Your PDF has successfully downloaded.

You may be interested in finding more content on these topics:


You are not currently logged in.

Access JSTOR through your library or other institution:


Log in through your institution.

How an Organism Dies Affects the Fitness of Its Neighbors

Pierre M. Durand, Armin Rashidi and Richard E. Michod
The American Naturalist
Vol. 177, No. 2 (February 2011), pp. 224-232
DOI: 10.1086/657686
Stable URL:
Page Count: 9
  • Download PDF
  • Add to My Lists
  • Cite this Item
We're having trouble loading this content. Download PDF instead.


AbstractProgrammed cell death (PCD), a genetically regulated cell suicide program, is ubiquitous in the living world. In contrast to multicellular organisms, in which cells cooperate for the good of the organism, in unicells the cell is the organism and PCD presents a fundamental evolutionary problem. Why should an organism actively kill itself as opposed to dying in a nonprogrammed way? Proposed arguments vary from PCD in unicells being maladaptive to the assumption that it is an extreme form of altruism. To test whether PCD could be beneficial to nearby cells, we induced programmed and nonprogrammed death in the unicellular green alga Chlamydomonas reinhardtii. Cellular contents liberated during non-PCD are detrimental to others, while the contents released during PCD are beneficial. The number of cells in growing cultures was used to measure fitness. Thermostability studies revealed that the beneficial effect of the PCD supernatant most likely involves simple heat-stable biomolecules. Non-PCD supernatant contains heat-sensitive molecules like cellular proteases and chlorophyll. These data indicate that the mode of death affects the origin and maintenance of PCD. The way in which an organism dies can have beneficial or deleterious effects on the fitness of its neighbors.

Notes and References

This item contains 26 references.

Literature Cited
  • ['Ackermann, M., B. Stecher, N. E. Freed, P. Songhet, W.-D. Hardt, and M. Doebeli. 2008. Self-destructive cooperation mediated by phenotypic noise. Nature 454:987–990.']
  • ['Ameisen, J. C. 2002. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death and Differentiation 9:367–393.']
  • ['Baroli, I., B. L. Gutman, H. K. Ledford, J. W. Shin, B. L. Chin, M. Havaux, and K. K. Niyogi. 2004. Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. Journal of Biological Chemistry 279:6337–6344.']
  • ['Bell, G. 1990. The ecology and genetics of fitness in Chlamydomonas. I. Genotype-by-environment interaction among pure strains. Proceedings of the Royal Society B: Biological Sciences 240:295–321.']
  • ['Fabrizio, P., L. Battistella, R. Vardavas, C. Gattazzo, L.-L. Liou, A. Diaspro, J. W. Dossen, E. B. Gralla, and V. D. Longo. 2004. Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. Journal of Cell Biology 166:1055–1067.']
  • ['Gardner, A., and R. Kümmerli. 2008. Social evolution: this microbe will self-destruct. Current Biology 18:1021–1023.']
  • ['Gorman, D. S., and R. P. Levine. 1965. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proceedings of the National Academy of Sciences of the USA 54:1665–1669.']
  • ['Greig, D., and M. Travisano. 2004. The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Proceedings of the Royal Society B: Biological Sciences 271:S25–S26.']
  • ['Hamilton, W. D. 1964a. The genetical evolution of social behaviour. I. Journal of Theoretical Biology 7:1–16.']
  • ['———. 1964b. The genetical evolution of social behaviour. II. Journal of Theoretical Biology 7:17–52.']
  • ['Herker, E., H. Jungwirth, K. A. Lehmann, C. Maldener, K.-U. Fröhlich, S. Wissing, S. Büttner, M. Fehr, S. Sigrist, and F. Madeo. 2004. Chronological aging leads to apoptosis in yeast. Journal of Cell Biology 164:501–507.']
  • ['Herron, M. D., and R. E. Michod. 2008. Evolution of complexity in the volvocine algae: transitions in individuality through Darwin’s eye. Evolution 62:436–445.']
  • ['Herron, M. D., J. D. Hackett, F. O. Aylward, and R. E. Michod. 2009. Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences of the USA 106:3254–3258.']
  • ['Jiménez, C., J. M. Capasso, C. L. Edelstein, C. J. Rivard, S. Lucia, S. Breusegem, T. Berl, and M. Segovia. 2009. Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. Journal of Experimental Botany 60:815–828.']
  • ['Leadsham, J. E., and C. W. Gourlay. 2008. Cytoskeletal induced apoptosis in yeast. Biochimica et Biophysica Acta 1783:1406–1412.']
  • ['Longo, V. D., J. Mitteldorf, and V. P. Skulachev. 2005. Programmed and altruistic ageing. Nature Reviews Genetics 6:866–872.']
  • ['Michod, R. E. 1980. Evolution of interactions in family-structured populations: mixed mating models. Genetics 96:275–296.']
  • ['———. 2007. Evolution of individuality during the transition from unicellular to multicellular life. Proceedings of the National Academy of Sciences of the USA 104:S8613–S8618.']
  • ['Moharikar, S., J. S. D’Souza, A. B. Kulkarni, and B. J. Rao. 2006. Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (Chlorophyceae) cells following UV irradiation: detection and functional analyses. Journal of Phycology 42:423–433.']
  • ['Nedelcu, A. M. 2005. Sex as a response to oxidative stress: stress genes co-opted for sex. Proceedings of the Royal Society B: Biological Sciences 272:1935–1940.']
  • ['———. 2006. Evidence for p53-like-mediated stress responses in green algae. FEBS Letters 580:3013–3017.']
  • ['Nedelcu, A. M., W. W. Driscoll, P. M. Durand, M. D. Herron, and A. Rashidi. 2010. On the paradigm of altruistic suicide in the unicellular world. Evolution, doi:10.1111/j.1558-5646.2010.01103.x.']
  • ['Queller, D. C. 2000. Relatedness and the fraternal major transitions. Philosophical Transactions of the Royal Society B: Biological Sciences 355:1647–1655.']
  • ['Washo-Stultz, D., C. Crowley, C. M. Payne, C. Bernstein, S. Marek, E. W. Gerner, and H. Bernstein. 2000. Increased susceptibility of cells to inducible apoptosis during growth from early to late log phase: an important caveat for in vitro apoptosis research. Toxicology Letters 116:199–207.']
  • ['Weis, E. 1982. Influence of light on the heat sensitivity of the photosynthetic apparatus in isolated spinach chloroplasts. Plant Physiology 70:1530–1534.']
  • ['Zhang, Y., C. Liu, S. Liu, Y. Shen, T. Kuang, and C. Yang. 2008. Structural stability and properties of three isoforms of the major light-harvesting chlorophyll a/b complexes of photosystem II. Biochimica et Biophysica Acta 1777:479–487.']