Trends in Genetics
ReviewThe cooperative amoeba: Dictyostelium as a model for social evolution
Section snippets
The evolution of social cooperation
Cooperation is common in nature. In social insects such as ants and bees, sterile or semi-sterile workers collectively rear eggs laid by the queen, and in mammals wolves hunt in packs, cooperatively trapping prey to secure their meal [1]. In these and other similar cases, social cooperation between individuals can be mutually beneficial and result in gains in fitness. The origins and maintenance of sociality, however, has long been recognized as presenting some difficulties for evolutionary
Dictyostelium as a model system for the study of social evolution
One of the best-studied examples of microbial sociality is in Dictyostelium discoideum, a soil amoeba principally distributed in eastern North America, Japan, and the east coast of China [9]. This species has been a key model system for understanding the genetic basis of social cooperation as well as development and cell–cell signaling [10]. The 34 Mb genome of D. discoideum has been completely sequenced and carefully annotated. In addition, several molecular approaches are available to dissect
Molecular mechanisms of social cooperation
The onset of the social fruiting-body phase leads to a major shift in developmental gene expression, which is followed by morphological change and cell fate determination (Figure 1). During the early mound stage, prestalk and prespore cells initially differentiate and sort into different positions; the former move more effectively in response to the cAMP signal, and exhibit differential cell adhesion, thereby progressing to the top of the mound [17]. Continued elongation of the mound leads to
Altruism and kin discrimination in Dictyostelium
The development of the multicellular fruiting body in D. discoideum is accompanied by the appearance of altruism as a key component of social cooperation. Approximately 20% of the cells that aggregate to form the fruiting body form the stalk cells, and these altruistically die to ensure the survival of the 80% of the cells that make up the spore-bearing sorus. In general, programmed cell death in multicellular systems is commonplace, but the case of Dictyostelium has a unique feature – the
The invasion of cheaters
One aspect of social cooperation is that it sets the stage for the evolution of cheaters – individuals that take advantage of the system to increase their own fitness but without contributing to the maintenance of cooperative behavior. In fruiting-body formation in D. discoideum, cheating genotypes are those that preferentially form spore cells at the expense of becoming the altruistic stalk cells that perish during fruiting-body development.
Cheating behavior could have diverse mechanisms and
The enigmatic sexual phase
Compared to the intensively studied asexual fruiting-body phase, much less is known about sex in D. discoideum. The sexual cycle in this species, which also has a social dimension, involves (i) sexual maturation of solitary amoebae, (ii) cell and nuclear fusion between cells of distinct mating types, (iii) aggregation of other solitary cells and cannibalization by the developing zygote, (iv) maturation of the macrocyst (a cellulose-coated zygotic structure [10]), and (v) germination of progeny
Concluding remarks: the genomics era and beyond
In the past decades D. discoideum has emerged as a pre-eminent genetic model system for social evolution (Table 1). Using several different approaches it has been possible to study in this microbial species the genetic basis of social cooperation and altruism, and to begin to identify mechanisms associated with the origin and maintenance of sociality. The use of D. discoideum as a model system has been reinforced by the development of several genomic resources that will facilitate future
Acknowledgments
We thank Joan Strassmann, Ulises Rosas and Jeanmaire Molina for constructive comments on the manuscript. Gareth Bloomfield is also thanked for insights into cannibalism during macrocyst formation.
Glossary
- Altruism
- a behavior that benefits the recipient(s) at the cost of the direct fitness of the actor. A clear example of altruism in D. discoideum is provided by the cells which sacrifice themselves in the stalk of fruiting bodies to increase the reproductive success of other coaggregate cells.
- Cheater
- an individual who gains benefit from social cooperation but without contributing proportionally to the collective production of the social trait. During fruiting-body formation, cheaters in D.
References (65)
- et al.
Sociomicrobiology: the connections between quorum sensing and biofilms
Trends Microbiol.
(2005) Dictyostelium mutants lacking DIF, a putative morphogen
Cell
(1983)- et al.
Initial cell type divergence in Dictyostelium is independent of DIF-1
Dev. Biol.
(1996) - et al.
The role of DIF-1 signaling in Dictyostelium development
Mol. Cell
(2000) Receptor-dependent and tyrosine phosphatase-mediated inhibition of GSK3 regulates cell fate choice
Dev. Cell
(2002)- et al.
Differential distribution of cAMP receptors cAR2 and cAR3 during Dictyostelium development
Dev. Biol.
(1996) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium
Curr. Biol.
(2009)Cells at the center of Dictyostelium aggregates become spores
Dev. Biol.
(1997)Dictyostelium discoideum: cell-type proportioning, cell-differentiation preference, cell fate, and the behavior of anterior-like cells in Hs1/Hs2 and G+/G- mixtures
Differentiation
(1986)- et al.
Cell-fate choice in Dictyostelium: intrinsic biases modulate sensitivity to DIF signaling
Dev. Biol.
(2000)
Quantification of social behavior in D. discoideum reveals complex fixed and facultative strategies
Curr. Biol.
The cold war of the social amoebae
Curr. Biol.
Genes involved in Dictyostelium discoideum sexual reproduction
Eur. J. Cell. Biol.
Altruism in insect societies and beyond: voluntary or enforced?
Trends Ecol. Evol.
The autoinhibitor of cell fusion in Dictyostelium inhibits calmodulin
Biochem. Biophys. Res. Commun.
The genetical evolution of social behavior, I & II
J. Theor. Biol.
Cooperation and competition in pathogenic bacteria
Nature
Communication in bacteria: an ecological and evolutionary perspective
Nat. Rev. Microbiol.
The sociobiology of biofilms
FEMS Microbiol. Rev.
Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus
Nature
Sociobiology of the myxobacteria
Annu. Rev. Microbiol.
Global distribution of forest soil dictyostelids
J. Biogeogr.
Dictyostelium – Evolution, Cell Biology, and The Development of Multicellularity
The genome of the social amoeba Dictyostelium discoideum
Nature
Insights into morphogenesis from a simple developmental system
Nat. Rev. Mol. Cell Biol.
Exploiting new terrain: an advantage to sociality in the slime mold Dictyostelium discoideum
Behav. Ecol.
How cellular slime molds evade nematodes
Proc. Natl. Acad. Sci. U. S. A.
Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum
Mol. Ecol.
The costs and benefits of being a chimera
Proc. Biol. Sci.
Three-dimensional in vivo analysis of Dictyostelium mounds reveals directional sorting of prestalk cells and defines a role for the myosin II regulatory light chain in prestalk cell sorting and tip protrusion
Development
Transcriptional regulation of Dictyostelium pattern formation
EMBO Rep.
Cited by (55)
Evolving social behavior through selection of single-cell adhesion in Dictyostelium discoideum
2022, iScienceCitation Excerpt :In this case, according to a common distinction, ‘cooperator’ and ‘cheater’ types compete within groups and can disrupt their collective functions. The ‘social amoeba’ Dictyostelium discoideum, whose life cycle comprises a multicellular body formed by aggregation of formerly independent cells, is an established model system to address the role of genetic conflicts on the evolution of multicellular organization (Strassmann et al., 2000; Li and Purugganan, 2011). Chimeric aggregates, where cells of different strains develop together and differentiate into several tissues, readily occur both in nature and in the lab (Fortunato et al., 2003b; Gilbert et al., 2007; Sathe et al., 2010; Castillo et al., 2011).
Secreted heme peroxidase from Dictyostelium discoideum: Insights into catalysis, structure, and biological role
2018, Journal of Biological ChemistryCitation Excerpt :In its natural habitat, D. discoideum is able to engulf, kill, and digest microorganisms at a rate of at least one/min (2). Upon starvation, it undergoes a program of multicellular development, leading to differentiation into fruiting bodies containing persistent spores (4, 5). Both the single-celled amoebae and the multicellular aggregates have developed antibacterial defense mechanisms that exhibit many parallels to mammalian innate immune responses, including phagocytosis by many types of white blood cells.
Cooperation induces other cooperation: Fruiting bodies promote the evolution of macrocysts in Dictyostelium discoideum
2017, Journal of Theoretical BiologyCitation Excerpt :Although D. discoideum normally lives as a free-living cell, it also exhibits two dormant phases during starvation; the fruiting body and the macrocyst. These two phases are considered cooperative; nonviable stalk cells facilitate the dispersal of spore cells in fruiting bodies (Li and Purugganan, 2011; smith et al., 2014), whereas vegetative cells are cannibalized to provide energy to zygotes during macrocyst formation (Urushihara and Muramoto, 2006). In fruiting body formation, tens of thousands of cells are attracted by cyclic AMP (cAMP) (Tyson and Murray, 1989).
Group Maintenance in Aggregative Multicellularity
2022, The Evolution of Multicellularity