population evolved the capacity to exploit citrate for >30,000 generations, although each population tested billions of mutations. A citrate-using (Cit+) variant finally evolved in one population by 31,500 generations, causing an increase in population size and diversity. The long-delayed and unique evolution of this function might indicate the involvement of some extremely rare mutation. Alternately, it may involve an ordinary mutation, but one whose physical occurrence or phenotypic expression is contingent on prior mutations in that population. We tested these hypotheses in experiments that "replayed" evolution from different points in that population's history. We observed no Cit+ mutants among 8.4 x 10(12) ancestral cells, nor among 9 x 10(12) cells from 60 clones sampled in the first 15,000 generations. However, we observed a significantly greater tendency for later clones to evolve Cit+, indicating that some potentiating mutation arose by 20,000 generations. This potentiating change increased the mutation rate to Cit+ but did not cause generalized hypermutability. Thus, the evolution of this phenotype was contingent on the particular history of that population. More generally, we suggest that historical contingency is especially important when it facilitates the evolution of key innovations that are not easily evolved by gradual, cumulative selection.
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            Repeatability and contingency in the evolution of a key innovation in phage lambda.

            The processes responsible for the evolution of key innovations, whereby lineages acquire qualitatively new functions that expand their ecological opportunities, remain poorly understood. We examined how a virus, bacteriophage λ, evolved to infect its host, Escherichia coli, through a novel pathway. Natural selection promoted the fixation of mutations in the virus's host-recognition protein, J, that improved fitness on the original receptor, LamB, and set the stage for other mutations that allowed infection through a new receptor, OmpF. These viral mutations arose after the host evolved reduced expression of LamB, whereas certain other host mutations prevented the phage from evolving the new function. This study shows the complex interplay between genomic processes and ecological conditions that favor the emergence of evolutionary innovations.
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              Experimental evolution of multicellularity.

              Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                06 November 2013
                : 4
                : 2742
                Affiliations
                [1 ]School of Biology, Georgia Institute of Technology , Atlanta, Georgia 30332-0230, USA
                [2 ]Ecology, Evolution and Behavior, University of Minnesota , Minneapolis, Minnesota 55108, USA
                [3 ]The BioTechnology Institute, University of Minnesota , Minneapolis, Minnesota 55108, USA
                [4 ]Division of Biological Sciences, The University of Montana , Missoula, Montana 59812, USA
                Author notes
                Article
                ncomms3742
                10.1038/ncomms3742
                3831279
                24193369
                2a5ae63a-9f64-41c7-98b1-41f98c61c833
                Copyright © 2013, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/

                History
                : 30 May 2013
                : 09 October 2013
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