Experimental evolution of prepared learning.

Animals learn some things more easily than others. To explain this so-called prepared learning, investigators commonly appeal to the evolutionary history of stimulus-consequence relationships experienced by a population or species. We offer a simple model that formalizes this long-standing hypothesis. The key variable in our model is the statistical reliability of the association between stimulus, action, and consequence. We use experimental evolution to test this hypothesis in populations of Drosophila. We systematically manipulated the reliability of two types of experience (the pairing of the aversive chemical quinine with color or with odor). Following 40 generations of evolution, data from learning assays support our basic prediction: Changes in learning abilities track the reliability of associations during a population's selective history. In populations where, for example, quinine-color pairings were unreliable but quinine-odor pairings were reliable, we find increased sensitivity to learning the quinine-odor experience and reduced sensitivity to learning quinine-color. To the best of our knowledge this is the first experimental demonstration of the evolution of prepared learning.

Why not lie? Costs enforce honesty in an experimental signalling game.

Communication depends on reliability. Yet, the existence of stable honest signalling presents an evolutionary puzzle. Why should animals signal honestly in the face of a conflict of interest? While students of animal signalling have offered several theoretical answers to this puzzle, the most widely studied model, commonly called the 'handicap principle', postulates that the costs of signals stabilize honesty. This model is the motivating force behind an enormous research enterprise that explores signal costs--whether they are physiological, immunological, neural, developmental or caloric. While there can be no question that many signals are costly, we lack definitive experimental evidence demonstrating that costs stabilize honesty. This study presents a laboratory signalling game using blue jays (Cyanocitta cristata) that provides, to our knowledge, the first experimental evidence showing honesty persists when costs are high and disappears when costs are low.

Subjective costs drive overly patient foraging strategies in rats on an intertemporal foraging task.

Laboratory studies of decision making often take the form of two-alternative, forced-choice paradigms. In natural settings, however, many decision problems arise as stay/go choices. We designed a foraging task to test intertemporal decision making in rats via stay/go decisions. Subjects did not follow the rate-maximizing strategy of choosing only food items associated with short delays. Instead, rats were often willing to wait for surprisingly long periods, and consequently earned a lower rate of food intake than they might have by ignoring long-delay options. We tested whether foraging theory or delay discounting models predicted the behavior we observed but found that these models could not account for the strategies subjects selected. Subjects' behavior was well accounted for by a model that incorporated a cost for rejecting potential food items. Interestingly, subjects' cost sensitivity was proportional to environmental richness. These findings are at odds with traditional normative accounts of decision making but are consistent with retrospective considerations having a deleterious influence on decisions (as in the "sunk-cost" effect). More broadly, these findings highlight the utility of complementing existing assays of decision making with tasks that mimic more natural decision topologies.

Tracking a changing environment: optimal sampling, adaptive memory and overnight effects.

Foraging in a variable environment presents a classic problem of decision making with incomplete information. Animals must track the changing environment, remember the best options and make choices accordingly. While several experimental studies have explored the idea that sampling behavior reflects the amount of environmental change, we take the next logical step in asking how change influences memory. We explore the hypothesis that memory length should be tied to the ecological relevance and the value of the information learned, and that environmental change is a key determinant of the value of memory. We use a dynamic programming model to confirm our predictions and then test memory length in a factorial experiment. In our experimental situation we manipulate rates of change in a simple foraging task for blue jays over a 36 h period. After jays experienced an experimentally determined change regime, we tested them at a range of retention intervals, from 1 to 72 h. Manipulated rates of change influenced learning and sampling rates: subjects sampled more and learned more quickly in the high change condition. Tests of retention revealed significant interactions between retention interval and the experienced rate of change. We observed a striking and surprising difference between the high and low change treatments at the 24h retention interval. In agreement with earlier work we find that a circadian retention interval is special, but we find that the extent of this 'specialness' depends on the subject's prior experience of environmental change. Specifically, experienced rates of change seem to influence how subjects balance recent information against past experience in a way that interacts with the passage of time.

Components of change in the evolution of learning and unlearned preference.

Several phenomena in animal learning seem to call for evolutionary explanations, such as patterns of what animals learn and do not learn. While several models consider how evolution should influence learning, we have very little data testing these models. Theorists agree that environmental change is a central factor in the evolution of learning. We describe a mathematical model and an experiment, testing two components of change: reliability of experience and predictability of the best action. Using replicate populations of Drosophila we varied statistical patterns of change across 30 generations. Our results provide the first experimental demonstration that some types of environmental change favour learning while others select against it, giving the first experimental support for a more nuanced interpretation of the selective factors influencing the evolution of learning.

Why do animals make better choices in patch-leaving problems?

This study compares two procedures for the study of choices that differ in time and amount, namely the self-control and patch procedures. The self-control procedure offers animals a binary mutually exclusive choice between a smaller-sooner and larger-later option. This procedure dominates the choice literature. It seems to address the idea of choice in a general, but relatively abstract way. Animals in the self-control situation frequently prefer the smaller-sooner option even when the larger-later option yields a higher long-term intake rate. In contrast, the patch procedure poses an economically similar question, but simulates the naturally occurring problem of patch exploitation. In the patch procedure, animals choose between leaving and staying. Emerging evidence suggests that animals perform better and achieve higher long-term intake rates in the patch situation. This observation raises the question of how a single set of choice mechanisms could produce these different outcomes. The experiment presented here tests two hypotheses about the relationship between the patch and self-control situations. First, it asks whether the short-term rate rule can predict choice behavior in both situations. Second, it tests the second-delivery hypothesis which holds that the patch situation favors choosing the larger more delayed option (staying) because this option ultimately leads to two food deliveries. The results of this experiment convincingly reject both of these hypotheses. Indeed, our results suggest that none of the simple rules based on time and amount can explain the observed differences between the patch and self-control situations. This result challenges the generality of existing models of choice.

Decision ecology: foraging and the ecology of animal decision making.

In this article, I review the approach taken by behavioral ecologists to the study of animal foraging behavior and explore connections with general analyses of decision making. I use the example of patch exploitation decisions in this article in order to develop several key points about the properties of naturally occurring foraging decisions. First, I argue that experimental preparations based on binary, mutually exclusive choice are not good models of foraging decisions. Instead, foraging choices have a sequential foreground-background structure, in which one option is in the background of all other options. Second, behavioral ecologists view foraging as a hierarchy of decisions that range from habitat selection to food choice. Finally, data suggest that foraging animals are sensitive to several important trade-offs. These trade-offs include the effects of competitors and group mates, as well as the problem of predator avoidance.

Effects of temporal clumping and payoff accumulation on impulsiveness and cooperation.

Animals show impulsiveness when they prefer a smaller more immediate option, even though a larger more delayed option produces a higher intake rate. This impulsive behavior has implications for several behavioral problems including social cooperation. This paper presents two experiments using captive blue jays (Cyanocitta cristata) that consider the effects of payoff accumulation and temporal clumping on impulsiveness and cooperation. Payoff accumulation refers to a situation where the benefits gained from each choice trial accumulate from one trial to the next, and only become available to the animal after it has completed a fixed number of trials. We hypothesized that this would reduce impulsiveness because it removes the advantage of quickly realizing food gains. Clumping refers to situation in which the animal experiences several choice trials in quick succession followed by a long pause before the next clump. We hypothesized that if payoffs accumulated over a clump of trials this would enhance the effect of accumulation. We tested the effects of accumulation and clumping on impulsiveness in a self-control situation. We found a significant interaction between clumping and accumulation. Payoff accumulation reduced impulsiveness, but only when trials were clumped. Post hoc analyses suggest that clumping alone increases impulsiveness. A second experiment applied these results to cooperation. This experiment reveals an interaction between payoff accumulation and trial's position within the clump. Jays were more likely to cooperate on the first trial of a clump, but the likelihood of cooperation dropped after the first trial. However, this drop was larger when payoffs did not accumulate. This observation suggests that the difference between accumulated and un-accumulated treatments that we reported previously may be largely due to differences in how animals behave in the first trial of a clump.

Information and its use by animals in evolutionary ecology.

Information is a crucial currency for animals from both a behavioural and evolutionary perspective. Adaptive behaviour relies upon accurate estimation of relevant ecological parameters; the better informed an individual, the better it can develop and adjust its behaviour to meet the demands of a variable world. Here, we focus on the burgeoning interest in the impact of ecological uncertainty on adaptation, and the means by which it can be reduced by gathering information, from both 'passive' and 'responsive' sources. Our overview demonstrates the value of adopting an explicitly informational approach, and highlights the components that one needs to develop useful approaches to studying information use by animals. We propose a quantitative framework, based on statistical decision theory, for analysing animal information use in evolutionary ecology. Our purpose is to promote an integrative approach to studying information use by animals, which is itself integral to adaptive animal behaviour and organismal biology.

Impulsiveness without discounting: the ecological rationality hypothesis.

Observed animal impulsiveness challenges ideas from foraging theory about the fitness value of food rewards, and may play a role in important behavioural phenomena such as cooperation and addiction. Behavioural ecologists usually invoke temporal discounting to explain the evolution of animal impulsiveness. According to the discounting hypothesis, delay reduces the fitness value of the delayed food. We develop an alternative model for the evolution of impulsiveness that does not require discounting. We show that impulsive or short-sighted rules can maximize long-term rates of food intake. The advantages of impulsive rules come from two sources. First, naturally occurring choices have a foreground-background structure that reduces the long-term cost of impulsiveness. Second, impulsive rules have a discrimination advantage because they tend to compare smaller quantities. Discounting contributes little to this result. Although we find that impulsive rules are optimal in a simple foreground-background choice situation in the absence of discounting, in contrast we do not find comparable impulsiveness in binary choice situations even when there is strong discounting.

Discrimination, discounting and impulsivity: a role for an informational constraint.

Feeding animals often prefer small, quickly delivered rewards over larger, more delayed rewards. Students of feeding behaviour typically explain this behaviour by saying that animals discount delayed benefits. Temporal discounting implies that delayed benefits are worth less than immediate benefits. This paper presents a new explanation of short-sighted decision-making called the discrimination advantage model that does not rely on discounting. A new model that includes several possible causes of discounting is developed. This model has many interesting features, but it cannot account for two empirical results: the strength of the 'discounting' effect and the fact that the time between choice presentations (the intertrial interval or ITI) has no effect. This leads to the conclusion that although discounting may be important it is probably not a complete explanation of the experimental facts. In the discrimination advantage model the observation that the ITI does not affect choice is seen as a strategy to make a cleaner discrimination between delayed alternatives in a noisy world. A simple example shows that when discrimination is imperfect a short-sighted choice rule can, in some situations, lead to a higher long-term rate than a rule that actually compares long-term rates. This idea is developed and extended in several ways.