The costs and benefits of flexibility as an expression of behavioural plasticity: a primate perspective

Abstract

Traditional neo-Darwinism ascribes geographical variation in morphology or in behaviour to varying selection on local genotypes. However, mobile and long-lived organisms cannot achieve local adaptation this way, leading to a renewed interest in plasticity. I examined geographical variation in orang-utan subsistence and social behaviour, and found this to be largely owing to behavioural plasticity, here called flexibility, both in the form of flexible individual decisions and of socially transmitted (cultural) innovations. Although comparison with other species is difficult, the extent of such flexibility is almost certainly limited by brain size. It is shown that brains can only increase relative to body size where the cognitive benefits they produce are reliably translated into improved survival rate. This means that organisms that are very small, face many predators, live in highly seasonal environments, or lack opportunities for social learning cannot evolve greater flexibility, and must achieve local adaptation through selection on specific genotypes. On the other hand, as body and brain size increase, local adaptation is increasingly achieved through selection on plasticity. The species involved are also generally those that most need it, being more mobile and longer-lived. Although high plasticity buffers against environmental change, the most flexible organisms face a clear limit because they respond slowly to selection. Thus, paradoxically, the largest-brained animals may actually be vulnerable to the more drastic forms of environmental change, such as those induced by human actions.

Taking note of Tinbergen, or: the promise of a biology of behaviour

“…Holekamp et al [9] argue that, in the trade-off between brain size and bite force, the balance has been tipped in favour of the feeding apparatus. The lack of equivalent behavioural flexibility in carnivores as compared with primates, despite often striking similarities in social organization and structure (as is the case for the spotted hyaena) thus supports van Schaik's [38] suggestion that flexibility in social behaviour is ultimately limited by the degree to which brain size expansion is possible within a given lineage.…”

“…Van Schaik [38] makes essentially the same argument as Schradin [34], but approaches the issue from the primate perspective, with an emphasis on brain size evolution. His argument is that flexibility in behaviour is limited by brain size, hence organisms that are small, face high predation, live in seasonal environments or lack opportunities for social learning cannot evolve greater flexibility in behaviour, as large brain size is not favoured by selection.…”

“…Data from orang-utans supports this idea, but also indicates that there can be significant costs: high flexibility buffers apes against environmental change, but also means that these animals respond very slowly to selection because of the constraints introduced by long generation times and slow reproductive turnover; these traits are likely to be strongly detrimental under conditions of drastic environmental change, such as anthropogenic habitat destruction. One can also make a link between van Schaik's [38] argument and Holekamp et al's [9] discussion of the morphological constraints that limit the extent to which the carnivores can undergo brain expansion. Carnivore jaws and skulls are built to resist high stresses and exert strong bite forces.…”

Constraints and flexibility in mammalian social behaviour: introduction and synthesis

“…One fundamental set of constraints is related to the genetic basis of species-specific traits that have evolved and differentiated during recursive rounds of adaptation and speciation over millennia, underpinning advantageous patterns of robustness that may turn into constraints under changing conditions (see also van Schaik [131]). The developmental trajectories of a recently fertilized oocyte of, say an insect, a fish or a mammal differ substantially from each other because of their divergent genetic make-up.…”

“…are linked either to a monogamous or promiscuous mating system with their attendant behavioural consequences [132], reflecting constraints on development in existing species. Similarly, van Schaik [131] argues that species differences in brain size in orangutans are responsible for concomitant differences in behavioural flexibility. The contribution by Holekamp et al [133] suggests instead the existence of ultimately genetic constraints on the course of evolution based on their analysis of adaptations in limb and skull morphology in carnivores and primates.…”