Abstract
Exceptionally for a developing system, the pathways of intercellular communication are fairly well characterised in the cellular slime molds. This paper attempts to provide adaptive explanations for the origin of the following features and consequences of communication between cellular slime mold cells: the tendency to congregate, chemotaxis to a released signal, signal relay from cell to cell, oscillatory signal release and an invariant ratio of the terminally differentiated cell types. For the sake of specificity attention is directed at the speciesDictyostelium discoideum. Central to the entire analysis is the assumption that contiguous groups of feeding cells are, and in the past were, genetically identical. It is suggested that, in respect of most of the features listed above, the critical event which started things off must have been the acquisition by the cell membrane of permeability for a substance normally produced intracellularly as a response to the stress of starvation. An argument is presented for treating social behaviour in these organisms, and in particular the suicide by cells which differentiate into stalk, as an example of group selection.
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References
Amagai A, Ishida S and Takeuchi I 1983 Cell differentiation in a temperature-sensitive stalkless mutant ofDictyostelium discoideum;J. Embryol. Exp. Morphol. 74 235–243
Armstrong D P 1984 Why don’t cellular slime molds cheat?;J. Theor. Biol. 109 271–283
Atkinson D E 1968 The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers;Biochemistry 7 4030–4034
Bonner J T, Koontz P G Jr and Paton D 1953 Size in relation to the rate of migration in the slime moldDictyostelium discoideum;Mycologia 45 235–240
Bonner J T 1967The Cellular Slime Molds, 2nd edition (New Jersey Princeton University Press)
Bonner J T, Barkley D S, Hall E M, Konijn T M, Mason J W, O’Keefe G and Wolfe P B 1969 Acrasin, acrasinase and the sensitivity to acrasin inDictyostelium discoideum;Dev. Biol. 20 72–77
Bonner J T 1980The Evolution of culture in Animals (New Jersey Princeton University Press)
Bonner J T 1982 Evolutionary strategies and developmental constraints in the cellular slime molds;Am. Nat. 119 530–552
Conner W E, Eisner T, Meer R K V, Guerrero A, Ghiringelli D and Meinwald J 1980 Sex attractant of an arctiid moth (Uthethesia ornatrix): a pulsed chemical signal;Behav. Ecol. Sociobiol. 7 55–63
Darmon M, Brachet P and Pereira da Silva L H 1975 Chemotactic signals induce cell differentiation inDictyostelium discoideum;Proc. Natl. Acad. Sci. USA 72 3163–3166
Ellison A M and Buss L W 1983 A naturally occurring developmental synergism between the cellular slime moldDictyostelium mucoroides and the fungusMucor hiemalis;Am. J. Bot. 70 298–302
Gerisch G 1976 Extracellular cyclic AMP phosphodiesterase regulation in agar plate cultures ofDictyostelium discoideum;Cell Differ. 5 21–25
Gerisch G and Wick U 1975 Intracellular oscillations and release of cyclic AMP fromDictyostelium cells;Biochem. Biophys. Res. Commun. 65 364–370
Gerisch G, Malchow D, Roos E, Wick U and Wurster B 1977 inCell interactions in Differentiation (eds) I Saxen and L Weiss (New York: Academic Press)
Gerisch G, Fromm H, Huesgen A and Wick U 1975 Control of cell-contact sites by cyclic AMP pulses in differentiatingDictyostelium cells;Nature (London) 255 547–549
Goldbeter A 1974 Modulation of the adenylate energy charge by sustained metabolic oscillations;FEBS Lett. 43 327–330
Goldbeter A and Segel L A 1977 Unified mechanism for relay and oscillation of cyclic AMP inDictyostelium discoideum;Proc. Natl. Acad. Sci. USA 74 1543–1547
Gregg J H 1971 Developmental potential of isolatedDictyostelium myxamoebae;Dev. Biol. 26 473–485
Gould S J and Lewontin R C 1979 The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme;Proc. R. Soc. London B205 581–598
Haldane J B S 1955 Animal communication and the origin of human language;Sci. Prog. 43 385–401
Hamilton W D 1964 The genetical theory of social behaviour, I, II;J. Theor. Biol. 7 1–52
Hess and Boiteaux 1971 Oscillatory phenomena in Biochemistry;Ann. Rev. Biochem. 40 237–258
Higgins J 1967 The theory of oscillating reactionsInd. Eng. Chem. 59 18–62
Ishida S 1980 A mutant ofDictyostelium discoideum capable of differentiating without morphogenesis;Dev. Growth Differ 22 143–152
Kaiser D, Manoil C and Dworkin M 1979 Myxobacteria: cell interactions, genetics and development;Annu. Rev. Microbiol. 33 595–639
Kay R R and Trevan D J 1981Dictyostelium amoebae can differentiate into spores without cell-to-cell contact;J. Embryol. Exp. Morphol. 62 369–378
Keating M T and Bonner J T 1977 Negative chemotaxis in cellular slime molds;J. Bacteriol. 130 144–147
Kessin R H 1977 Mutations causing rapid development inDictyostelium discoideum;Cell 10 703–708
Lokeshwar B L 1983A quantitative study of spatial patterning in the cellular slime mold Dictyostelium discoideum, Ph.D. Thesis, Indian Institute of Science, Bangalore
Lokeshwar B L and Nanjundiah V 1983 Tip regeneration and positional information in the slug ofDictyostelium discoideum;J. Embryol. Exp. Morphol. 73 151–162
Lokeshwar B L and Nanjundiah V 1985 Intercellular communication in the multicellular stages ofDictyostelium discoideum; Differentiation (in press)
Loomis W F 1975Dictyostelium discoideum: a developmental system (New York: Academic Press)
Loomis W F 1982The development of Dictyostelium discoideum (New York: Academic Press)
McRobbie S J and Newell P C 1983 Changes in actin associated with the cytoskeleton following chemotactic stimulation ofDictyostelium discoideum;Biochem. Biophys. Res. Commun. 115 351–359
Morrissey J H 1983 Two signals to shape a slime mould;Nature (London) 303 203–204
Morrissey J H, Farnsworth P A and Loomis W F 1981 Pattern formation inDictyostelium discoideum: an analysis of mutants altered in cell proportioning;Dev. Biol. 83 1–8
Nanjundiah V 1973 Chemotaxis, signal relaying and aggregation morphologyJ. Theor. Biol. 42 63–105
Nanjundiah V 1976 Signal relay by single cells during wave propagation in a cellular slime mold;J. Theor. Biol. 56 275–282
Nanjundiah V 1978 The evolution of chemical communication; inProceedings of the Workshop on Chemical Evolution, Origin of Life and Evolution of Life Processes (ed) M S Chadha (New Delhi: Insdoc)
Nanjundiah V and Malchow D 1976 A theoretical study of the effects of cyclic AMP phosphodiesterase during aggregation inDictyostelium;J. Cell. Sci. 22 49–58
Newell P C, Longlands M and Sussman M 1971 Control of enzyme synthesis by cellular interaction during development of the cellular slime moldDictyostelium discoideum;J. Mol. Biol. 58 541–554
Newell P C 1977 Aggregation and cell surface receptors in cellular slime molds: inMicrobiol Interactions: Receptors and Recognition, Series B(3) (ed) J L Reissig (London: Chapman and Hall)
Raper K B 1940 Pseudoplasmodium formation and organisation inDictyostelium discoideum;J. Elisha Mitchell Sci. Soc. 56 241–282
Richter P H and Ross J 1981 Concentration oscillations and efficiency: glycolysis;Science 211 715–717
Roos W, Nanjundiah V, Malchow D and Gerisch G 1975 Amplification of cyclic AMP signals in aggregating cells ofDictyostelium discoideum;FEBS Lett. 53 139–142
Schaap P and Wang M 1984 The possible involvement of oscillatory cAMP signalling in multicellular morphogenesis of the cellular slime molds;Dev. Biol. 105 470–478
Schindler J and Sussman M 1977 Ammonia determines the choice of morphogenetic pathways inDictyostelium discoideum;J. Mol. Biol. 116 161–179
Shaffer B M 1957 Aspects of aggregation in cellular slime moulds. I. Orientation and Chemotaxis;Am. Nat. 91 19–35
Shaffer B M 1975 Secretion of cyclic AMP induced by cyclic AMP in the cellular slime moldDictyostelium discoideum;Nature (London) 255 549–552
Stenhouse F O and Williams K L 1977 Patterning inDictyostelium discoideum: the proportions of three differentiated cell types (spore, stalk and basal disc) in the fruiting body;Dev. Biol. 59 140–152
Takeuchi I and Sakai Y 1971 Dedifferentiation of the disaggregated slug cell of the cellular slime moldDictyostelium discoideum;Dev. Growth Differ. 13 201–210
Takeuchi I, Hayashi M and Tasaka M 1977 Cell differentiation and pattern formation inDictyostelium; in “Development and Differentiation in the Cellular Slime Molds” (eds) P Cappuccinelli and J Ashworth (Elsevier)
Waddell D R 1982 A predatory slime mould;Nature (London) 298 464–466
Wilson E O 1975Sociobiology (Harvard: Belknap Press)
Winfree A 1980The Geometry of Biological Time (New York: Springer Verlag)
Wurster B and Bumann J 1981 Cell differentiation in the absence of intracellular cyclic AMP pulses inDictyostelium discoideum;Dev. Biol. 85 262–265
Wurster B and Schubiger K 1977 Oscillations and cell development inDictyostelium discoideum stimulated by folic acid pulses;J. Cell Sci. 27 105–114
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Nanjundiah, V. The evolution of communication and social behaviour inDictyostelium discoideum . Proc Ani Sci 94, 639–653 (1985). https://doi.org/10.1007/BF03191865
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DOI: https://doi.org/10.1007/BF03191865