High Relatedness Is Necessary and Sufficient to Maintain Multicellularity in Dictyostelium
Abstract
Most complex multicellular organisms develop clonally from a single cell. This should limit conflicts between cell lineages that could threaten the extensive cooperation of cells within multicellular bodies. Cellular composition can be manipulated in the social amoeba Dictyostelium discoideum, which allows us to test and confirm the two key predictions of this theory. Experimental evolution at low relatedness favored cheating mutants that could destroy multicellular development. However, under high relatedness, the forces of mutation and within-individual selection are too small for these destructive cheaters to spread, as shown by a mutation accumulation experiment. Thus, we conclude that the single-cell bottleneck is a powerful stabilizer of cellular cooperation in multicellular organisms.
Get full access to this article
View all available purchase options and get full access to this article.
Already a Subscriber?Sign In
Supplementary Material
File (1213272-kuzdzal-fick.som.pdf)
References and Notes
1
L. W. Buss, The Evolution of Individuality (Princeton Univ. Press, Princeton, NJ, 1987).
2
J. Maynard Smith, E. Szathmáry, The Major Transitions in Evolution (Freeman, San Francisco, 1995).
3
J. Maynard Smith, in Evolutionary Progress, M. H. Nitecki, Ed. (Univ. of Chicago Press, Chicago, 1989), pp. 219–230.
4
Queller D. C., Relatedness and the fraternal major transitions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1647 (2000).
5
Grosberg R. K., Strathmann R. R., The evolution of multicellularity: A minor major transition? Annu. Rev. Ecol. Evol. Syst. 38, 621 (2007).
6
A. F. G. Bourke, Principles of Social Evolution (Oxford Univ. Press, Oxford, 2011), pp. 288.
7
L. Keller, Ed., Levels of Selection in Evolution (Princeton Univ. Press, Princeton, NJ, 1999).
8
Hughes W. O., Oldroyd B. P., Beekman M., Ratnieks F. L., Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213 (2008).
9
Michod R. E., Roze D., Transitions in individuality. Proc. Biol. Sci. 264, 853 (1997).
10
Michod R. E., Cooperation and conflict in the evolution of individuality. II. Conflict mediation. Proc. Biol. Sci. 263, 813 (1996).
11
Michod R. E., Cooperation and conflict in the evolution of individuality. I. Multilevel selection of the organism. Am. Nat. 149, 607 (1997).
12
Ennis H. L., Dao D. N., Pukatzki S. U., Kessin R. H., Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc. Natl. Acad. Sci. U.S.A. 97, 3292 (2000).
13
Santorelli L. A., et al., Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107 (2008).
14
R. H. Kessin, Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity (Cambridge Univ. Press, Cambridge, 2001).
15
J. T. Bonner, The Cellular Slime Molds (Princeton Univ. Press, Princeton, NJ, 1967).
16
Buss L. W., Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sci. U.S.A. 79, 5337 (1982).
17
Strassmann J. E., Zhu Y., Queller D. C., Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408, 965 (2000).
18
Travisano M., Velicer G. J., Strategies of microbial cheater control. Trends Microbiol. 12, 72 (2004).
19
Materials and methods are available as supporting material on Science Online.
20
Grafen A., A geometric view of relatedness. Oxford Surv. Evol. Biol. 2, 28 (1985).
21
Lynch M., et al., Perspective: Spontaneous deleterious mutation. Evolution 53, 645 (1999).
22
Gilbert O. M., Foster K. R., Mehdiabadi N. J., Strassmann J. E., Queller D. C., High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl. Acad. Sci. U.S.A. 104, 8913 (2007).
23
Le Gac M., Doebeli M., Environmental viscosity does not affect the evolution of cooperation during experimental evolution of colicigenic bacteria. Evolution 64, 522 (2010).
24
Brockhurst M. A., Population bottlenecks promote cooperation in bacterial biofilms. PLoS ONE 2, e634 (2007).
25
Chen G., Kuspa A., Prespore cell fate bias in G1 phase of the cell cycle in Dictyostelium discoideum. Eukaryot. Cell 4, 1755 (2005).
26
Ostrowski E. A., Katoh M., Shaulsky G., Queller D. C., Strassmann J. E., Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6, e287 (2008).
27
Hirose S., Benabentos R., Ho H. I., Kuspa A., Shaulsky G., Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333, 467 (2011).
28
Ratnieks F. L., Foster K. R., Wenseleers T., Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581 (2006).
29
Bonner J. T., Frascella E. B., Variations in cell size during the development of the slime mold, Dictyostelium discoideum. Biol. Bull. 104, 297 (1953).
30
Sussman M., Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol. 28, 9 (1987).
31
Saxer G., Brock D. A., Queller D. C., Strassmann J. E., Cheating does not explain selective differences at high and low relatedness in a social amoeba. BMC Evol. Biol. 10, 76 (2010).
32
Kuzdzal-Fick J. J., Queller D. C., Strassmann J. E., An invitation to die: Initiators of sociality in a social amoeba become selfish spores. Biol. Lett. 6, (suppl.), 800 (2010).
33
Brock D. A., Gomer R. H., A cell-counting factor regulating structure size in Dictyostelium. Genes Dev. 13, 1960 (1999).
34
M. Sussman, in Methods in Cell Physiology, D. Prescott, Ed. (Academic Press, New York, 1966), vol. 2, pp. 397–410.
35
Mehdiabadi N. J., et al., Social evolution: Kin preference in a social microbe. Nature 442, 881 (2006).
36
J. H. McDonald, Handbook of Biological Statistics (Sparky House Publishing, Baltimore, ed. 2, 2009).
Information & Authors
Information
Published In

Science
Volume 334 | Issue 6062
16 December 2011
16 December 2011
Copyright
Copyright © 2011, American Association for the Advancement of Science.
Submission history
Received: 29 August 2011
Accepted: 4 November 2011
Published in print: 16 December 2011
Acknowledgments
Supported by the NSF grants DEB-0918931 and DEB-0816690. J.J.K. and S.A.F. were supported partly by Wray-Todd Graduate Fellowships. We thank J. Potter and A. Smith for laboratory work, G. Saxer for advice, and C. Kuzdzal Fick for advice and for comments on the manuscript. Data are available in the supporting online material.
Authors
Metrics & Citations
Metrics
Article Usage
Altmetrics
Citations
Export citation
Select the format you want to export the citation of this publication.
Cited by
- Bacterial Quorum Sensing and Metabolic Incentives to Cooperate, Science, 338, 6104, (264-266), (2021)./doi/10.1126/science.1227289
Loading...
View Options
Get Access
Log in to view the full text
AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.
- Become a AAAS Member
- Activate your AAAS ID
- Purchase Access to Other Journals in the Science Family
- Account Help
Log in via OpenAthens.
Log in via Shibboleth.
More options
Register for free to read this article
As a service to the community, this article is available for free. Login or register for free to read this article.
Buy a single issue of Science for just $15 USD.
View options
PDF format
Download this article as a PDF file
Download PDF





