How Can We Study the Evolution of Animal Minds?

Abstract

During the last 50 years, comparative cognition and neurosciences have improved our understanding of animal minds while evolutionary ecology has revealed how selection acts on traits through evolutionary time. We describe how cognition can be subject to natural selection like any other biological trait and how this evolutionary approach can be used to understand the evolution of animal cognition. We recount how comparative and fitness methods have been used to understand the evolution of cognition and outline how these approaches could extend our understanding of cognition. The fitness approach, in particular, offers unprecedented opportunities to study the evolutionary mechanisms responsible for variation in cognition within species and could allow us to investigate both proximate (i.e., neural and developmental) and ultimate (i.e., ecological and evolutionary) underpinnings of animal cognition together. We highlight recent studies that have successfully shown that cognitive traits can be under selection, in particular by linking individual variation in cognition to fitness. To bridge the gap between cognitive variation and fitness consequences and to better understand why and how selection can occur on cognition, we end this review by proposing a more integrative approach to study contemporary selection on cognitive traits combining socio-ecological data, minimally invasive neuroscience methods and measurement of ecologically relevant behaviors linked to fitness. Our overall goal in this review is to build a bridge between cognitive neuroscientists and evolutionary biologists, illustrate how their research could be complementary, and encourage evolutionary ecologists to include explicit attention to cognitive processes in their studies of behavior.

Keywords: brood parasites; cognitive ecology; fitness cost; heredity; individual differences; natural selection; path analysis.

FIGURE 1

Mate choice and cognitive capacities that could hypothetically play a role. In bi-parental breeding songbirds, choosing an appropriate mate according to available male stock, previous breeding experience and actual environmental conditions is a behavior that will have drastic fitness consequences for any female and that is likely to rely on the interplay between various cognitive functions. Recognition of ornaments linked to different male qualities (e.g., good genes, parental care, nest defense, etc.) uses perception (visual and auditory) to detect male signals and categorization to group and identify male quality according to their ornaments (1). The use of previous breeding experience relies on past learning linking male ornaments and reproductive success from previous experiences (2). Mate choice itself, integrates all information available to the female including current ecology, mate options, and past experience supposedly through decision-making mechanisms (3). Finding the chosen mate, once the decision has been taken, probably relies on spatial memory to relocate the territory defended by the chosen male and endogenous attention to detect the chosen male from among the background of other males and environmental features (4).

FIGURE 2

How to study brain and cognition selection? Ideal studies looking at contemporary selection on neurocognitive traits should integrate socio-ecological conditions (left), neurocognitive traits (middle left), ecologically relevant behaviors (middle right), and fitness (right) variables. Such an approach seeks to truly merge behavioral and evolutionary (green background) and cognitive neuroscience (yellow background) methods. As examples: Socio-ecological contexts of selection could correspond to natural gradients in sociality (i.e., Population density, gregariousness), habitat quality (i.e., level of fragmentation, urbanization) and/or distribution of resources (i.e., harshness of the environment). Experimental manipulations of ecological factors, such as variation in food supplementation or reintroduction in a novel environment, are of particular interest to isolate ecological causes of selection. Cognitive abilities can be measured in the wild using automated foraging tasks. Such methods rely on individual identification usually mediated by passive integrated transponders (PIT) tags. However, some cognitive functions are difficult to measure in the wild and one may want to have a better control on motivational state and environmental parameters. Short-term periods of captivity seem appropriate in such a framework and potentially enable us to use current psychophysics protocols and equipment developed in comparative cognition labs. Development of embedded cameras or microphones has the potential to reveal spontaneous cognitive capabilities like tool use, social cognition or vocal communication. Likewise, neurologgers or transmitters enable us to measure brain activity (electroencephalogram, single unit activity) in free ranging wild animals. Spatial and whole brain measurement could also be assessed using MRI or PET devices in short term scanning protocol. Ecologically relevant behaviors linked to fitness such as parental care, mate choice, foraging, predator avoidance, should be measured to evaluate interactions between agents of selection and between cognitive abilities that are hypothesized to underlie these behaviors. The fitness benefit is traditionally assessed through evaluation of reproductive success (number of offspring who breed) or a measure of survival. Behavior associated with reproductive success (i.e., mating, number of offspring born, parental care) can also be used as proxies of fitness.

FIGURE 3

Mapping the relationship between traits and how selection acts on cognition: a path approach. Schematic example of a generic, hypothetical path analysis linking fitness (number of babies) that depends on two behaviors (parental care and territory defense), which in turn are dependent on a number of cognitive abilities. Arrows show the direction in which selection acts with solid arrows showing a positive relationship and dashed arrows a negative relationship and the thickness of arrows represents the strength of the relationship (partial correlation coefficient). Note that the direction opposite the arrows should indicate effects that underlie the above measure; for example, Cog1 plays an important role in the expression of Behav1. In this example, each behavior is linked to a number of cognitive abilities, but in different ways. Each behavior is linked to one cognitive ability that is only associated with that one behavior (Cog1 and Cog5), but also three other cognitive abilities that are also linked to both behaviors (Cog2–4). Cognitive traits that influence both behaviors show different patterns: attention (Cog 2, 3) shows opposite patterns between the two behaviors whereas memory (Cog4) has a positive relationship with both behaviors. The resulting selection and evolutionary dynamics will reflect these patterns: intense positive selection on memory, but more muted selection on attention. Path models can also estimate the relationship between traits such as the negative relationship we illustrate here as a double headed arrow (correlation with no causation implied) between parental care behavior and territory defense often thought to be antagonistic due to the effects of testosterone on each behavior.