A non-adaptationist hypothesis of play behaviour

J Physiol. 2023 Sep 1. doi: 10.1113/JP284413. Online ahead of print.

Abstract

Play is a suite of apparently non-functional, pleasurable behaviours observed in human and non-human animals. Although the phenomenon has been studied extensively, no adaptationist behavioural theory of how play evolved can be supported by the available evidence. However, the advancement of the extended evolutionary synthesis and developments in systems biology offer alternative avenues for non-adaptationist physiological hypotheses. I therefore propose a hypothesis of play, based upon a complex ACh activity that is under agential control of the organism, whereby play initiates ACh-mediated feedforward and feedback processes which act to: (i) regulate metabolic processes; (ii) form new ACh receptors via ACh mRNA activity; (iii) mediate attention, memory consolidation and learning; and (iv) mediate social behaviours, reproduction and embryonic development. However, play occurs across taxa, but does not occur across all taxonomic groups or within all species of a taxonomic group. Thus, to support the validity of the proposed hypothesis, I further propose potential explanations for this anomaly, which include sampling and observer biases, altricial versus precocial juvenile development, and the influence of habitat niche and environmental conditions on behaviour. The proposed hypothesis thus offers new avenues for study in both the biological and social sciences, in addition to having potential applications in applied sciences, such as animal welfare and biomedical research. Crucially, it is hoped that this hypothesis will promote further study of a valid and behaviourally significant, yet currently enigmatic, biological phenomenon.

Keywords: acetylcholine; agency; animal behaviour; cholinergic system; extended evolutionary synthesis; play behaviour.

Publication types

  • Review