First among equals: competition between genetically identical cells

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ABSTRACT Competition between genetically identical organisms is considered insignificant in evolutionary theory because it is presumed to have little selective consequence. We argue that


competition between genetically identical cells could improve the fitness of a multicellular organism by directing fitter cells to the germ line or by eliminating unfit cells, and that


cell-competition mechanisms have been conserved in multicellular organisms. We propose that competition between genetically identical or highly similar units could have similar selective


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institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS EVOLUTION OF BIOLOGICAL COOPERATION: AN ALGORITHMIC APPROACH Article Open access


17 January 2024 THE EVOLUTION OF MECHANISMS TO PRODUCE PHENOTYPIC HETEROGENEITY IN MICROORGANISMS Article Open access 25 January 2022 ANCESTRAL SOCIAL ENVIRONMENTS PLUS NONLINEAR BENEFITS


CAN EXPLAIN COOPERATION IN HUMAN SOCIETIES Article Open access 24 November 2022 REFERENCES * Hamilton, W. D. The genetical evolution of social behaviour. I. _J. Theor. Biol._ 7, 1–16 (1964).


Article  CAS  PubMed  Google Scholar  * Hamilton, W. D. The genetical evolution of social behaviour. II. _J. Theor. Biol._ 7, 17–52 (1964). Article  CAS  PubMed  Google Scholar  * Maynard


Smith, J. & Szathmary, E. _The Major Transitions in Evolution_ (Oxford Univ. Press, New York, 1995). Google Scholar  * Michod, R. _Darwinian Dynamics_ (Princeton Univ. Press, Princeton,


New Jersey, 1999). Google Scholar  * Shaulsky, G. & Loomis, W. F. Cell type regulation in response to expression of ricin A in _Dictyostelium_. _Dev. Biol._ 160, 85–98 (1993). Article 


CAS  PubMed  Google Scholar  * Greenwald, I. LIN-12/Notch signaling: lessons from worms and flies. _Genes Dev._ 12, 1751–1762 (1998). Article  CAS  PubMed  Google Scholar  * Rooke, J. E.


& Xu, T. Positive and negative signals between interacting cells for establishing neural fate. _Bioessays_ 20, 209–214 (1998). Article  CAS  PubMed  Google Scholar  * Lewis, J. Notch


signalling and the control of cell fate choices in vertebrates. _Semin. Cell Dev. Biol._ 9, 583–589 (1998). Article  CAS  PubMed  Google Scholar  * Morata, G. & Ripoll, P. Minutes:


mutants of _Drosophila_ autonomously affecting cell division rate. _Dev. Biol._ 42, 211–221 (1975). Article  CAS  PubMed  Google Scholar  * Lambertsson, A. The minute genes in _Drosophila_


and their molecular functions. _Adv. Genet._ 38, 69–134 (1998). Article  CAS  PubMed  Google Scholar  * Simpson, P. & Morata, G. Differential mitotic rates and patterns of growth in


compartments in the _Drosophila_ wing. _Dev. Biol._ 85, 299–308 (1981). Article  CAS  PubMed  Google Scholar  * Prober, D. A. & Edgar, B. A. Ras1 promotes cellular growth in the


_Drosophila_ wing. _Cell_ 100, 435–446 (2000). Article  CAS  PubMed  Google Scholar  * de la Cova, C., Abril, M., Bellosta, P., Gallant, P. & Johnston, L. A. _Drosophila_ Myc regulates


organ size by inducing cell competition. _Cell_ 117, 107–116 (2004). Article  CAS  PubMed  Google Scholar  * Moreno, E. & Basler, K. dMyc transforms cells into super-competitors. _Cell_


117, 117–129 (2004). Article  CAS  PubMed  Google Scholar  * Burke, R. & Basler, K. Dpp receptors are autonomously required for cell proliferation in the entire developing _Drosophila_


wing. _Development_ 122, 2261–2269 (1996). CAS  PubMed  Google Scholar  * Johnston, L. A. & Sanders, A. L. Wingless promotes cell survival but constrains growth during _Drosophila_ wing


development. _Nature Cell Biol._ 5, 827–833 (2003). Article  CAS  PubMed  Google Scholar  * Abrams, J. M. Competition and compensation: coupled to death in development and cancer. _Cell_


110, 403–406 (2002). Article  CAS  PubMed  Google Scholar  * Milan, M. Survival of the fittest. Cell competition in the _Drosophila_ wing. _EMBO Rep._ 3, 724–725 (2002). Article  CAS  PubMed


  PubMed Central  Google Scholar  * Moreno, E., Basler, K. & Morata, G. Cells compete for decapentaplegic survival factor to prevent apoptosis in _Drosophila_ wing development. _Nature_


416, 755–759 (2002). Article  CAS  PubMed  Google Scholar  * Oliver, E. R., Saunders, T. L., Tarle, S. A. & Glaser, T. Ribosomal protein L24 defect in belly spot and tail (_Bst_), a


mouse _Minute_. _Development_ 131, 3907–3920 (2004). Article  CAS  PubMed  Google Scholar  * Gallardo, M. H., Bickham, J. W., Honeycutt, R. L., Ojeda, R. A. & Kohler, N. Discovery of


tetraploidy in a mammal. _Nature_ 401, 341 (1999). Article  CAS  PubMed  Google Scholar  * Eakin, G. S. & Behringer, R. R. Tetraploid development in the mouse. _Dev. Dyn._ 228, 751–766


(2003). Article  PubMed  Google Scholar  * Eakin, G. S., Hadjantonakis, A. K., Papaioannou, V. E. & Behringer, R. R. Developmental potential and behavior of tetraploid cells in the mouse


embryo. _Dev. Biol._ 288, 150–159 (2005). Article  CAS  PubMed  Google Scholar  * Heard, E., Clerc, P. & Avner, P. X-chromosome inactivation in mammals. _Annu. Rev. Genet._ 31, 571–610


(1997). Article  CAS  PubMed  Google Scholar  * Migeon, B. R. Non-random X chromosome inactivation in mammalian cells. _Cytogenet. Cell. Genet._ 80, 142–148 (1998). Article  CAS  PubMed 


Google Scholar  * Van den Veyver, I. B. Skewed X inactivation in X-linked disorders. _Semin. Reprod. Med._ 19, 183–191 (2001). Article  CAS  PubMed  Google Scholar  * Belmont, J. W. Genetic


control of X inactivation and processes leading to X-inactivation skewing. _Am. J. Hum. Genet._ 58, 1101–1108 (1996). CAS  PubMed  PubMed Central  Google Scholar  * Conley, M. E. et al.


Expression of the gene defect in X-linked agammaglobulinemia. _N. Engl. J. Med._ 315, 564–567 (1986). Article  CAS  PubMed  Google Scholar  * Fearon, E. R., Winkelstein, J. A., Civin, C. I.,


Pardoll, D. M. & Vogelstein, B. Carrier detection in X-linked agammaglobulinemia by analysis of X-chromosome inactivation. _N. Engl. J. Med._ 316, 427–431 (1987). Article  CAS  PubMed 


Google Scholar  * Puck, J. M., Nussbaum, R. L. & Conley, M. E. Carrier detection in X-linked severe combined immunodeficiency based on patterns of X chromosome inactivation. _J. Clin.


Invest._ 79, 1395–1400 (1987). Article  CAS  PubMed  PubMed Central  Google Scholar  * Fearon, E. R., Kohn, D. B., Winkelstein, J. A., Vogelstein, B. & Blaese, R. M. Carrier detection in


the Wiskott Aldrich syndrome. _Blood_ 72, 1735–1739 (1988). CAS  PubMed  Google Scholar  * Greer, W. L. et al. X-chromosome inactivation in the Wiskott–Aldrich syndrome: a marker for


detection of the carrier state and identification of cell lineages expressing the gene defect. _Genomics_ 4, 60–67 (1989). Article  CAS  PubMed  Google Scholar  * Parrish, J. E., Scheuerle,


A. E., Lewis, R. A., Levy, M. L. & Nelson, D. L. Selection against mutant alleles in blood leukocytes is a consistent feature in incontinentia pigmenti type 2. _Hum. Mol. Genet._ 5,


1777–1783 (1996). Article  CAS  PubMed  Google Scholar  * Wengler, G., Gorlin, J. B., Williamson, J. M., Rosen, F. S. & Bing, D. H. Nonrandom inactivation of the X chromosome in early


lineage hematopoietic cells in carriers of Wiskott–Aldrich syndrome. _Blood_ 85, 2471–2477 (1995). CAS  PubMed  Google Scholar  * Parolini, O. et al. X-linked Wiskott–Aldrich syndrome in a


girl. _N. Engl. J. Med._ 338, 291–295 (1998). Article  CAS  PubMed  Google Scholar  * Ellermeier, C. D., Hobbs, E. C., Gonzalez-Pastor, J. E. & Losick, R. A three-protein signaling


pathway governing immunity to a bacterial cannibalism toxin. _Cell_ 124, 549–559 (2006). Article  CAS  PubMed  Google Scholar  * Gonzalez-Pastor, J. E., Hobbs, E. C. & Losick, R.


Cannibalism by sporulating bacteria. _Science_ 301, 510–513 (2003). Article  CAS  PubMed  Google Scholar  * Loomis, W. F. Dictyostelium discoideum. _A Developmental System_ (Academic Press,


New York, 1975). Google Scholar  * Kessin, R. H. Dictyostelium _— Evolution, Cell Biology, and the Development of Multicellularity_ (Cambridge Univ. Press, Cambridge, UK, 2001). Book  Google


Scholar  * Leach, C. K., Ashworth, J. M. & Garrod, D. R. Cell sorting out during the differentiation of mixtures of metabolically distinct populations of _Dictyostelium discoideum_. _J.


Embryol. Exp. Morphol._ 29, 647–661 (1973). CAS  PubMed  Google Scholar  * Tasaka, M. & Takeuchi, I. Role of cell sorting in pattern formation in _Dictyostelium discoideum_.


_Differentiation_ 18, 191–196 (1981). Article  CAS  PubMed  Google Scholar  * Thompson, C. R. & Kay, R. R. Cell-fate choice in _Dictyostelium_: intrinsic biases modulate sensitivity to


DIF signaling. _Dev. Biol._ 227, 56–64 (2000). Article  CAS  PubMed  Google Scholar  * Blaschke, A., Weijer, C. & MacWilliams, H. _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_ 32, 1–9 (1986). Article  Google Scholar  * McDonald, S.


A. & Durston, A. J. The cell cycle and sorting behaviour in _Dictyostelium discoideum_. _J. Cell Sci._ 66, 195–204 (1984). CAS  PubMed  Google Scholar  * Araki, T., Nakao, H., Takeuchi,


I. & Maeda, Y. Cell-cycle-dependent sorting in the development of _Dictyostelium_ cells. _Dev. Biol._ 162, 221–228 (1994). Article  CAS  PubMed  Google Scholar  * Weijer, C. J., Duschl,


G. & David, C. N. Dependence of cell-type proportioning and sorting on cell cycle phase in _Dictyostelium discoideum_. _J. Cell Sci._ 70, 133–145 (1984). CAS  PubMed  Google Scholar  *


Strassmann, J. E., Zhu, Y. & Queller, D. C. Altruism and social cheating in the social amoeba _Dictyostelium discoideum_. _Nature_ 408, 965–967 (2000). Article  CAS  PubMed  Google


Scholar  * Laird, D. J., De Tomaso, A. W. & Weissman, I. L. Stem cells are units of natural selection in a colonial ascidian. _Cell_ 123, 1351–1360 (2005). Article  CAS  PubMed  Google


Scholar  * De Tomaso, A. W. et al. Isolation and characterization of a protochordate histocompatibility locus. _Nature_ 438, 454–459 (2005). Article  CAS  PubMed  PubMed Central  Google


Scholar  * Stoner, D. S. & Weissman, I. L. Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. _Proc. Natl Acad. Sci.


USA_ 93, 15254–15259 (1996). Article  CAS  PubMed  PubMed Central  Google Scholar  * Stoner, D. S., Rinkevich, B. & Weissman, I. L. Heritable germ and somatic cell lineage competitions


in chimeric colonial protochordates. _Proc. Natl Acad. Sci. USA_ 96, 9148–9153 (1999). Article  CAS  PubMed  PubMed Central  Google Scholar  * Extavour, C. G. & Akam, M. Mechanisms of


germ cell specification across the metazoans: epigenesis and preformation. _Development_ 130, 5869–5884 (2003). Article  CAS  PubMed  Google Scholar  * Buss, L. W. Evolution, development,


and the units of selection. _Proc. Natl Acad. Sci. USA_ 80, 1387–1391 (1983). Article  CAS  PubMed  PubMed Central  Google Scholar  * Johnson, J. et al. Oocyte generation in adult mammalian


ovaries by putative germ cells in bone marrow and peripheral blood. _Cell_ 122, 303–315 (2005). Article  CAS  PubMed  Google Scholar  * Miyata, H. & Miyata, M. Mode of conjugation in


homothallic cells of _Schizosaccharomyces pombe_. _J. Gen. Appl. Microbiol._ 27, 365–371 (1981). Article  Google Scholar  * Klar, A. J. Differentiated parental DNA strands confer


developmental asymmetry on daughter cells in fission yeast. _Nature_ 326, 466–470 (1987). Article  CAS  PubMed  Google Scholar  * Klar, A. J. The developmental fate of fission yeast cells is


determined by the pattern of inheritance of parental and grandparental DNA strands. _EMBO J._ 9, 1407–1415 (1990). Article  CAS  PubMed  PubMed Central  Google Scholar  * Lark, K. G.


Nonrandom segregation of sister chromatids in _Vicia faba_ and _Triticum boeoticum_. _Proc. Natl Acad. Sci. USA_ 58, 352–359 (1967). Article  CAS  PubMed  PubMed Central  Google Scholar  *


Rosenberger, R. F. & Kessel, M. Nonrandom sister chromatid segregation and nuclear migration in hyphae of _Aspergillus nidulans_. _J. Bacteriol._ 96, 1208–1213 (1968). CAS  PubMed 


PubMed Central  Google Scholar  * Lark, K. G., Consigli, R. A. & Minocha, H. C. Segregation of sister chromatids in mammalian cells. _Science_ 154, 1202–1205 (1966). Article  CAS  PubMed


  Google Scholar  * Potten, C. S., Hume, W. J., Reid, P. & Cairns, J. The segregation of DNA in epithelial stem cells. _Cell_ 15, 899–906 (1978). Article  CAS  PubMed  Google Scholar  *


Potten, C. S., Owen, G. & Booth, D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. _J. Cell Sci._ 115, 2381–2388 (2002). CAS  PubMed  Google


Scholar  * Merok, J. R., Lansita, J. A., Tunstead, J. R. & Sherley, J. L. Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell


kinetics. _Cancer Res._ 62, 6791–6795 (2002). CAS  PubMed  Google Scholar  * Karpowicz, P. et al. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically


_in vitro_. _J. Cell Biol._ 170, 721–732 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Kaykov, A. & Arcangioli, B. A programmed strand-specific and modified nick in _S.


pombe_ constitutes a novel type of chromosomal imprint. _Curr. Biol._ 14, 1924–1928 (2004). Article  CAS  PubMed  Google Scholar  * Vengrova, S. & Dalgaard, J. Z. RNase-sensitive DNA


modification(s) initiates _S. pombe_ mating-type switching. _Genes Dev._ 18, 794–804 (2004). Article  CAS  PubMed  PubMed Central  Google Scholar  * Cairns, J. Mutation selection and the


natural history of cancer. _Nature_ 255, 197–200 (1975). Article  CAS  PubMed  Google Scholar  * Armakolas, A. & Klar, A. J. Cell type regulates selective segregation of mouse chromosome


7 DNA strands in mitosis. _Science_ 311, 1146–1149 (2006). Article  CAS  PubMed  Google Scholar  * Frank, S. A. Mutual policing and repression of competition in the evolution of cooperative


groups. _Nature_ 377, 520–522 (1995). Article  CAS  PubMed  Google Scholar  * Jacob, F. Evolution and tinkering. _Science_ 196, 1161–1166 (1977). Article  CAS  PubMed  Google Scholar 


Download references ACKNOWLEDGEMENTS We thank D. Queller, L. Santorelli, A. Kuspa and B. Loomis for critical review of this manuscript and for helpful discussions. We thank Z. Pancer, J.


Strassmann and N. Boerkoel for enlightening discussions. This work has been supported by a FIBR (Frontiers in Integrative Biological Research) grant from the US National Science Foundation.


AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, 77030, Texas, USA Anupama Khare & Gad


Shaulsky Authors * Anupama Khare View author publications You can also search for this author inPubMed Google Scholar * Gad Shaulsky View author publications You can also search for this


author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Gad Shaulsky. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. RELATED


LINKS RELATED LINKS DATABASES OMIM incontinentia pigmenti type 2 Wiskott–Aldrich syndrome X-linked agammaglobulinaemia X-linked severe combined immunodeficiency FURTHER INFORMATION Gad


Shaulsky's homepage RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Khare, A., Shaulsky, G. First among equals: competition between genetically


identical cells. _Nat Rev Genet_ 7, 577–583 (2006). https://doi.org/10.1038/nrg1875 Download citation * Published: 16 May 2006 * Issue Date: 01 July 2006 * DOI:


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