How does variation in the environment and individual cognition explain the existence of consistent behavioral differences?

Abstract

According to recent studies on animal personalities, the level of behavioral plasticity, which can be viewed as the slope of the behavioral reaction norm, varies among individuals, populations, and species. Still, it is conceptually unclear how the interaction between environmental variation and variation in animal cognition affect the evolution of behavioral plasticity and expression of animal personalities. Here, we (1) use literature to review how environmental variation and individual variation in cognition explain population and individual level expression of behavioral plasticity and (2) draw together empirically yet nontested, conceptual framework to clarify how these factors affect the evolution and expression of individually consistent behavior in nature. The framework is based on simple principles: first, information acquisition requires cognition that is inherently costly to build and maintain. Second, individual differences in animal cognition affect the differences in behavioral flexibility, i.e. the variance around the mean of the behavioral reaction norm, which defines plasticity. Third, along the lines of the evolution of cognition, we predict that environments with moderate variation favor behavioral flexibility. This occurs since in those environments costs of cognition are covered by being able to recognize and use information effectively. Similarly, nonflexible, stereotypic behaviors may be favored in environments that are either invariable or highly variable, since in those environments cognition does not give any benefits to cover the costs or cognition is not able to keep up with environmental change, respectively. If behavioral plasticity develops in response to increasing environmental variability, plasticity should dominate in environments that are moderately variable, and expression of animal personalities and behavioral syndromes may differ between environments. We give suggestions how to test our hypothesis and propose improvements to current behavioral testing protocols in the field of animal personality.

Keywords: Animal personalities; behavioral flexibility; behavioral plasticity; behavioral syndromes; cognition; reaction norm.

Figure 1

(A) Personality trait (here boldness) measured from the same individual in two different contexts: context 1 = feeding context and context 2 = mating context. Boldness has been measured three times in each contexts (black dots), from which one can see behavioral flexibility (dashed line area). Behavioral plasticity between contexts can be seen from the slope of the behavioral reaction norm (dashed arrows). In figure (B), boldness is measured multiple times from two individuals (X and Y, black dots and triangles, respectively) across environmental gradient in one context. Individual X shows higher behavioral flexibility (larger dashed line area) but similar plasticity (dashed arrows) compared with individual Y. Because individual X has higher flexibility, its behavioral plasticity could be considerably higher across some other environmental gradient, where this kind of plasticity would be adaptive. However, individual Y would still show similar, restricted plasticity, because of its limited potential for flexibility. Reaction norm from individual Y can be estimated more precisely, since its flexibility is considerably lower. In general, personality exists in cases where flexibility does not exceed consistency (repeatability) so that a behavioral reaction norm can be estimated for any given individual.

Figure 2

Behavioral type-dependent fitness benefits of information usage within and between behavioral types in environments with different environmental variability. In grey area the benefits of cognition exceeds its costs. Therefore, responsive behavioral types (dashed line) with high (H) and low (L) cognitive abilities dominate in these kinds of environments, compared with stereotypic behavioral types (solid lines) that instead dominate in invariable or highly variable environments (i.e. outside grey area). Variation in cognitive abilities within and between behavioral types leads to environment-dependent coexistence of different behavioral types (black area). In the grey area the high plasticity and flexibility in behavior potentially restricts the consistency in behaviors in time and across contexts and therefore, may limit the abundance or affect the expression of animal personalities.