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Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity

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Abstract

Predation was a powerful selective force promoting increased morphological complexity in a unicellular prey held in constant environmental conditions. The green alga, Chlorella vulgaris, is a well-studied eukaryote, which has retained its normal unicellular form in cultures in our laboratories for thousands of generations. For the experiments reported here, steady-state unicellular C. vulgaris continuous cultures were inoculated with the predator Ochromonas vallescia, a phagotrophic flagellated protist (‘flagellate’). Within less than 100 generations of the prey, a multicellular Chlorella growth form became dominant in the culture (subsequently repeated in other cultures). The prey Chlorella first formed globose clusters of tens to hundreds of cells. After about 10–20 generations in the presence of the phagotroph, eight-celled colonies predominated. These colonies retained the eight-celled form indefinitely in continuous culture and when plated onto agar. These self-replicating, stable colonies were virtually immune to predation by the flagellate, but small enough that each Chlorella cell was exposed directly to the nutrient medium.

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References

  • Abrams, P.A. (1986) Adaptive responses of predators to prey and prey to predators: The failure of the armsrace analogy. Evolution 40, 1229–1247.

    Article  Google Scholar 

  • Bakker, R.T. (1983) The deer flees, the wolf pursues: Incongruencies in predator-prey evolution. In Coevolution (D.J. Futuyma and M. Slatkin, eds), pp. 350-382. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Bennett, W.N. and Boraas, M.E. (1989) A demographic profile of the fastest growing metazoan: A strain of Brachionus calyciflorus Pallas (Rotifera). Oikos 55, 365–369.

    Google Scholar 

  • Bennett, W.N., Boraas, M.E. and Seale, D.B. (1993) Turbidostat culture of Brachionus calyciflorus: An experimental system to assess biological limits on population growth. In Plankton Regulation Dynamics(N. Walz, ed.), pp. 77–86. Springer-Verlag, Berlin.

    Google Scholar 

  • Bonner, J.T. (1988) The Evolution of Complexity by Means of Natural Selection. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Boraas, M.E. (1979) Dynamics of nitrate, algae, and rotifers in continuous culture: Experiments and model simulations. PhD thesis, The Pennsylvania State University, State College, PA.

    Google Scholar 

  • Boraas, M.E. (1980) A chemostat system for the study of rotifer-algal-nitrate interactions. In Evolution and Ecology of Zooplankton Communities (W.C. Kerfoot, ed.), pp. 173–182. University Press of New England, Hanover, NH.

    Google Scholar 

  • Boraas, M.E. (1983) Population dynamics of food-limited rotifers in two-stage chemostat culture. Limnol. Oceanogr. 28, 546–563

    Article  Google Scholar 

  • Boraas, M.E., Estep, K.W., Johnson, P.W. and Sieburth, J.McN. (1988) Phagotrophic phototrophs: The ecological significance of mixotrophy. J. Protozool. 35, 249–252.

    Google Scholar 

  • Boraas, M.E., Seale, D.B. and Holen, D. (1992) Predatory behavior of Ochromonas analyzed with video microscopy. Arch. Hydrobiol. 123, 459–468.

    Google Scholar 

  • Brodie, E.D., III and Brodie, E.D., Jr (1990) Tetrodotoxin resistance in garter snakes: An evolutionary response of predators to dangerous prey. Evolution 44, 651–659.

    Article  Google Scholar 

  • Brodie, E.D., III and Brodie, E.D., Jr (1991) Evolutionary response of predators to dangerous prey: Reduction of toxicity of newts and resistance of garter snakes in island populations. Evolution 45, 221–224.

    Article  Google Scholar 

  • Chao, L., Levin, B.R. and Stewart, F.M. (1977) A complex community in a simple habitat: An experimental study with bacteria and phage. Ecology 58, 369–378.

    Article  Google Scholar 

  • Dawkins, R. and Krebs, J.R. (1979) Arms races between and within species. Proc. R. Soc. Lond. B 205, 489–511.

    Article  PubMed  CAS  Google Scholar 

  • Dodson, S.I. (1989) The ecological role of chemical stimuli for the zooplankton: Predator-induced morphology in Daphnia. Oecologia 78, 361–367.

    Article  Google Scholar 

  • Fott, B. and Novakova, M. (1969) A monograph of the genus Chlorella, the freshwater species. In Studies in Phycology (B. Fott, ed.), pp. 10–74. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.

    Google Scholar 

  • Gillott, M., Holen, D., Ekman, J., Harry, M. and Boraas, M. (1993) Predation-induced E. coli filaments: Are they multicellular? In Proceedings of the 51st Annual Meeting of the Microscopy Society of America (G. Baily and C. Reider, eds), p. 420. San Francisco Press, San Francisco, CA.

    Google Scholar 

  • Gould, S.J. (1975) A direct assault upon the citadel itself. Paleobiology 1, 125–129.

    Google Scholar 

  • Gray, M.W. and Doolittle, W.F. (1982) Has the endosymbiotic hypothesis been proven? Microbiol. Rev. 46, 1–42.

    PubMed  CAS  Google Scholar 

  • Hanson, E.D. (1977) The Origin and Early Evolution of Animals. Wesleyan University Press, Middletown, CT.

    Google Scholar 

  • Hessen, D.O. and Van Donk, E. (1993) Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch. Hydrobiol. 127, 129–140.

    Google Scholar 

  • Holen, D.A. and Boraas, M.E. (1991) The feeding behavior of Spumella sp. as a function of particle size: Implications for bacterial size in pelagic systems. Hydrobiologia 220, 73–88.

    Article  Google Scholar 

  • Holen, D.A. and Boraas, M.E. (1995) Mixotrophy in chrysophytes. In Chrysophyte Algae: Ecology, Phylogeny and Development (C. Sandgren, J.P. Smol and J. Kristiansen, eds), pp. 119–140. Cambridge University Press, Cambridge.

    Google Scholar 

  • Hori, M. (1993) Frequency dependent natural selection in the handedness of scale-eating cichlid fish. Science 260, 216–219.

    PubMed  Google Scholar 

  • Jerison, H.J. (1970) Brain evolution: New light on old principles. Science 170, 1224–1225.

    PubMed  CAS  Google Scholar 

  • Jerison, H.J. (1973) Evolution of the Brain and Intelligence. Academic Press, New York.

    Google Scholar 

  • Margulis, L. (1981) Symbiosis in Cell Evolution. W.H. Freeman, San Francisco, CA.

    Google Scholar 

  • Paine, R.T. (1966) Food web complexity and species diversity. Am. Nat. 100, 65–75.

    Article  Google Scholar 

  • Radinsky, L. (1978) Evolution of brain size in carnivores and ungulates. Am. Nat. 112, 815–831.

    Article  Google Scholar 

  • Schaffer, W.N. and Rosenzweig, M.L. (1978) Homage to the Red Queen. I. Coevolution of predators and their victims. Theor. Pop. Biol. 14, 135–157.

    Article  CAS  Google Scholar 

  • Seale, D.B. (1980) Influence of amphibian larvae on primary production, nutrient flux, and competition in a pond ecosystem. Ecology 61, 1531–1550.

    Article  Google Scholar 

  • Seale, D.B. (1982) Obligate and facultative suspension feeding in anuran larvae: Feeding regulation in Xenopusand Rana . Biol. Bull. 162, 214–231.

    Google Scholar 

  • Seale, D.B., Boraas, M.E., Holen, D.A. and Nealson, K.H. (1990) Use of bioluminescent bacteria, Xenorhabdus luminescens, to measure predation by freshwater microflagellates. FEMS Microb. Ecol. 73, 31–40.

    Google Scholar 

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

    Google Scholar 

  • Stanley, S.M. (1973) An ecological theory for the sudden origin of multicellular life in the Late Precambrian. PNAS 70, 1486–1489.

    Article  PubMed  Google Scholar 

  • Stephens, D.W. and Krebs, D.W. (1986) Foraging Theory. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Thompson, J.N. (1982) Interaction and Coevolution. John Wiley, New York.

    Google Scholar 

  • Tilman, D. (1982) Resource Competition and Community Structure. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Townsend, C.R. and Calow, P. (1981) Physiological Ecology: An Evolutionary Approach to Resource Use. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Van Valen, L. (1973) A new evolutionary law. Evol. Theory 1, 1–30.

    Google Scholar 

  • Vermeij, G.J. (1987) Evolution and Escalation: An Ecological History of Life. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Weis, A.E., McCrea, K.D. and Abrahamson, W.G. (1989) Can there be an escalation arms race without coevolution? Implications from a host-parasitoid simulation. Evol. Ecol. 3, 361–370.

    Article  Google Scholar 

  • Williams, F.M. (1971) Dynamics of microbial populations. In Systems Analysis and Simulation in Ecology(B.C. Patten, ed.), pp. 197–267. Academic Press, New York.

    Google Scholar 

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Boraas, M.E., Seale, D.B. & Boxhorn, J.E. Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity. Evolutionary Ecology 12, 153–164 (1998). https://doi.org/10.1023/A:1006527528063

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