Predation and the formation of multicellular groups in algae

Background: The evolution of multicellular organisms must, at some point, have involved the congregating of single-celled organisms. Algal species exist that sometimes live in groups and sometimes live as single cells. Understanding the conditions that lead to algal assemblage in such cases may cast light on the selective forces that favour multicellularity. Hypothesis: Forming groups could defend algae against predation if predators are unable to engulf large-sized entities. Organisms: Three algal prey (Chlorella sorokiniana, Chlorella vulgaris, and Scenedesmus obliquus) and three predators (Ochromonas spp., Tetrahymena thermophila, and Daphnia magna). Methods: We tested the tendency to aggregate in all nine different prey–predator combinations. Results: At least two of the predators, Ochromonas and Daphnia, were significant predators because their presence decreased algal density. In all nine combinations, adding the predator species led to the formation of algal groups. In three combinations, adding merely products of the predators in the absence of the predators themselves stimulated group formation.

[1]  M. Lürling,et al.  Consumer-induced changes in phytoplankton: inducibility, costs, benefits, and the impact on grazers , 1999 .

[2]  Andrew F. G. Bourke,et al.  Principles of Social Evolution , 2011 .

[3]  Wolpert,et al.  The Origin of Metazoa and the Egg: a Role for Cell Death. , 1998, Journal of theoretical biology.

[4]  M. Lürling,et al.  FO-spectra of chlorophyll fluorescence for the determination of zooplankton grazing , 2004, Hydrobiologia.

[5]  K. Porter,et al.  Enhancement of Algal Growth and Productivity by Grazing Zooplankton , 1976, Science.

[6]  G. J. Velicer,et al.  Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus , 2003, Nature.

[7]  K. Jürgens,et al.  Direct and Indirect Effects of Protist Predation on Population Size Structure of a Bacterial Strain with High Phenotypic Plasticity , 2006, Applied and Environmental Microbiology.

[8]  R. Grosberg,et al.  The Evolution of Multicellularity: A Minor Major Transition? , 2007 .

[9]  Toshiyuki Nakajima,et al.  Exploitation or cooperation? Evolution of a host (ciliate)-benefiting alga in a long-term experimental microcosm culture , 2013, Biosyst..

[10]  E. Elert,et al.  Colony formation in Scenedesmus: grazer-mediated release and chemical features of the infochemical , 1999 .

[11]  Kevin R Foster,et al.  Improved use of a public good selects for the evolution of undifferentiated multicellularity , 2013, eLife.

[12]  MARTIN E. Boraas,et al.  Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity , 1998, Evolutionary Ecology.

[13]  S. West,et al.  Cooperation, clumping and the evolution of multicellularity , 2015, Proceedings of the Royal Society B: Biological Sciences.

[14]  M. Boraas,et al.  Predatory behavior of Ochromonas analyzed with video microscopy , 1992 .

[15]  Ko Yasumoto,et al.  Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones , 2005 .

[16]  K. Rothhaupt,et al.  Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia) , 1994 .

[17]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[18]  M. Lürling,et al.  Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? , 2000 .

[19]  J. Bonner,et al.  The Myxobacteria: New Directions in Studies of Procaryotic Development , 1972 .

[20]  A. Gardner,et al.  Major evolutionary transitions in individuality , 2015, Proceedings of the National Academy of Sciences.

[21]  John H. Koschwanez,et al.  Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity , 2011, PLoS Biology.

[22]  S. West,et al.  Multicellular group formation in response to predators in the alga Chlorella vulgaris , 2016, Journal of evolutionary biology.

[23]  N. King,et al.  Genomic, phylogenetic, and cell biological insights into metazoan origins , 2009 .

[24]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[25]  Dennis Claessen,et al.  Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies , 2014, Nature Reviews Microbiology.

[26]  Hideaki Matsuoka,et al.  Auto-/heterotrophic endosymbiosis evolves in a mature stage of ecosystem development in a microcosm composed of an alga, a bacterium and a ciliate , 2009, Biosyst..

[27]  J. Benndorf,et al.  Direct effects of Daphnia-grazing, not infochemicals, mediate a shift towards large inedible colonies of the gelatinous green alga Sphaerocystis schroeteri , 2007 .

[28]  J. Ryther.  Inhibitory Effects of Phytoplankton upon the Feeding of Daphnia Magna with Reference to Growth, Reproduction, and Survival , 1954 .

[29]  S. Stanley.  An ecological theory for the sudden origin of multicellular life in the late precambrian. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E Szathmary,et al.  The transition from single cells to multicellularity , 2003 .

[31]  J. Kirby,et al.  Deciphering the hunting strategy of a bacterial wolfpack. , 2009, FEMS microbiology reviews.

[32]  Rachel E. Pepper,et al.  Cooperatively generated stresslet flows supply fresh fluid to multicellular choanoflagellate colonies. , 2013, Physical review letters.

[33]  S. West,et al.  Group Formation, Relatedness, and the Evolution of Multicellularity , 2013, Current Biology.

[34]  J. Strassmann,et al.  Fruiting bodies of the social amoeba Dictyostelium discoideum increase spore transport by Drosophila , 2014, BMC Evolutionary Biology.

[35]  Ko Yasumoto,et al.  Time-of-Flight LC/MS Identification and Confirmation of a Kairomone in Daphnia magna Cultured Medium , 2008 .