Symbiotic physiology promotes homeostasis in Daisyworld

Richard A. Boyle, Timothy M. Lenton, Andrew J. Watson

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14 Citations (Scopus)


A connection is hypothesized between the physiological consequences of mutualistic symbiosis and life's average long-term impact on certain highly biologically conserved environmental variables. This hypothesis is developed analytically and with a variant of the Daisyworld model. Biological homeostasis is frequently effective due to co-ordination between opposing physiological “rein” functions, which buffer an organism in response to an external (often environmental) perturbation. It is proposed that during evolutionary history the pooling of different species' physiological functions in mutualistic symbioses increased the range of suboptimal environmental conditions that could be buffered against—a mutual tolerance benefit sometimes sufficient to outweigh the cost of cooperation. A related argument is that for a small number of biologically-crucial physical variables (i) the difference between organism interiors and the life-environment interface is relatively low, and (ii) the biologically optimum level of that variable is relatively highly conserved across different species. For such variables, symbiosis tends to cause (at a cost) an increase in the number of environmental buffering functions per unit of selection, which in turn biases the overall impact of the biota on the state of the variable towards the biological optimum. When a costly but more temperature-tolerant and physiologically versatile symbiosis between one black (warming) and one white (cooling) “daisy” is added to the (otherwise unaltered) Daisyworld parable, four new results emerge: (1) The extension of habitability to a wider luminosity range, (2) resistance to the impact of “cheater” white daisies with cold optima, that derive short-term benefit from environmental destabilisation, (3) the capacity to maintain residual, oscillatory regulation in response to forcings that change more rapidly than allele frequencies and (crucially) (4) “succession”-type dynamics in which the tolerant symbiosis colonises and to an extent makes habitable an otherwise lifeless environment, but is later displaced by free-living genotypes that have higher local fitness once conditions improve. The final result is arguably analogous to lichen colonisation of the Neoproterozoic land surface, followed by the Phanerozoic rise of vascular plants. Caution is necessary in extrapolating from the Daisyworld parable to real ecology/geochemistry, but sufficiently conserved variables may be water potential, macronutrient stoichiometry and (to a lesser extent) the temperature window for metabolic activity.
Original languageEnglish
Pages (from-to)170-182
Number of pages13
JournalJournal of Theoretical Biology
Issue number1
Publication statusPublished - 2011

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