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Response from Crespi: The evolution of social behavior in microorganisms
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interpret as patterns. These patterns emerge because of the existence of gradients of chemicals with which individual molecules and/or cells react. The theoretical basis of emergent properties through self-organization of groups consisting of identical units (dead or alive) can be found in complexity theory3. However, the fact that selforganization underlies complex behavior does not exclude sociality. For example, the complex social behavior of a honeybee Apis mellifera colony is largely governed by selforganizing processes4. The question then becomes whether patterns emerge as epiphenomena (secondary phenomena or characteristics that arise as by-products of something else) through a combination of physical forces and individual properties without having any functional purpose, or whether natural selection acts on the emergent pattern, adapting it for such a purpose5. In the case of physical and chemical systems, no one would argue that these patterns arise because of the underlying interactions of the components that make up the system. So why does this view change as soon as we consider living systems? Crespi’s examples of microbial microfilms, colony structures in E. coli and quorum sensing are clear examples of patterns and structures arising as epiphenomena of nonlinear interactions2,5. However, this does not mean that selective pressures do not have a role. Once these patterns and structures are in place, biological factors can operate as selective agents, maintaining or changing the existing patterns and structures. Spore formation of Dictylostelium spp. is a good example of selection acting on those cells that can reach the spore-forming organ and disperse. But the presence of patterns and structures in itself does not prove the existence of functionality or an adaptive purpose, let alone that a system exhibits social behaviour. It is my strong view that, if we know little or nothing about the adaptive significance of the patterns described by Crespi, we should appreciate that not all we see in nature is adaptive. Madeleine Beekman Schools of Biological Sciences & Mathematics and Statistics, University of Sydney, Sydney, NSW 2006, Australia. e-mail: [email protected] http://tree.trends.com
TRENDS in Ecology & Evolution Vol.16 No.11 November 2001
References 1 Crespi, B.J. (2001) The evolution of social behavior in microorganisms. Trends in Ecol. Evol. 16, 178–183 2 Ball, P. (1999) The Self-made Tapestry. Pattern Formation in Nature, Oxford University Press 3 Haken, H. (1983) Synergetics, an Introduction: Nonequilibrium Phase Transitions and Selforganization in Physics, Chemistry, and Biology, Springer-Verlag 4 Seeley, T.D. (1995) The Wisdom of the Hive, Harvard University Press 5 Parrish, J.K. and Edelstein-Keshet, L. (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284, 99–101
The evolution of social behavior in microorganisms Response from Crespi
The goal of my recent article in TREE1 was to employ the methods of functional design2 and broad scale comparative analysis3 to explore sociality in microorganisms, and thus connect two disciplines, the evolution of social behavior and microbiology, which, traditionally, have remained largely separate. The conclusion of the article was that adaptation has seldom been demonstrated to explain the behavior of microorganisms, although the literature is rife with tantalizing examples of apparently adaptive social phenomena, some of which have important implications for medicine and agriculture. Separating adaptation from either nonadaptation or maladaptation has never been simple4. For microorganisms, the task is made harder by their lilliputian scale, obscure habitats, clonal habits, and phenotypes that involve cell-type differentiation and molecular interactions rather than the more familiar queens and workers of honeybees Apis mellifera or alarm signalling in vervet monkeys Cercopithecus tantalus. Beekman5 suggests that another property of microorganisms, their ability to generate complex patterns as epiphenomena of metabolic, demographic or other processes at the individual level, makes identifying adaptation even more challenging. This suggestion harks back to Darwin6, who noted that many structures ‘have no direct relation to the habits of life of each species’, and to Williams2, who pointed out that some
607
phenomena, such as the structure of fish shoals, might represent emergent effects of individual behavior rather than adaptations per se. Darwin and Williams were undaunted by unexplored complexity and alternatives to adaptation, and neither should we shy from applying convergence and functional design methods to social microbes. The key lies in linking phenotypes with environments and fitness, via observational and experimental analyses of costs and benefits, modeling, identification of parallels across diverse taxa, and recognition of the distinction between proximate and ultimate causes7. Epiphenomena will be rapidly revealed under such a multifaceted assault. What microbial phenotypes remain open to suspicion? Biofilms and quorum sensing each involves secretion of specific molecules under well-defined circumstances, with consequences that apparently benefit the secreting cells1. As such, they are a far cry from selforganizing crystals. Aspects of colony structure in E. coli are indeed more problematic; they have been suggested to be adaptive8,9, but the fitness benefits to colonies in nature have yet to be determined. Without evidence, we must assume neither adaptation nor nonadaptation; instead hypotheses based on each can be tested using the best tools of evolution and microbiology. Bernard J. Crespi Behavioural Ecology Research Group, Department of Biosciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6. References 1 Crespi, B.J. (2001) The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178–183 2 Williams, G.C. (1966) Adaptation and Natural Selection, Princeton University Press 3 Harvey, P.H. and Pagel, M.P. (1991) The Comparative Method in Evolutionary Biology, Oxford University Press 4 Crespi, B.J. (2000) The evolution of maladaptation. Heredity 84, 623–629 5 Beekman, M. (2001) The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 606–607 6 Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, John Murray 7 Sherman, P.W. (1988) The levels of analysis. Anim. Behav. 36, 616–619 8 Ben-Jacob, E. et al. (1998) Cooperative organization of bacterial colonies: from genotype to morphotype. Annu. Rev. Microbiol. 52, 779–806 9 Shapiro, J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104
0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
interpret as patterns. These patterns emerge because of the existence of gradients of chemicals with which individual molecules and/or cells react. The theoretical basis of emergent properties through self-organization of groups consisting of identical units (dead or alive) can be found in complexity theory3. However, the fact that selforganization underlies complex behavior does not exclude sociality. For example, the complex social behavior of a honeybee Apis mellifera colony is largely governed by selforganizing processes4. The question then becomes whether patterns emerge as epiphenomena (secondary phenomena or characteristics that arise as by-products of something else) through a combination of physical forces and individual properties without having any functional purpose, or whether natural selection acts on the emergent pattern, adapting it for such a purpose5. In the case of physical and chemical systems, no one would argue that these patterns arise because of the underlying interactions of the components that make up the system. So why does this view change as soon as we consider living systems? Crespi’s examples of microbial microfilms, colony structures in E. coli and quorum sensing are clear examples of patterns and structures arising as epiphenomena of nonlinear interactions2,5. However, this does not mean that selective pressures do not have a role. Once these patterns and structures are in place, biological factors can operate as selective agents, maintaining or changing the existing patterns and structures. Spore formation of Dictylostelium spp. is a good example of selection acting on those cells that can reach the spore-forming organ and disperse. But the presence of patterns and structures in itself does not prove the existence of functionality or an adaptive purpose, let alone that a system exhibits social behaviour. It is my strong view that, if we know little or nothing about the adaptive significance of the patterns described by Crespi, we should appreciate that not all we see in nature is adaptive. Madeleine Beekman Schools of Biological Sciences & Mathematics and Statistics, University of Sydney, Sydney, NSW 2006, Australia. e-mail: [email protected] http://tree.trends.com
TRENDS in Ecology & Evolution Vol.16 No.11 November 2001
References 1 Crespi, B.J. (2001) The evolution of social behavior in microorganisms. Trends in Ecol. Evol. 16, 178–183 2 Ball, P. (1999) The Self-made Tapestry. Pattern Formation in Nature, Oxford University Press 3 Haken, H. (1983) Synergetics, an Introduction: Nonequilibrium Phase Transitions and Selforganization in Physics, Chemistry, and Biology, Springer-Verlag 4 Seeley, T.D. (1995) The Wisdom of the Hive, Harvard University Press 5 Parrish, J.K. and Edelstein-Keshet, L. (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284, 99–101
The evolution of social behavior in microorganisms Response from Crespi
The goal of my recent article in TREE1 was to employ the methods of functional design2 and broad scale comparative analysis3 to explore sociality in microorganisms, and thus connect two disciplines, the evolution of social behavior and microbiology, which, traditionally, have remained largely separate. The conclusion of the article was that adaptation has seldom been demonstrated to explain the behavior of microorganisms, although the literature is rife with tantalizing examples of apparently adaptive social phenomena, some of which have important implications for medicine and agriculture. Separating adaptation from either nonadaptation or maladaptation has never been simple4. For microorganisms, the task is made harder by their lilliputian scale, obscure habitats, clonal habits, and phenotypes that involve cell-type differentiation and molecular interactions rather than the more familiar queens and workers of honeybees Apis mellifera or alarm signalling in vervet monkeys Cercopithecus tantalus. Beekman5 suggests that another property of microorganisms, their ability to generate complex patterns as epiphenomena of metabolic, demographic or other processes at the individual level, makes identifying adaptation even more challenging. This suggestion harks back to Darwin6, who noted that many structures ‘have no direct relation to the habits of life of each species’, and to Williams2, who pointed out that some
607
phenomena, such as the structure of fish shoals, might represent emergent effects of individual behavior rather than adaptations per se. Darwin and Williams were undaunted by unexplored complexity and alternatives to adaptation, and neither should we shy from applying convergence and functional design methods to social microbes. The key lies in linking phenotypes with environments and fitness, via observational and experimental analyses of costs and benefits, modeling, identification of parallels across diverse taxa, and recognition of the distinction between proximate and ultimate causes7. Epiphenomena will be rapidly revealed under such a multifaceted assault. What microbial phenotypes remain open to suspicion? Biofilms and quorum sensing each involves secretion of specific molecules under well-defined circumstances, with consequences that apparently benefit the secreting cells1. As such, they are a far cry from selforganizing crystals. Aspects of colony structure in E. coli are indeed more problematic; they have been suggested to be adaptive8,9, but the fitness benefits to colonies in nature have yet to be determined. Without evidence, we must assume neither adaptation nor nonadaptation; instead hypotheses based on each can be tested using the best tools of evolution and microbiology. Bernard J. Crespi Behavioural Ecology Research Group, Department of Biosciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6. References 1 Crespi, B.J. (2001) The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178–183 2 Williams, G.C. (1966) Adaptation and Natural Selection, Princeton University Press 3 Harvey, P.H. and Pagel, M.P. (1991) The Comparative Method in Evolutionary Biology, Oxford University Press 4 Crespi, B.J. (2000) The evolution of maladaptation. Heredity 84, 623–629 5 Beekman, M. (2001) The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 606–607 6 Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, John Murray 7 Sherman, P.W. (1988) The levels of analysis. Anim. Behav. 36, 616–619 8 Ben-Jacob, E. et al. (1998) Cooperative organization of bacterial colonies: from genotype to morphotype. Annu. Rev. Microbiol. 52, 779–806 9 Shapiro, J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104
0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.