Kin Discrimination Increases with Genetic Distance in a Social Amoeba

Ostrowski, Elizabeth A.; Katoh, Masahiko; Shaulsky, Gad; Queller, David C.; Strassmann, Joan E.

doi:10.1371/journal.pbio.0060287

Cited by 139 publications

(191 citation statements)

References 36 publications

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“…During the evolution of multicellularity, a degree of unrelatedness-and therefore conflict-had to be overcome, perhaps by recognition or via some other mechanism [30][31][32][33]. We show that a sufficient degree of structured growth may be sufficient to achieve this, despite the mobility of amoebae that tends to mix cells.…”

Section: Discussionmentioning

confidence: 87%

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum

et al. 2012

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One condition for the evolution of altruism is genetic relatedness between altruist and beneficiary, often achieved through active kin recognition. Here, we investigate the power of a passive process resulting from genetic drift during population growth in the social amoeba Dictyostelium discoideum. We put labelled and unlabelled cells of the same clone in the centre of a plate, and allowed them to proliferate outward. Zones formed by genetic drift owing to the small population of actively growing cells at the colony edge. We also found that single cells could form zones of high relatedness. Relatedness increased at a significantly higher rate when food was in short supply. This study shows that relatedness can be significantly elevated before the social stage without a small founding population size or recognition mechanism.

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Section: Discussionmentioning

confidence: 87%

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum

et al. 2012

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“…A couple of studies found some evidence for sorting, particularly between clones collected far apart (58) or, in another study, particularly between clones found close together (59). Neither approached the levels of sorting found in another species, Dictylostelium purpureum (60).…”

Section: Control Of Cheatingmentioning

confidence: 99%

Evolution of cooperation and control of cheating in a social microbe

Strassmann

Queller

2011

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

194

200

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Much of what we know about the evolution of altruism comes from animals. Here, we show that studying a microbe has yielded unique insights, particularly in understanding how social cheaters are controlled. The social stage of Dictylostelium discoideum occurs when the amoebae run out of their bacterial prey and aggregate into a multicellular, motile slug. This slug forms a fruiting body in which about a fifth of cells die to form a stalk that supports the remaining cells as they form hardy dispersal-ready spores. Because this social stage forms from aggregation, it is analogous to a social group, or a chimeric multicellular organism, and is vulnerable to internal conflict. Advances in cell labeling, microscopy, single-gene knockouts, and genomics, as well as the results of decades of study of D. discoideum as a model for development, allow us to explore the genetic basis of social contests and control of cheaters in unprecedented detail. Cheaters are limited from exploiting other clones by high relatedness, kin discrimination, pleiotropy, noble resistance, and lottery-like role assignment. The active nature of these limits is reflected in the elevated rates of change in social genes compared with nonsocial genes. Despite control of cheaters, some conflict is still expressed in chimeras, with slower movement of slugs, slightly decreased investment in stalk compared with spore cells, and differential contributions to stalk and spores. D. discoideum is rapidly becoming a model system of choice for molecular studies of social evolution.kin selection | kin recognition | multicellularity | major transitions

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“…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)(6)(7)(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.…”

mentioning

confidence: 99%

Experimental evolution of multicellularity

Ratcliff

Denison²,

Borrello³

et al. 2012

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

473

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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Kin Discrimination Increases with Genetic Distance in a Social Amoeba

Cited by 139 publications

References 36 publications

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum

Evolution of cooperation and control of cheating in a social microbe

Experimental evolution of multicellularity

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