Developmental constraints on behavioural flexibility

Abstract

We suggest that variation in mammalian behavioural flexibility not accounted for by current socioecological models may be explained in part by developmental constraints. From our own work, we provide examples of constraints affecting variation in behavioural flexibility, not only among individuals, but also among species and higher taxonomic units. We first implicate organizational maternal effects of androgens in shaping individual differences in aggressive behaviour emitted by female spotted hyaenas throughout the lifespan. We then compare carnivores and primates with respect to their locomotor and craniofacial adaptations. We inquire whether antagonistic selection pressures on the skull might impose differential functional constraints on evolvability of skulls and brains in these two orders, thus ultimately affecting behavioural flexibility in each group. We suggest that, even when carnivores and primates would theoretically benefit from the same adaptations with respect to behavioural flexibility, carnivores may nevertheless exhibit less behavioural flexibility than primates because of constraints imposed by past adaptations in the morphology of the limbs and skull. Phylogenetic analysis consistent with this idea suggests greater evolutionary lability in relative brain size within families of primates than carnivores. Thus, consideration of developmental constraints may help elucidate variation in mammalian behavioural flexibility.

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

“…In addition, Sachser et al's [29] finding that these effects are a feature of adolescence and not simply the pre-and early post-natal periods shows how adaptive adjustment can be quite finely tuned. In similar fashion, Faulkes & Bennett [12] trace the neurobiological and developmental underpinnings of the mole-rat adaptation to arid environments and, like Sachser et al [29] and Holekamp et al [9], provide an exemplary case study of the value of a fully integrative approach. Runcie et al [15] add to this by showing how an integrative, developmentally oriented approach can help explain individual differences in baboon behaviour, via an exploration of gene  environment interactions (GEIs).…”

“…Both Sachser et al [29] and Holekamp et al [9] demonstrate the influence of social factors with respect to epigenetic effects, exemplifying this integrative approach, and illustrating its scope: guinea pigs and hyaenas are very different kinds of creatures, but social influences-most notably those of mothers-produce long-lasting effects on offspring development and behavioural responses as adults; their studies highlight how particular kinds of social stressors can produce adaptive developmental plasticity with respect to prevailing or future environmental conditions. In addition, Sachser et al's [29] finding that these effects are a feature of adolescence and not simply the pre-and early post-natal periods shows how adaptive adjustment can be quite finely tuned.…”

“…As noted above, technological and methodological innovations are in large part responsible for presenting these new opportunities, and behavioural researchers have been swift to apply these techniques and reap the benefits. Consequently, it is becoming increasingly clear that, as Holekamp et al [9] note, a developmental perspective helps to bridge the gap between proximate and ultimate explanations-the traditional focus of behavioural researchers-because it draws our attention to the origins and adaptive value of behavioural variation, so enabling a better understanding of the range of phenotypes available to selection. By the same token, the addition of ontogeny naturally brings in the phylogenetic level of explanation; we are beginning to appreciate more fully how significant evolutionary change may be brought about by small changes in gene regulatory mechanisms, and the manner in which these cascade throughout development to produce large changes in the phenotypic characteristics that are visible to selection [30].…”

“…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.…”

“…Any expansion in brain volume thus impinges on available muscle area within the zygomatic arches, and reduces the maximal bite force possible. 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.…”