Browse by volumes Browse by section
Browse issues Volume 1 (2021) article no. e58
Social conflicts in Dictyostelium discoideum : a matter of scales
Forget, Mathieu1, 2 ; Adiba, Sandrine2 ; De Monte, Silvia1, 2
1 Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Plön, Germany
2 Institut de Biologie de l'Ecole Normale Supérieure, Département de Biologie, Ecole Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, France
10.24072/pcjournal.39 - Peer Community Journal, Volume 1 (2021), article no. e58.
Get full text PDF Peer reviewed and recommended by PCI
The social amoeba Dictyostelium discoideum, where aggregation of genetically heterogeneous cells produces functional collective structures, epitomizes social conflicts associated with multicellular organization. 'Cheater' populations that have a higher chance - quantified by a positive spore bias - of surviving to the next generation when mixed with cooperators bear a selective advantage. Their spread is thus expected to undermine collective functions over evolutionary times. In this review, we discuss the two main approaches adopted to conceptualize social conflicts in Dictyostelium discoideum: describing social interactions as a property of cell populations (strains), or as a result of individual cell choices during the developmental process. These two points of view are often held equivalent and used interchangeably. While the population-level view grants more direct evolutionary inference, however, the cell-level interpretation reveals that such evolutionary predictions may be modified if mechanisms such as dependence on the environment, development and intrinsic unpredictability of cell fate choices are taken into account. We conclude by proposing a set of open questions that in our opinion lie at the core of a multi-scale description of aggregative life cycles, where the formulation of predictive evolutionary models would include cell-level mechanisms responsible for spore bias alongside population-level descriptors of multicellular organization.
Peer-Reviews
DOI: 10.24072/pcjournal.39
Author's affiliations:
Forget, Mathieu 1, 2; Adiba, Sandrine 2; De Monte, Silvia 1, 2
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_39,
author = {Forget, Mathieu and Adiba, Sandrine and De Monte, Silvia},
title = {Social conflicts in {\protect\emph{Dictyostelium} discoideum} : a matter of scales},
journal = {Peer Community Journal},
eid = {e58},
publisher = {Peer Community In},
doi = {10.24072/pcjournal.39},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.39/}
AU  - Forget, Mathieu
AU  - Adiba, Sandrine
AU  - De Monte, Silvia
TI  - Social conflicts in Dictyostelium discoideum : a matter of scales
JO  - Peer Community Journal
DA  - 2021///
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.39/
UR  - https://doi.org/10.24072/pcjournal.39
DO  - 10.24072/pcjournal.39
ID  - 10_24072_pcjournal_39
%0 Journal Article
%A Forget, Mathieu
%A Adiba, Sandrine
%A De Monte, Silvia
%T Social conflicts in Dictyostelium discoideum : a matter of scales
%J Peer Community Journal
%V 1
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.39
%R 10.24072/pcjournal.39
%F 10_24072_pcjournal_39
Forget, Mathieu; Adiba, Sandrine; De Monte, Silvia. Social conflicts in Dictyostelium discoideum : a matter of scales. Peer Community Journal, Volume 1 (2021), article  no. e58. doi : 10.24072/pcjournal.39. https://peercommunityjournal.org/articles/10.24072/pcjournal.39/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100122
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Ackermann, M. A functional perspective on phenotypic heterogeneity in microorganisms, Nature Reviews Microbiology, Volume 13 (2015) no. 8, pp. 497-508 | DOI
[2] Aerts, R. J.; Durston, A. J.; Moolenaar, W. H. Cytoplasmic pH and the regulation of the dictyostelium cell cycle, Cell, Volume 43 (1985) no. 3, pp. 653-657 | DOI
[3] Aktipis, C. A.; Boddy, A. M.; Jansen, G.; Hibner, U.; Hochberg, M. E.; Maley, C. C.; Wilkinson, G. S. Cancer across the tree of life: cooperation and cheating in multicellularity, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 370 (2015) no. 1673 | DOI
[4] d'Alessandro, J.; Mas, L.; Aubry, L.; Rieu, J.-P.; Rivière, C.; Anjard, C. Collective regulation of cell motility using an accurate density-sensing system, Journal of The Royal Society Interface, Volume 15 (2018) no. 140 | DOI
[5] Altschuler, S. J.; Wu, L. F. Cellular Heterogeneity: Do Differences Make a Difference?, Cell, Volume 141 (2010) no. 4, pp. 559-563 | DOI
[6] Antolović, V.; Lenn, T.; Miermont, A.; Chubb, J. R. Transition state dynamics during a stochastic fate choice, Development, Volume 146 (2019) no. 12 | DOI
[7] Antolović, V.; Miermont, A.; Corrigan, A. M.; Chubb, J. R. Generation of Single-Cell Transcript Variability by Repression, Current Biology, Volume 27 (2017) no. 12 | DOI
[8] Araki, T.; Maeda, Y. Cell-cycle progression during the development of Dictyostelium discoideum and its relation to the subsequent cell-sorting in the multicellular structures, Development, Growth and Differentiation, Volume 37 (1995) no. 5, pp. 479-485 | DOI
[9] Arias Del Angel, J. A.; Nanjundiah, V.; Benítez, M.; Newman, S. A. Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity, EvoDevo, Volume 11 (2020) no. 1 | DOI
[10] Azhar, M.; Kennady, P.; Pande, G.; Espiritu, M.; Holloman, W.; Brazill, D.; Gomer, R. H.; Nanjundiah, V. Cell cycle phase, cellular Ca2+ and development in Dictyostelium discoideum, International Journal of Developmental Biology, Volume 45 (2002) no. 2, pp. 405-414
[11] Azhar, M.; Kennady, P.; Pande, G.; Nanjundiah, V. Stimulation by DIF Causes an Increase of Intracellular Ca2+inDictyostelium discoideum, Experimental Cell Research, Volume 230 (1997) no. 2, pp. 403-406 | DOI
[12] Azhar, M.; Manogaran, P.; Kennady, P.; Pande, G.; Nanjundiah, V. A Ca2+-Dependent Early Functional Heterogeneity in Amoebae ofDictyostelium discoideum,Revealed by Flow Cytometry, Experimental Cell Research, Volume 227 (1996) no. 2, pp. 344-351 | DOI
[13] Balázsi, G.; van Oudenaarden, A.; Collins, J. J. Cellular Decision Making and Biological Noise: From Microbes to Mammals, Cell, Volume 144 (2011) no. 6, pp. 910-925 | DOI
[14] Beatrici, C. P.; Brunnet, L. G. Cell sorting based on motility differences, Physical Review E, Volume 84 (2011) no. 3 | DOI
[15] Benabentos, R.; Hirose, S.; Sucgang, R.; Curk, T.; Katoh, M.; Ostrowski, E. A.; Strassmann, J. E.; Queller, D. C.; Zupan, B.; Shaulsky, G.; Kuspa, A. Polymorphic Members of the lag Gene Family Mediate Kin Discrimination in Dictyostelium, Current Biology, Volume 19 (2009) no. 7, pp. 567-572 | DOI
[16] Bonner, J. T. A Theory of the Control of Differentiation in the Cellular Slime Molds, The Quarterly Review of Biology, Volume 32 (1957) no. 3, pp. 232-246 | DOI
[17] Bonner, J. T.; Clarke, W. W.; Neely, C. L.; Slifkin, M. K. The orientation to light and the extermely sensitive orientation to temperature gradients in the slime mold Dictyostelium discoideum, Journal of Cellular and Comparative Physiology, Volume 36 (1950) no. 2, pp. 149-158 | DOI
[18] Brown, J. M.; Firtel, R. A. Regulation of Cell-Fate Determination in Dictyostelium, Developmental Biology, Volume 216 (1999) no. 2, pp. 426-441 | DOI
[19] Buss, L. W. Somatic cell parasitism and the evolution of somatic tissue compatibility., Proceedings of the National Academy of Sciences, Volume 79 (1982) no. 17, pp. 5337-5341 | DOI
[20] Buttery, N. J.; Rozen, D. E.; Wolf, J. B.; Thompson, C. R. Quantification of Social Behavior in D. discoideum Reveals Complex Fixed and Facultative Strategies, Current Biology, Volume 19 (2009) no. 16, pp. 1373-1377 | DOI
[21] Buttery, N. J.; Thompson, C. R. L.; Wolf, J. B. Complex genotype interactions influence social fitness during the developmental phase of the social amoeba Dictyostelium discoideum, Journal of Evolutionary Biology, Volume 23 (2010) no. 8, pp. 1664-1671 | DOI
[22] Chattwood, A.; Nagayama, K.; Bolourani, P.; Harkin, L.; Kamjoo, M.; Weeks, G.; Thompson, C. R. Developmental lineage priming in Dictyostelium by heterogeneous Ras activation, eLife, Volume 2 (2013) | DOI
[23] Chattwood, A.; Thompson, C. R. L. Non-genetic heterogeneity and cell fate choice in Dictyostelium discoideum, Development, Growth & Differentiation, Volume 53 (2011) no. 4, pp. 558-566 | DOI
[24] Chuang, J. S.; Rivoire, O.; Leibler, S. Simpson's Paradox in a Synthetic Microbial System, Science, Volume 323 (2009) no. 5911, pp. 272-275 | DOI
[25] Clarke, M.; Baron, A. Myosin filaments in cytoskeletons ofDictyostelium amoebae, Cell Motility and the Cytoskeleton, Volume 7 (1987) no. 4, pp. 293-303 | DOI
[26] Colizzi, E. S.; Vroomans, R. M.; Merks, R. M. Evolution of multicellularity by collective integration of spatial information, eLife, Volume 9 (2020) | DOI
[27] Corrigan, A. M.; Chubb, J. R. Regulation of Transcriptional Bursting by a Naturally Oscillating Signal, Current Biology, Volume 24 (2014) no. 2, pp. 205-211 | DOI
[28] Dawkins, R. The selfish gene, Oxford University Press, 1976, 224 pages
[29] De Monte, S.; Rainey, P. B. Nascent multicellular life and the emergence of individuality, Journal of Biosciences, Volume 39 (2014), pp. 237-248 | DOI
[30] Devreotes, P. N.; Zigmond, S. H. Chemotaxis in Eukaryotic Cells: A Focus on Leukocytes and Dictyostelium, Annual Review of Cell Biology, Volume 4 (1988) no. 1, pp. 649-686 | DOI
[31] Doebeli, M.; Hauert, C.; Killingback, T. The Evolutionary Origin of Cooperators and Defectors, Science, Volume 306 (2004) no. 5697, pp. 859-862 | DOI
[32] Doulcier, G.; Lambert, A.; De Monte, S.; Rainey, P. B. Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity, eLife, Volume 9 (2020) | DOI
[33] Draghi, J. Links between evolutionary processes and phenotypic robustness in microbes, Seminars in Cell & Developmental Biology, Volume 88 (2019), pp. 46-53 | DOI
[34] Du, Q.; Kawabe, Y.; Schilde, C.; Chen, Z.-h.; Schaap, P. The Evolution of Aggregative Multicellularity and Cell–Cell Communication in the Dictyostelia, Journal of Molecular Biology, Volume 427 (2015) no. 23, pp. 3722-3733 | DOI
[35] Dubravcic, D.; van Baalen, M.; Nizak, C. An evolutionarily significant unicellular strategy in response to starvation in Dictyostelium social amoebae, F1000Research, Volume 3 (2014) | DOI
[36] Early, A.; Gaskell, M.; Traynor, D.; Williams, J. Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination, Trends in Genetics, Volume 9 (1993) no. 10 | DOI
[37] 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, Proceedings of the National Academy of Sciences, Volume 97 (2000) no. 7, pp. 3292-3297 | DOI
[38] Fisher, P. R.; Merkl, R.; Gerisch, G. Quantitative analysis of cell motility and chemotaxis in Dictyostelium discoideum by using an image processing system and a novel chemotaxis chamber providing stationary chemical gradients., Journal of Cell Biology, Volume 108 (1989) no. 3, pp. 973-984 | DOI
[39] Flowers, J. M.; Li, S. I.; Stathos, A.; Saxer, G.; Ostrowski, E. A.; Queller, D. C.; Strassmann, J. E.; Purugganan, M. D. Variation, Sex, and Social Cooperation: Molecular Population Genetics of the Social Amoeba Dictyostelium discoideum, PLoS Genetics, Volume 6 (2010) no. 7 | DOI
[40] Fortunato, A.; Queller, D. C.; Strassmann, J. E. A linear dominance hierarchy among clones in chimeras of the social amoebaDictyostelium discoideum, Journal of Evolutionary Biology, Volume 16 (2003) no. 3, pp. 438-445 | DOI
[41] Fortunato, A.; Strassmann, J. E.; Santorelli, L.; Queller, D. C. Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum, Molecular Ecology, Volume 12 (2003) no. 4, pp. 1031-1038 | DOI
[42] Fujimori, T.; Nakajima, A.; Shimada, N.; Sawai, S. Tissue self-organization based on collective cell migration by contact activation of locomotion and chemotaxis, Proceedings of the National Academy of Sciences, Volume 116 (2019) no. 10, pp. 4291-4296 | DOI
[43] Garcia, T.; Brunnet, L. G.; De Monte, S. Differential Adhesion between Moving Particles as a Mechanism for the Evolution of Social Groups, PLoS Computational Biology, Volume 10 (2014) no. 2 | DOI
[44] Garcia, T.; Doulcier, G.; De Monte, S. The evolution of adhesiveness as a social adaptation, eLife, Volume 4 (2015) | DOI
[45] Gardner, A.; West, S. A. Inclusive fitness: 50 years on, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 369 (2014) no. 1642 | DOI
[46] van Gestel, J.; Nowak, M. A. Phenotypic Heterogeneity and the Evolution of Bacterial Life Cycles, PLOS Computational Biology, Volume 12 (2016) no. 2 | DOI
[47] van Gestel, J.; Tarnita, C. E. On the origin of biological construction, with a focus on multicellularity, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 42, pp. 11018-11026 | DOI
[48] 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, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 21, pp. 8913-8917 | DOI
[49] Glöckner, G.; Lawal, H. M.; Felder, M.; Singh, R.; Singer, G.; Weijer, C. J.; Schaap, P. The multicellularity genes of dictyostelid social amoebas, Nature Communications, Volume 7 (2016) no. 1 | DOI
[50] Godfrey-Smith, P. Darwinian Populations and Natural Selection, Oxford University Press, Oxford, New York, 2009 | DOI
[51] Gokhale, C. S.; Traulsen, A. Evolutionary Multiplayer Games, Dynamic Games and Applications, Volume 4 (2014) no. 4, pp. 468-488 | DOI
[52] Gomer, R. H.; Ammann, R. R. A Cell-Cycle Phase-Associated Cell-Type Choice Mechanism Monitors the Cell Cycle Rather Than Using an Independent Timer, Developmental Biology, Volume 174 (1996) no. 1, pp. 82-91 | DOI
[53] Goury-Sistla, P.; Nanjundiah, V.; Pande, G. Bimodal distribution of motility and cell fate in Dictyostelium discoideum, The International Journal of Developmental Biology, Volume 56 (2012) no. 4, pp. 263-272 | DOI
[54] Gregor, T.; Fujimoto, K.; Masaki, N.; Sawai, S. The Onset of Collective Behavior in Social Amoebae, Science, Volume 328 (2010) no. 5981, pp. 1021-1025 | DOI
[55] Grimbergen, A. J.; Siebring, J.; Solopova, A.; Kuipers, O. P. Microbial bet-hedging: the power of being different, Current Opinion in Microbiology, Volume 25 (2015), pp. 67-72 | DOI
[56] Grosberg, R. K.; Strathmann, R. R. The Evolution of Multicellularity: A Minor Major Transition?, Annual Review of Ecology, Evolution, and Systematics, Volume 38 (2007) no. 1, pp. 621-654 | DOI
[57] Gruenheit, N.; Parkinson, K.; Brimson, C. A.; Kuwana, S.; Johnson, E. J.; Nagayama, K.; Llewellyn, J.; Salvidge, W. M.; Stewart, B.; Keller, T.; van Zon, W.; Cotter, S. L.; Thompson, C. R. Cell Cycle Heterogeneity Can Generate Robust Cell Type Proportioning, Developmental Cell, Volume 47 (2018) no. 4 | DOI
[58] Gruenheit, N.; Parkinson, K.; Stewart, B.; Howie, J. A.; Wolf, J. B.; Thompson, C. R. L. A polychromatic 'greenbeard' locus determines patterns of cooperation in a social amoeba, Nature Communications, Volume 8 (2017) no. 1, pp. 1-9 | DOI
[59] Guttal, V.; Couzin, I. D. Social interactions, information use, and the evolution of collective migration, Proceedings of the National Academy of Sciences, Volume 107 (2010) no. 37, pp. 16172-16177 | DOI
[60] Hamilton, W. The genetical evolution of social behaviour. I, Journal of Theoretical Biology, Volume 7 (1964) no. 1, pp. 1-16 | DOI
[61] Hardin, G. The Tragedy of the Commons, Science, Volume 162 (1968) no. 3859, pp. 1243-1248 | DOI
[62] Hauert, C.; De Monte, S.; Hofbauer, J.; Sigmund, K. Volunteering as Red Queen Mechanism for Cooperation in Public Goods Games, Science, Volume 296 (2002) no. 5570, pp. 1129-1132 | DOI
[63] Hauert, C.; De Monte, S.; Hofbauer, J.; Sigmund, K. Replicator Dynamics for Optional Public Good Games, Journal of Theoretical Biology, Volume 218 (2002) no. 2, pp. 187-194 | DOI
[64] Hiraoka, H.; Nakano, T.; Kuwana, S.; Fukuzawa, M.; Hirano, Y.; Ueda, M.; Haraguchi, T.; Hiraoka, Y. Intracellular ATP levels influence cell fates in Dictyostelium discoideum differentiation, Genes to Cells, Volume 25 (2020) no. 5, pp. 312-326 | DOI
[65] Hochberg, M. E.; Rankin, D. J.; Taborsky, M. The coevolution of cooperation and dispersal in social groups and its implications for the emergence of multicellularity, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | DOI
[66] Hofbauer, J.; Sigmund, K. Evolutionary Games and Population Dynamics, Cambridge University Press, 1998 | DOI
[67] Houle, J.; Balthazar, J.; West, C. M. A glycosylation mutation affects cell fate in chimeras of Dictyostelium discoideum., Proceedings of the National Academy of Sciences, Volume 86 (1989) no. 10, pp. 3679-3683 | DOI
[68] Huang, H.-J.; Takagawa, D.; Weeks, G.; Pears, C. Cells at the Center ofDictyosteliumAggregates Become Spores, Developmental Biology, Volume 192 (1997) no. 2, pp. 564-571 | DOI
[69] Hudson, R. E.; Aukema, J. E.; Rispe, C.; Roze, D. Altruism, Cheating, and Anticheater Adaptations in Cellular Slime Molds, The American Naturalist, Volume 160 (2002) no. 1, pp. 31-43 | DOI
[70] Jang, W.; Gomer, R. H. Initial Cell Type Choice in Dictyostelium, Eukaryotic Cell, Volume 10 (2011) no. 2, pp. 150-155 | DOI
[71] Joshi, J.; Couzin, I. D.; Levin, S. A.; Guttal, V. Mobility can promote the evolution of cooperation via emergent self-assortment dynamics, PLOS Computational Biology, Volume 13 (2017) no. 9 | DOI
[72] Kaushik, S.; Katoch, B.; Nanjundiah, V. Social behaviour in genetically heterogeneous groups of Dictyostelium giganteum, Behavioral Ecology and Sociobiology, Volume 59 (2006) no. 4, pp. 521-530 | DOI
[73] Kay, R. R.; Dhokia, B.; Jermyn, K. A. Purification of stalk-cell-inducing morphogens from Dictyostelium discoideum, European Journal of Biochemistry, Volume 136 (1983) no. 1, pp. 51-56 | DOI
[74] Kerr, W. E. Evolution of the Mechanism of Caste Determination in the Genus melipona, Evolution, Volume 4 (1950) no. 1 | DOI
[75] Kerr, B.; Godfrey-Smith, P. GENERALIZATION OF THE PRICE EQUATION FOR EVOLUTIONARY CHANGE, Evolution, Volume 63 (2009) no. 2, pp. 531-536 | DOI
[76] Kessin, R. H. Dictyostelium, Cambridge University Press, 2001 | DOI
[77] Kubohara, Y.; Arai, A.; Gokan, N.; Hosaka, K. Pharmacological evidence that stalk cell differentiation involves increases in the intracellular Ca2+ and H+ concentrations in Dictyostelium discoideum, Development, Growth & Differentiation, Volume 49 (2007) no. 3, pp. 253-264 | DOI
[78] Kubohara, Y.; Okamoto, K. Cytoplasmic Ca2+ and H+ concentrations determine cell fate in Dictyostelium discoideum, The FASEB Journal, Volume 8 (1994) no. 11, pp. 869-874 | DOI
[79] Kussell, E.; Leibler, S. Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments, Science, Volume 309 (2005) no. 5743, pp. 2075-2078 | DOI
[80] Kuzdzal-Fick, J. J.; Fox, S. A.; Strassmann, J. E.; Queller, D. C. High Relatedness Is Necessary and Sufficient to Maintain Multicellularity in Dictyostelium, Science, Volume 334 (2011) no. 6062, pp. 1548-1551 | DOI
[81] Kuzdzal-Fick, J. J.; Queller, D. C.; Strassmann, J. E. An invitation to die: initiators of sociality in a social amoeba become selfish spores, Biology Letters, Volume 6 (2010) no. 6, pp. 800-802 | DOI
[82] Ladoux, B.; Mège, R.-M. Mechanobiology of collective cell behaviours, Nature Reviews Molecular Cell Biology, Volume 18 (2017) no. 12, pp. 743-757 | DOI
[83] Leach, C. K.; Ashworth, J. M.; Garrod, D. R. Cell sorting out during the differentiation of mixtures of metabolically distinct populations of Dictyostelium discoideum, Development, Volume 29 (1973) no. 3, pp. 647-661 | DOI
[84] Liautaud, K.; van Nes, E. H.; Barbier, M.; Scheffer, M.; Loreau, M. Superorganisms or loose collections of species? A unifying theory of community patterns along environmental gradients, Ecology Letters, Volume 22 (2019), pp. 1243-1252 | DOI
[85] Lion, S. Theoretical Approaches in Evolutionary Ecology: Environmental Feedback as a Unifying Perspective, The American Naturalist, Volume 191 (2018) no. 1, pp. 21-44 | DOI
[86] Loomis, W. F. Cell signaling during development of Dictyostelium, Developmental Biology, Volume 391 (2014) no. 1, pp. 1-16 | DOI
[87] Madgwick, P. G.; Stewart, B.; Belcher, L. J.; Thompson, C. R. L.; Wolf, J. B. Strategic investment explains patterns of cooperation and cheating in a microbe, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 21 | DOI
[88] Maeda, Y. A New Method for Inducing Synchronous Growth of Dictyostelium discoideum Cells Using Temperature Shifts, Microbiology, Volume 132 (1986) no. 5, pp. 1189-1196 | DOI
[89] Maeda, Y. Cell-cycle checkpoint for transition from cell division to differentiation, Development, Growth & Differentiation, Volume 53 (2011) no. 4, pp. 463-481 | DOI
[90] Maree, A. F. M.; Hogeweg, P. How amoeboids self-organize into a fruiting body: Multicellular coordination in Dictyostelium discoideum, Proceedings of the National Academy of Sciences, Volume 98 (2001) no. 7, pp. 3879-3883 | DOI
[91] Martínez-García, R.; Tarnita, C. E. Lack of Ecological and Life History Context Can Create the Illusion of Social Interactions in Dictyostelium discoideum, PLOS Computational Biology, Volume 12 (2016) no. 12 | DOI
[92] Matsuda, H.; Harada, Y. Evolutionarily stable stalk to spore ratio in cellular slime molds and the law of equalization in net incomes, Journal of Theoretical Biology, Volume 147 (1990) no. 3, pp. 329-344 | DOI
[93] Medina, J. M.; Shreenidhi, P.; Larsen, T. J.; Queller, D. C.; Strassmann, J. E. Cooperation and conflict in the social amoeba Dictyostelium discoideum, The International Journal of Developmental Biology, Volume 63 (2019) no. 8-9-10, pp. 371-382 | DOI
[94] Michod, R. E. Evolution of individuality during the transition from unicellular to multicellular life, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. Supplement 1, pp. 8613-8618 | DOI
[95] Miele, L.; De Monte, S. Aggregative cycles evolve as a solution to conflicts in social investment, PLOS Computational Biology, Volume 17 (2021) no. 1 | DOI
[96] Muramoto, T.; Chubb, J. R. Live imaging of theDictyosteliumcell cycle reveals widespread S phase during development, a G2 bias in spore differentiation and a premitotic checkpoint, Development, Volume 135 (2008) no. 9, pp. 1647-1657 | DOI
[97] Nanjundiah, V. Many roads lead to Rome: Neutral phenotypes in microorganisms, Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Volume 332 (2019) no. 8, pp. 339-348 | DOI
[98] Nichols, J. M.; Antolović, V.; Reich, J. D.; Brameyer, S.; Paschke, P.; Chubb, J. R. Cell and molecular transitions during efficient dedifferentiation, eLife, Volume 9 (2020) | DOI
[99] Noh, S.; Christopher, L.; Strassmann, J. E.; Queller, D. C. Wild Dictyostelium discoideum social amoebae show plastic responses to the presence of nonrelatives during multicellular development, Ecology and Evolution, Volume 10 (2020) no. 3, pp. 1119-1134 | DOI
[100] Noh, S.; Geist, K. S.; Tian, X.; Strassmann, J. E.; Queller, D. C. Genetic signatures of microbial altruism and cheating in social amoebas in the wild, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 12, pp. 3096-3101 | DOI
[101] Norman, T. M.; Lord, N. D.; Paulsson, J.; Losick, R. Stochastic Switching of Cell Fate in Microbes, Annual Review of Microbiology, Volume 69 (2015) no. 1, pp. 381-403 | DOI
[102] Nowak, M. A. Five Rules for the Evolution of Cooperation, Science, Volume 314 (2006) no. 5805, pp. 1560-1563 | DOI
[103] Ohmori, T.; Maeda, Y. The developmental fate of dictyostelium discoideum cells depends greatly on the cell-cycle position at the onset of starvation, Cell Differentiation, Volume 22 (1987) no. 1, pp. 11-18 | DOI
[104] Okasha, S. Evolution and the Levels of Selection, Oxford University Press, 2006 | DOI
[105] de Oliveira, J. L.; Morales, A. C.; Stewart, B.; Gruenheit, N.; Engelmoer, J.; Brown, S. B.; de Brito, R. A.; Hurst, L. D.; Urrutia, A. O.; Thompson, C. R. L.; Wolf, J. B. Conditional expression explains molecular evolution of social genes in a microbe, Nature Communications, Volume 10 (2019) no. 1 | DOI
[106] Ostrowski, E. A. Enforcing Cooperation in the Social Amoebae, Current Biology, Volume 29 (2019) no. 11 | DOI
[107] Ostrowski, E. A.; Katoh, M.; Shaulsky, G.; Queller, D. C.; Strassmann, J. E. Kin Discrimination Increases with Genetic Distance in a Social Amoeba, PLoS Biology, Volume 6 (2008) no. 11 | DOI
[108] Ostrowski, E. A.; Shen, Y.; Tian, X.; Sucgang, R.; Jiang, H.; Qu, J.; Katoh-Kurasawa, M.; Brock, D. A.; Dinh, C.; Lara-Garduno, F.; Lee, S. L.; Kovar, C. L.; Dinh, H. H.; Korchina, V.; Jackson, L.; Patil, S.; Han, Y.; Chaboub, L.; Shaulsky, G.; Muzny, D. M.; Worley, K. C.; Gibbs, R. A.; Richards, S.; Kuspa, A.; Strassmann, J. E.; Queller, D. C. Genomic Signatures of Cooperation and Conflict in the Social Amoeba, Current Biology, Volume 25 (2015) no. 12, pp. 1661-1665 | DOI
[109] Parfrey, L. W.; Lahr, D. J. G. Multicellularity arose several times in the evolution of eukaryotes (Response to DOI 10.1002/bies.201100187), BioEssays, Volume 35 (2013) no. 4, pp. 339-347 | DOI
[110] Parkinson, K.; Buttery, N. J.; Wolf, J. B.; Thompson, C. R. L. A Simple Mechanism for Complex Social Behavior, PLoS Biology, Volume 9 (2011) no. 3 | DOI
[111] Peña, J.; Lehmann, L.; Nöldeke, G. Gains from switching and evolutionary stability in multi-player matrix games, Journal of Theoretical Biology, Volume 346 (2014), pp. 23-33 | DOI
[112] Peña, J.; Nöldeke, G.; Lehmann, L. Evolutionary dynamics of collective action in spatially structured populations, Journal of Theoretical Biology, Volume 382 (2015), pp. 122-136 | DOI
[113] Perkins, T. J.; Swain, P. S. Strategies for cellular decision‐making, Molecular Systems Biology, Volume 5 (2009) no. 1 | DOI
[114] Queller, D. C. Genetic relatedness in viscous populations, Evolutionary Ecology, Volume 8 (1994) no. 1, pp. 70-73 | DOI
[115] Rainey, P. B. Precarious development: The uncertain social life of cellular slime molds, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 9, pp. 2639-2640 | DOI
[116] Rainey, P. B.; De Monte, S. Resolving Conflicts During the Evolutionary Transition to Multicellular Life, Annual Review of Ecology, Evolution, and Systematics, Volume 45 (2014) no. 1, pp. 599-620 | DOI
[117] Rainey, P. B.; Kerr, B. Cheats as first propagules: A new hypothesis for the evolution of individuality during the transition from single cells to multicellularity, BioEssays, Volume 32 (2010) no. 10, pp. 872-880 | DOI
[118] Raper, K. Pseudoplasmodium formation and organization in Dictyostelium discoideum, Journal of the Elisha Mitchell Scientific Society, Volume 56 (1940) no. 2, pp. 241-282
[119] Rossine, F. W.; Martinez-Garcia, R.; Sgro, A. E.; Gregor, T.; Tarnita, C. E. Eco-evolutionary significance of "loners", PLOS Biology, Volume 18 (2020) no. 3 | DOI
[120] Sathe, S.; Kaushik, S.; Lalremruata, A.; Aggarwal, R. K.; Cavender, J. C.; Nanjundiah, V. Genetic Heterogeneity in Wild Isolates of Cellular Slime Mold Social Groups, Microbial Ecology, Volume 60 (2010) no. 1, pp. 137-148 | DOI
[121] Sathe, S.; Nanjundiah, V. Complex interactions underpin social behaviour in Dictyostelium giganteum, Behavioral Ecology and Sociobiology, Volume 72 (2018) no. 10 | DOI
[122] 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 Evolutionary Biology, Volume 10 (2010) no. 1 | DOI
[123] Schreiber, F.; Ackermann, M. Environmental drivers of metabolic heterogeneity in clonal microbial populations, Current Opinion in Biotechnology, Volume 62 (2020), pp. 202-211 | DOI
[124] Segota, I.; Boulet, L.; Franck, D.; Franck, C. Spontaneous emergence of large-scale cell cycle synchronization in amoeba colonies, Physical Biology, Volume 11 (2014) no. 3 | DOI
[125] Sgro, A. E.; Schwab, D. J.; Noorbakhsh, J.; Mestler, T.; Mehta, P.; Gregor, T. From intracellular signaling to population oscillations: bridging size‐ and time‐scales in collective behavior, Molecular Systems Biology, Volume 11 (2015) no. 1 | DOI
[126] Smith, J.; Queller, D. C.; Strassmann, J. E. Fruiting bodies of the social amoeba Dictyostelium discoideum increase spore transport by Drosophila, BMC Evolutionary Biology, Volume 14 (2014) no. 1 | DOI
[127] Soll, D. R.; Waddell, D. R. Morphogenesis in the slime mold Dictyostelium discoideum, Developmental Biology, Volume 47 (1975) no. 2, pp. 292-302 | DOI
[128] Staps, M.; van Gestel, J.; Tarnita, C. E. Emergence of diverse life cycles and life histories at the origin of multicellularity, Nature Ecology & Evolution, Volume 3 (2019) no. 8, pp. 1197-1205 | DOI
[129] Steinberg, M. S. Differential adhesion in morphogenesis: a modern view, Current Opinion in Genetics & Development, Volume 17 (2007) no. 4, pp. 281-286 | DOI
[130] Strandkvist, C.; Juul, J.; Baum, B.; Kabla, A. J.; Duke, T. A kinetic mechanism for cell sorting based on local variations in cell motility, Interface Focus, Volume 4 (2014) no. 6 | DOI
[131] Strassmann, J. E.; Queller, D. C. Evolution of cooperation and control of cheating in a social microbe, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. Supplement_2, pp. 10855-10862 | DOI
[132] Strassmann, J. E.; Zhu, Y.; Queller, D. C. Altruism and social cheating in the social amoeba Dictyostelium discoideum, Nature, Volume 408 (2000) no. 6815, pp. 965-967 | DOI
[133] Sucgang, R.; Kuo, A.; Tian, X.; Salerno, W.; Parikh, A.; Feasley, C. L.; Dalin, E.; Tu, H.; Huang, E.; Barry, K.; Lindquist, E.; Shapiro, H.; Bruce, D.; Schmutz, J.; Salamov, A.; Fey, P.; Gaudet, P.; Anjard, C.; Babu, M. M.; Basu, S.; Bushmanova, Y.; van der Wel, H.; Katoh-Kurasawa, M.; Dinh, C.; Coutinho, P. M.; Saito, T.; Elias, M.; Schaap, P.; Kay, R. R.; Henrissat, B.; Eichinger, L.; Rivero, F.; Putnam, N. H.; West, C. M.; Loomis, W. F.; Chisholm, R. L.; Shaulsky, G.; Strassmann, J. E.; Queller, D. C.; Kuspa, A.; Grigoriev, I. V. Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum, Genome Biology, Volume 12 (2011) no. 2 | DOI
[134] Takeuchi, I.; Noce, T.; Tasaka, M. Chapter 17 Prestalk and Prespore Differentiation During Development of Dictyosteuum Discoideum, Current Topics in Developmental Biology, Elsevier, 1986, pp. 243-256 | DOI
[135] Tarnita, C. E. Fast evolution unlocks forbidden communities, Nature Ecology & Evolution, Volume 2 (2018) no. 10, pp. 1525-1526 | DOI
[136] Tarnita, C. E.; Washburne, A.; Martinez-Garcia, R.; Sgro, A. E.; Levin, S. A. Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 9, pp. 2776-2781 | DOI
[137] Thompson, C. R.; Kay, R. R. Cell-Fate Choice in Dictyostelium: Intrinsic Biases Modulate Sensitivity to DIF Signaling, Developmental Biology, Volume 227 (2000) no. 1, pp. 56-64 | DOI
[138] Thompson, C. R.; Kay, R. R. The Role of DIF-1 Signaling in Dictyostelium Development, Molecular Cell, Volume 6 (2000) no. 6, pp. 1509-1514 | DOI
[139] Tilman, A. R.; Plotkin, J. B.; Akçay, E. Evolutionary games with environmental feedbacks, Nature Communications, Volume 11 (2020) no. 1 | DOI
[140] Uchinomiya, K.; Iwasa, Y. Evolution of stalk/spore ratio in a social amoeba: Cell-to-cell interaction via a signaling chemical shaped by cheating risk, Journal of Theoretical Biology, Volume 336 (2013), pp. 110-118 | DOI
[141] Umeda, T.; Inouye, K. Cell sorting by differential cell motility: a model for pattern formation in Dictyostelium, Journal of Theoretical Biology, Volume 226 (2004) no. 2, pp. 215-224 | DOI
[142] van Boxtel, C.; van Heerden, J. H.; Nordholt, N.; Schmidt, P.; Bruggeman, F. J. Taking chances and making mistakes: non-genetic phenotypic heterogeneity and its consequences for surviving in dynamic environments, Journal of The Royal Society Interface, Volume 14 (2017) no. 132 | DOI
[143] Van Cleve, J. Stags, Hawks, and Doves: Social Evolution Theory and Individual Variation in Cooperation, Integrative and Comparative Biology, Volume 57 (2017) no. 3, pp. 566-579 | DOI
[144] Van Duijn, B.; Inouye, K. Regulation of movement speed by intracellular pH during Dictyostelium discoideum chemotaxis., Proceedings of the National Academy of Sciences, Volume 88 (1991) no. 11, pp. 4951-4955 | DOI
[145] Velicer, G. J.; Kroos, L.; Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus, Nature, Volume 404 (2000) no. 6778, pp. 598-601 | DOI
[146] Vidal-Henriquez, E.; Gholami, A. Spontaneous center formation in Dictyostelium discoideum, Scientific Reports, Volume 9 (2019) no. 1 | DOI
[147] Walmod, P.; Hartmann-Petersen, R.; Prag, S.; Lepekhin, E.; Röpke, C.; Berezin, V.; Bock, E. Cell-cycle-dependent regulation of cell motility and determination of the role of Rac1, Experimental Cell Research, Volume 295 (2004) no. 2, pp. 407-420 | DOI
[148] Wang, M.; Aerts, R. J.; Spek, W.; Schaap, P. Cell cycle phase in Dictyostelium discoideum is correlated with the expression of cyclic AMP production, detection, and degradation, Developmental Biology, Volume 125 (1988) no. 2, pp. 410-416 | DOI
[149] Weijer, C. J. Morphogenetic cell movement in Dictyostelium, Seminars in Cell & Developmental Biology, Volume 10 (1999) no. 6, pp. 609-619 | DOI
[150] Weijer, C.; Duschl, G.; David, C. A revision of the Dictyostelium discoideum cell cycle, Journal of Cell Science, Volume 70 (1984) no. 1, pp. 111-131 | DOI
[151] Weijer, C.; Williams, J. Dictyostelium : cell sorting and patterning In: Encyclopedia of Life Sciences (2001) | DOI
[152] Weitz, J. S.; Eksin, C.; Paarporn, K.; Brown, S. P.; Ratcliff, W. C. An oscillating tragedy of the commons in replicator dynamics with game-environment feedback, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 47 | DOI
[153] Wolinsky, E.; Libby, E. Evolution of regulated phenotypic expression during a transition to multicellularity, Evolutionary Ecology, Volume 30 (2016) no. 2, pp. 235-250 | DOI
[154] Yumura, S.; Furuya, K.; Takeuchi, I. Intracellular free calcium responses during chemotaxis of Dictyostelium cells, Journal of Cell Science, Volume 109 (1996) no. 11, pp. 2673-2678
[155] Zada-Hames, I. M.; Ashworth, J. M. The cell cycle and its relationship to development in Dictyostelium discoideum, Developmental Biology, Volume 63 (1978) no. 2, pp. 307-320 | DOI
[156] Zahavi, A.; Harris, K. D.; Nanjundiah, V. An individual-level selection model for the apparent altruism exhibited by cellular slime moulds, Journal of Biosciences, Volume 43 (2018) no. 1, pp. 49-58 | DOI
Cited by Sources:
Web publisher