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On the transfer of fitness from the cell to the multicellular organism

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Abstract

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ–soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae – which contain both unicellular and multicellular members – to illustrate the principles and conclusions discussed.

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References

  • Bell G. (1985). The origin and early evolution of germ cells as illustrated by the Volvocales. In: Halvorson H.O., Monroy A. (eds), The Origin and Evolution of Sex. Alan R. Liss, Inc., New York, pp. 221–256

    Google Scholar 

  • Benkman C.W. (1993). Adaptation to single resources and the evolution of Crossbill (Loxia) diversity. Ecol. Monogr. 63:305–325

    Article  Google Scholar 

  • Benson K.E., Stephens D.W. (1996). Interruptions, tradeoffs, and temporal discounting. Am. Zool. 36:506–517

    Google Scholar 

  • Blows M.W., Chenoweth S.F., Hine E. (2004). Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 163:E329–E340

    Article  Google Scholar 

  • Buchheim M.A., McAuley M.A., Zimmer E.A., Theriot E.C., Chapman R.L. (1994). Multiple origins of colonial green flagellates from unicells: evidence from molecular and organismal characters. Mol. Phylogenet. Evol. 3:322–343

    Article  PubMed  Google Scholar 

  • Buss L.W. (1987). The Evolution of Individuality. Princeton University, Princeton, NJ

    Google Scholar 

  • Carriere Y., Roff D.A. (1995). The evolution of offspring size and number - a test of the Smith–Fretwell model in 3 species of crickets. Oecologia (Berlin) 102:389–396

    Article  Google Scholar 

  • Charlesworth B., Leon J.A. (1976). The relation of reproductive effort to age. Am. Nat. 110:449–459

    Article  Google Scholar 

  • Coleman A.W. (1999). Phylogenetic analysis of ‘Volvocacae’ for comparative genetic studies. Proc. Natl. Acad. Sci. USA 96:13892–13897

    Article  PubMed  Google Scholar 

  • Damuth J., Heisler I.L. (1988). Alternative Formulations of Multilevel Selection. Biol. Phil. 3:407–430

    Article  Google Scholar 

  • Desnitski A.G. (1995). A review on the evolution of development in Volvox–morphological and physiological aspects. Eur. J. Protistol. 31:241–247

    Google Scholar 

  • Enquist B.J., Niklas K.J. (2001). Invariant scaling relations across tree-dominated communities. Nature (London) 410:655–660

    Article  Google Scholar 

  • Fewell J., Page R.E. Jr. (1999). The emergence of division of labour in forced associations of normally solitary ant queens. Evol. Ecol. Res. 1:1–12

    Google Scholar 

  • Foster K.R., Fortunato A., Strassmann J.E., Queller D.C. (2002). The costs and benefits of being a chimera. Proc. R. Soc. Lond B Biol. Sci. 269:2357–2362

    Article  Google Scholar 

  • Hudson R.E., Aukema J.E., Rispe C., Roze D. (2002). Altruism, cheating, and anticheater adaptations in cellular slime molds. The Am. Nat. 160:31–43

    Article  Google Scholar 

  • King N., Carroll S.B. (2001). A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. Proc. Natl. Acad. Sci. USA 98:15032–15037

    Article  PubMed  Google Scholar 

  • Kirk D.L. (1997). The genetic program for germ-soma differentiation in Volvox. Annu. Rev. Genet. 31:359–380

    Article  PubMed  Google Scholar 

  • Kirk D.L. (1998). Volvox: Molecular-genetic Origins of Multicellularity and Cellular Differentiation. Cambridge University Press, Cambridge

    Google Scholar 

  • Kirk D.L., Moleirinho A., Patuzzi R.B. (1997). Microphonic and DPOAE measurements suggest a micromechanical mechanism for the ‘bounce’ phenomenon following low-frequency tones. Hear. Res. 112:69–86

    Article  PubMed  Google Scholar 

  • Kisdi E. (2001). Long-term adaptive diversity in Levene-type models. Evol. Ecol. Res. 3:721–727

    Google Scholar 

  • Koufopanou V. (1994). The evolution of soma in the Volvocales. The Am. Nat. 143:907–931

    Article  Google Scholar 

  • Koufopanou V., Bell G. (1993). Soma and germ - an experimental approach using Volvox. Proc. R. Soc. London B. Biol. Sci. 254:107–113

    Article  Google Scholar 

  • Lachmann M., Blackstone N.W., Haig D., Kowald A., Michod R.E., Szathmáry E., Werren J.H., Wolpert L. (2003). Group report: cooperation and conflict in the evolution of genomes, cells, and multicellular organisms. In: Hammerstein P. (eds), Genetic and Cultural Evolution of Cooperation. MIT Press, Cambridge MA, pp. 327–356

    Google Scholar 

  • Larson A., Kirk M.M., Kirk D.L. (1992). Molecular phylogeny of the volvocine flagellates. Mol. Biol. Evol. 9:85–105

    PubMed  Google Scholar 

  • Levins R. 1968. Evolution in Changing Environments, Some Theoretical Explorations. Princeton University Press

  • Maynard Smith J.M. (1988). Evolutionary progress and levels of selection. In: Nitecki M.H. (eds), Evolutionary Progress. University of Chicago Press, Chicago, pp. 219–230

    Google Scholar 

  • Maynard Smith J.M. (1991). A Darwinian view of symbiosis. In: Margulis L., Fester R. (eds), Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge, pp. 26–39

    Google Scholar 

  • Maynard Smith J.M., Szathmáry E. (1995). The Major Transitions in Evolution. W.H. Freeman, San Francisco

    Google Scholar 

  • Michod R.E. (1978). Evolution of life histories in response to age-specific mortality factors. Am. Nat. 113:531–550

    Article  Google Scholar 

  • Michod R.E. (1996). Cooperation and conflict in the evolution of individuality. II. Conflict mediation. Proc. R. Soc. London B Biol. Sci. 263:813–822

    Article  Google Scholar 

  • Michod R.E. (1997a). Cooperation and conflict in the evolution of individuality. I. Multi-level selection of the organism. Am. Nat. 149:607–645

    Article  Google Scholar 

  • Michod R.E. (1997b). Evolution of the individual. Am. Nat. 150:S5–S21

    Article  Google Scholar 

  • Michod R.E. (1999). Darwinian Dynamics, Evolutionary Transitions in Fitness and Individuality. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Michod R.E. (2003). Cooperation and conflict mediation during the origin of multicellularity. In: Hammerstein P. (eds), Genetic and Cultural Evolution of Cooperation. MIT Press, Cambridge, MA, pp. 261–307

    Google Scholar 

  • Michod R.E., Nedelcu A.M. (2003). Cooperation and conflict during the unicellular-multicellular and prokaryotic–eukaryotic transitions. In: Moya A., Font E. (eds), Evolution: From molecules to ecosystems. Oxford University Press, Oxford, pp. 195–208

    Google Scholar 

  • Michod R.E., Nedelcu A.M., Roze D. (2003). Cooperation and conflict in the evolution of individuality IV. Conflict mediation and evolvability in Volvox carteri. BioSystems 69:95–114

    Article  PubMed  Google Scholar 

  • Michod R.E., Roze D. (1997). Transitions in individuality. Proc. R. Soc. London B Biol. Sci. 264:853–857

    Article  Google Scholar 

  • Michod R.E., Roze D. (1999). Cooperation and conflict in the evolution of individuality. III. Transitions in the unit of fitness. In: Nehaniv C.L. (eds), Mathematical and Computational Biology: Computational Morphogenesis, Hierarchical Complexity, and Digital Evolution. American Mathematical Society, Providence, Rhode Island, pp. 47–92

    Google Scholar 

  • Michod R.E., Roze D. (2000). Some aspects of reproductive mode and the origin of multicellularity. Selection 1:97–109

    Article  Google Scholar 

  • Michod R.E., Roze D. (2001). Cooperation and conflict in the evolution of multicellularity. Heredity 81:1–7

    Article  Google Scholar 

  • Michod R.E., Viossat Y., Solari C.A., Nedelcu A.M. and Hurrand M. 2005. Life history evolution and the origin of multicellularity. J. Theor. Biol. In Press

  • Morgan N.C. (1980). Secondary production. In: Le Cren E.D., Lowe-McConell R.H. (eds), The Functioning of Freshwater Ecosystems, IBP 22. Cambridge University Press, Cambridge, pp. 247–340

    Google Scholar 

  • Nedelcu A.M., Michod R.E. (2003). Evolvability, modularity, and individuality during the transition to multicellularity in volvocalean green algae. In: Schlosser G., Wagner G.P. (eds), Modularity in development and evolution. University of Chicago Press, Chicago, pp. 466–489

    Google Scholar 

  • Niklas K.J. (1994). Plant Allometry: The Scaling of Form and Process. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Niklas K.J. (2000). The evolution of plant body plans-A biomechanical perspective. Ann. Bot. 85:411–438

    Article  Google Scholar 

  • Niklas K.J., Enquist B.J. (2001). From the Cover: Invariant scaling relationships for interspecific plant biomass production rates and body size. Proc. Natl. Acad. Sci. USA 98:2922–2927

    Article  PubMed  Google Scholar 

  • Nozaki H., Ohta N., Takano H., Watanabe M.M. (1999). Reexamination of phylogenetic relationships within the colonial volvocales (chlorophyta): an analysis of atpB and rbcL gene sequences. J. Phycol. 35:104–112

    Article  Google Scholar 

  • Nozaki H. (2003). Origin and evolution of the genera Pleodorina and Volvox (Volvocales). Biologia 58:425–431

    Google Scholar 

  • Nozaki H., Misawa K., Kajita T., Kato M., Nohara S., Watanabe M. (2000). Origin and evolution of the colonial Volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Mol. Phylogenet. Evol. 17:256–268

    Article  PubMed  Google Scholar 

  • Nozaki H., Misumi O., Kuroiwa T. (2003). Phylogeny of the quadriflagellate Volvocales (Chlorophyceae) based on chloroplast multigene sequences. Mol. Phylogenet. Evol. 29:58–66

    Article  PubMed  Google Scholar 

  • Nozaki H., Takahara M., Nakazawa A., Kita Y., Yamada T., Takano H., Kawano S., Kato M. (2002). Evolution of rbcL group IA introns and intron open reading frames within the colonial Volvocales (Chlorophyceae). Mol. Phylogenet. Evol. 23:326–338

    Article  PubMed  Google Scholar 

  • Okasha S. 2006. Multi-level selection and the major transitions in evolution. Proc. Phil. Sci. Assoc. PSA2004 (forthcoming)

  • Pentecost A. (1983). The distribution of daughter colonies and cell numbers in a natural population of Volvox aureus Ehrenb. Ann. Bot. 52:769–776

    Google Scholar 

  • Porter K.G. (1977). Plant–animal interface in freshwater ecosystems. Am. Sci. 65:159–170

    Google Scholar 

  • Queller D.C. (2000). Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. London B Biol. Sci. 355:1647–1655

    Article  Google Scholar 

  • Queller D.C., Ponte E., Bozzaro S., Strassmann J.E. (2003). Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science (Washington, D.C.) 299:105–106

    Article  Google Scholar 

  • Rausch H., Larsen N., Schmitt R. (1989). Phylogenetic relationships of the green alga Volvox carteri deduced from small-subunit ribosomal RNA comparisons. J. Mol. Evol. 29:255–265

    Article  PubMed  Google Scholar 

  • Reynolds C.S. (1984). The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Reznick D. (1985). Costs of reproduction - an evaluation of the empirical-evidence. Oikos 44:257–267

    Article  Google Scholar 

  • Roff D.A. (2000). Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence. J. Evol. Biol. 13:434–445

    Article  Google Scholar 

  • Roff D.A. (2002). Life History Evolution. Sinauer Assoc, Sunderland, Mass

    Google Scholar 

  • Roze D., Michod R.E. (2001). Mutation load, multi-level selection and the evolution of propagule size during the origin of multicellularity. Am. Nat. 158:638–654

    Article  Google Scholar 

  • Rueffler C., Van Dooren T.J.M., Metz J.A.J. (2004). Adaptive walks on changing landscapes: Levins’ approach extended. Theor. Popul. Biol. 65:165–178

    Article  PubMed  Google Scholar 

  • Sato H. (2002). Invasion of unisexuals in hermaphrodite populations of animal-pollinated plants: Effects of pollination ecology and floral size-number trade-offs. Evolution 56:2374–2382

    PubMed  Google Scholar 

  • Schaffer W.M. (1974). Selection for optimal life histories: the effects of age structure. Ecology 55:291–303

    Article  Google Scholar 

  • Shikano S., Luckinbill L.S., Kurihara Y. (1990). Changes of traits in a bacterial population associated with protozoal predation. Microb. Ecol. 20:75–84

    Article  Google Scholar 

  • Shimkets L.J. (1990). Social and developmental biology of the myxobacteria. Microbiol. Rev. 54:473–501

    PubMed  Google Scholar 

  • Solari, C. A. 2005. A Hydrodynamics Approach to Fitness in Volvocine Algae. University of Arizona. Ref Type: Thesis/Dissertation

  • Solari, C.A., Kessler J.O. and Michod R.E. 2006a. A hydrodynamics approach to the evolution of multicellularity: Flagellar motility and cell differentiation in volvocalean green algae. The American Naturalist In press

  • Solari C.A., Ganguly S., Kessler J.O., Michod R.E. and Goldstein R.E. 2006b. Multicellularity and the functional interdependence of motility and molecular transport. Proc. Natl. Acad. Sci. USA In press

  • Solari C.A., Nedelcu A.M., Michod R.E. (2003). Fitness and complexity in volvocalean green algae. In: Lipson H., Antonsson E.K., Koza J.R. (eds), Computational Synthesis, From Basic Building Blocks to High-level Functionality. AAAI Press, Menlo Park, CA, pp. 218–225

    Google Scholar 

  • Sommer U., Giliwicz Z.M. (1986). Long-range vertical migration of Volvox in tropical Lake Cahora Bassa (Mozambique). Limnol. Oceanogr. 31:650–653

    Article  Google Scholar 

  • Stearns S.C. (1992). The Evolution of Life Histories. Oxford University Press, Oxford

    Google Scholar 

  • Strassmann J.E., Zhu Y., Queller D.C. (2000). Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature (London) 408:965–967

    Article  Google Scholar 

  • Strohm E., Linsenmair K.E. (2000). Allocation of parental investment among individual offspring in the European beewolf Philanthus triangulum F. (Hymenoptera : Sphecidae). Biol. J. Linn. Soc. 69:173–192

    Article  Google Scholar 

  • Takada T., Nakajima H. (1996). The optimal allocation for seed reproduction and vegetative reproduction in perennial plants: An application to the density-dependent transition matrix model. J. Theor. Biol. 182:179–191

    Article  Google Scholar 

  • Velicer G.J., Kroos L., Lenski R.E. (2000). Developmental cheating in the social bacterium Myxococcus xanthus. Nature (London) 404:598–601

    Article  Google Scholar 

  • West G.B., Brown J.H., Enquist B.J. (1997). A general model for the origin of allometric scaling laws in biology. Science (Washington, D.C.) 276:122–126

    Article  Google Scholar 

  • West G.B., Brown J.H., Enquist B.J. (1999). The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science (Washington, D.C.) 284:1677–1679

    Article  Google Scholar 

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Acknowledgements

Research supported by NSF grant DEB-9527716. The ideas presented here have been discussed and developed with the help of many colleagues, especially, in alphabetical order, M. Herron, M. Hurrand, T. Huxman, J. Kessler, A. Nedelcu, D. Roze, C. Solari, and Y. Viossat. I also appreciate the comments of S. Okasha which improved the manuscript.

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Michod, R.E. On the transfer of fitness from the cell to the multicellular organism. Biol Philos 20, 967–987 (2005). https://doi.org/10.1007/s10539-005-9018-2

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