Trust your gut: using physiological states as a source of information is almost as effective as optimal Bayesian learning

Approaches to understanding adaptive behaviour often assume that animals have perfect information about environmental conditions or are capable of sophisticated learning. If such learning abilities are costly, however, natural selection will favour simpler mechanisms for controlling behaviour when faced with uncertain conditions. Here, we show that, in a foraging context, a strategy based only on current energy reserves often performs almost as well as a Bayesian learning strategy that integrates all previous experiences to form an optimal estimate of environmental conditions. We find that Bayesian learning gives a strong advantage only if fluctuations in the food supply are very strong and reasonably frequent. The performance of both the Bayesian and the reserve-based strategy are more robust to inaccurate knowledge of the temporal pattern of environmental conditions than a strategy that has perfect knowledge about current conditions. Studies assuming Bayesian learning are often accused of being unrealistic; our results suggest that animals can achieve a similar level of performance to Bayesians using much simpler mechanisms based on their physiological state. More broadly, our work suggests that the ability to use internal states as a source of information about recent environmental conditions will have weakened selection for sophisticated learning and decision-making systems.

[1]  K. Evans,et al.  Climate change and annual survival in a temperate passerine: partitioning seasonal effects and predicting future patterns , 2014 .

[2]  A Houston,et al.  The application of statistical decision theory to animal behaviour. , 1980, Journal of theoretical biology.

[3]  The influence of the food–predation trade-off on the foraging behaviour of central-place foragers , 2015, Behavioral Ecology and Sociobiology.

[4]  M. C. Ferrari,et al.  Evolution and behavioural responses to human-induced rapid environmental change , 2011, Evolutionary applications.

[5]  Nicky J Welton,et al.  Acquisition and maintenance costs in the long-term regulation of avian fat reserves , 1997 .

[6]  J. Biernaskie,et al.  Bumblebees Learn to Forage like Bayesians , 2009, The American Naturalist.

[7]  E. Charnov Optimal Foraging: Attack Strategy of a Mantid , 1976, The American Naturalist.

[8]  Pete C. Trimmer,et al.  On the Evolution and Optimality of Mood States , 2013, Behavioral sciences.

[9]  Guy Cowlishaw,et al.  How do foragers decide when to leave a patch? A test of alternative models under natural and experimental conditions. , 2013, The Journal of animal ecology.

[10]  A. Kacelnik,et al.  State-Dependent Decisions Cause Apparent Violations of Rationality in Animal Choice , 2004, PLoS biology.

[11]  S. Lea,et al.  The cognitive mechanisms of optimal sampling , 2012, Behavioural Processes.

[12]  P. Nonacs State dependent behavior and the Marginal Value Theorem , 2001 .

[13]  Alasdair I Houston,et al.  Foraging currencies, metabolism and behavioural routines. , 2014, The Journal of animal ecology.

[14]  I. Cuthill,et al.  The ecological costs of avian fat storage. , 1993, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  A. Sih Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview , 2013, Animal Behaviour.

[16]  Ola Olsson,et al.  Bayes' theorem and its applications in animal behaviour , 2006 .

[17]  J. Hutchinson,et al.  Simple heuristics and rules of thumb: Where psychologists and behavioural biologists might meet , 2005, Behavioural Processes.

[18]  Roderich Groß,et al.  Simple learning rules to cope with changing environments , 2008, Journal of The Royal Society Interface.

[19]  A I Houston,et al.  The ecological rationality of state-dependent valuation. , 2012, Psychological review.

[20]  Daniel Nettle,et al.  The Evolutionary Origins of Mood and Its Disorders , 2012, Current Biology.

[21]  H. Schekkerman,et al.  Mortality of Black-tailed Godwit Limosa limosa and Northern Lapwing Vanellus vanellus chicks in wet grasslands: influence of predation and agriculture , 2008, Journal of Ornithology.

[22]  K. Evans,et al.  Breeding season weather determines long-tailed tit reproductive success through impacts on recruitment , 2015 .

[23]  James A. R. Marshall,et al.  Decision-making under uncertainty: biases and Bayesians , 2011, Animal Cognition.

[24]  P. Trimmer Optimal behaviour can violate the principle of regularity , 2013, Proceedings of the Royal Society B: Biological Sciences.

[25]  A. Houston,et al.  Integrating function and mechanism. , 2009, Trends in ecology & evolution.

[26]  Pete C. Trimmer,et al.  Generalized Optimal Risk Allocation: Foraging and Antipredator Behavior in a Fluctuating Environment , 2012, The American Naturalist.

[27]  P. Todd,et al.  Patch leaving in humans: can a generalist adapt its rules to dispersal of items across patches? , 2008, Animal Behaviour.

[28]  E. Charnov Optimal foraging, the marginal value theorem. , 1976, Theoretical population biology.

[29]  A. Houston,et al.  The value of fat reserves and the tradeoff between starvation and predation , 1990, Acta biotheoretica.

[30]  M. C. Ferrari,et al.  The paradox of risk allocation: a review and prospectus , 2009, Animal Behaviour.

[31]  R. Ydenberg Great tits and giving-up times: decision rules for leaving patches , 1984 .

[32]  D. Stephens Change, regularity, and value in the evolution of animal learning , 1991 .

[33]  J. M. Smith,et al.  Optimality theory in evolutionary biology , 1990, Nature.

[34]  Luc-Alain Giraldeau,et al.  Finding the evolutionarily stable learning rule for frequency-dependent foraging , 2009, Animal Behaviour.

[35]  Dave Goulson,et al.  Why do pollinators visit proportionally fewer flowers in large patches , 2000 .

[36]  J. Bowers,et al.  Bayesian just-so stories in psychology and neuroscience. , 2012, Psychological bulletin.

[38]  P. Taylor,et al.  Test of optimal sampling by foraging great tits , 1978 .

[39]  Graham H. Pyke,et al.  Optimal Foraging: A Selective Review of Theory and Tests , 1977, The Quarterly Review of Biology.

[40]  D. Stephens,et al.  Components of change in the evolution of learning and unlearned preference , 2009, Proceedings of the Royal Society B: Biological Sciences.

[41]  Alexander Lange,et al.  Bayesian Approximations and Extensions: Optimal Decisions for Small Brains and Possibly Big Ones Too , 2022 .

[42]  James A. R. Marshall,et al.  Does natural selection favour the Rescorla-Wagner rule? , 2012, Journal of theoretical biology.

[43]  L. Giraldeau,et al.  Exposing the behavioral gambit: the evolution of learning and decision rules , 2013 .

[44]  Andrew L. Nevai,et al.  State-dependent choice and ecological rationality. , 2007, Journal of theoretical biology.

[45]  A. Houston,et al.  Violations of transitivity under fitness maximization , 2007, Biology Letters.

[46]  Pete C. Trimmer,et al.  The evolution of decision rules in complex environments , 2014, Trends in Cognitive Sciences.

[47]  M. Mangel,et al.  Effects of the Emotion System on Adaptive Behavior , 2013, The American Naturalist.

[48]  Foraging in a patchy environment by a predatory net-spinning caddis larva: A test of optimal foraging theory , 2004, Oecologia.

[49]  Thomas J. Valone,et al.  Are animals capable of Bayesian updating? An empirical review , 2006 .