Cheats as first propagules: A new hypothesis for the evolution of individuality during the transition from single cells to multicellularity

Rainey, Paul B.; Kerr, Benjamin

doi:10.1002/bies.201000039

Cited by 104 publications

(112 citation statements)

References 66 publications

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“…The evolution of multicellularity requires an increasing role for natural selection among multicellular individuals, relative to selection among cells within individuals (1,3,15,17,27,28). We investigated the transition between unicellular and multicellular life by studying two emergent traits of multicellular snowflake-phenotype yeast, cluster reproduction, and settling survival.…”

Section: Resultsmentioning

confidence: 99%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

470

619

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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.T he evolution of multicellularity was transformative for life on earth (1). In addition to larger size, multicellularity increased biological complexity through the formation of new biological structures. For example, multicellular organisms have evolved sophisticated, higher-level functionality via cooperation among component cells with complementary behaviors (2, 3). However, dissolution and death of multicellular individuals occurs when cooperation breaks down, cancer being a prime example (4). There are multiple mechanisms to help ensure cooperation of component cells in most extant multicellular species (5-8), but the origin and the maintenance of multicellularity are two distinct evolutionary problems. Component cells in a nascent multicellular organism would appear to have frequent opportunities to pursue noncooperative reproductive strategies at a cost to the reproduction of the multicellular individual. How, then, does the transition to multicellularity occur?Understanding the evolution of complex multicellular individuals from unicellular ancestors has been extremely challenging, largely because the first steps in this process occurred in the deep past (>200 million years ago) (9, 10). As a result, transitional forms have been lost to extinction, and little is known about the physiology, ecology, and evolutionary processes of incipient multicellularity (11). Nonetheless, several key steps have been identified for this transition. Because multicellular organisms are composed of multiple cells, the first step in this transition was likely the evolution of genotypes that form simple cellular clusters (1, 3, 12-16). It is not known whether this occurs more readily through aggregation of genetically distinct cells, as in biofilms, or by mother-daughter cell adhesion after division. Once simple clusters have evolved, selection among multicelled clusters must predominate over selection among single cells within clusters (1,15,17,18). T...

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Section: Resultsmentioning

confidence: 99%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

470

619

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“…Group formation offers distinct advantages over a strictly solitary lifestyle such as protection from predation [31,32], access to new niches [4], and survival in harsh environments [33]. However, for groups to qualify as units of selection, they must also possess the capacity to beget group offspring [27,34,35]. In this experimental yeast system, clusters grew in size and as a result of cell death or physical strain they fragmented and thereby reproduced.…”

Section: Discussionmentioning

confidence: 99%

Geometry shapes evolution of early multicellularity

Libby

Ratcliff

Travisano

et al. 2014

Preprint

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Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units in which reproduction is the sole responsibility of a subset of units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular ''snowflake-like'' cluster formed in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.

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“…In order for an ETI to occur, either a demographic mechanism that ensures high relatedness (such as group formation by single propagules; Rainey and Kerr 2010) or a behavioral mechanism that ensures high behavioral responsiveness (such as strong prosocial preferences or policing) is needed to eliminate within-group selection. Once within-group selection is eliminated, extended between-group selection can drive a population toward a convergence-stable outcome with social behaviors that maximize group fitness.…”

Section: The Scope For Group Optimalitymentioning

confidence: 99%

Behavioral Responses in Structured Populations Pave the Way to Group Optimality

Akçay

Cleve

2012

The American Naturalist

185

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An unresolved controversy regarding social behaviors is exemplified when natural selection might lead to behaviors that maximize fitness at the social-group level but are costly at the individual level. Except for the special case of groups of clones, we do not have a general understanding of how and when group-optimal behaviors evolve, especially when the behaviors in question are flexible. To address this question, we develop a general model that integrates behavioral plasticity in social interactions with the action of natural selection in structured populations. We find that group-optimal behaviors can evolve, even without clonal groups, if individuals exhibit appropriate behavioral responses to each other's actions. The evolution of such behavioral responses, in turn, is predicated on the nature of the proximate behavioral mechanisms. We model a particular class of proximate mechanisms, prosocial preferences, and find that such preferences evolve to sustain maximum group benefit under certain levels of relatedness and certain ecological conditions. Thus, our model demonstrates the fundamental interplay between behavioral responses and relatedness in determining the course of social evolution. We also highlight the crucial role of proximate mechanisms such as prosocial preferences in the evolution of behavioral responses and in facilitating evolutionary transitions in individuality. Disciplines Behavior and Ethology | Biology | Population Biology CommentsAt the time of publication, author Erol Akçay was affiliated with the University of Tennessee. Currently, he is a faculty member at the Department of Biology at the University of Pennsylvania. Online enhancement: appendix.abstract: An unresolved controversy regarding social behaviors is exemplified when natural selection might lead to behaviors that maximize fitness at the social-group level but are costly at the individual level. Except for the special case of groups of clones, we do not have a general understanding of how and when group-optimal behaviors evolve, especially when the behaviors in question are flexible. To address this question, we develop a general model that integrates behavioral plasticity in social interactions with the action of natural selection in structured populations. We find that group-optimal behaviors can evolve, even without clonal groups, if individuals exhibit appropriate behavioral responses to each other's actions. The evolution of such behavioral responses, in turn, is predicated on the nature of the proximate behavioral mechanisms. We model a particular class of proximate mechanisms, prosocial preferences, and find that such preferences evolve to sustain maximum group benefit under certain levels of relatedness and certain ecological conditions. Thus, our model demonstrates the fundamental interplay between behavioral responses and relatedness in determining the course of social evolution. We also highlight the crucial role of proximate mechanisms such as prosocial preferences in the evolution of behavioral respons...

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Cheats as first propagules: A new hypothesis for the evolution of individuality during the transition from single cells to multicellularity

Cited by 104 publications

References 66 publications

Experimental evolution of multicellularity

Experimental evolution of multicellularity

Geometry shapes evolution of early multicellularity

Behavioral Responses in Structured Populations Pave the Way to Group Optimality

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