Reference: Biol. Brr//. 191: 92-100. (August, 1996) The Economy of Winter: Phenotypic Plasticity in Behavior and Brain Structure LUCIA F. JACOBS Department of Psychology, University of California at Berkebv, Berkeley, California 94720-1650 Abstract. Mobile animals must learn the spatial distri- butions of resources. The cost of foraging increases dra- matically for temperate-zone animals during the winter. Two strategies may be used to balance the energetic budget: reducing costs of foraging and reducing need to forage. Both strategies are correlated with changes in brain structure, specifically in the hippocampus, a fore- brain structure used by birds and mammals to map spa- tial distributions of resources. Small mammals that re- duce their need to forage, through hibernation or reduc- tion in body size, show a specific reduction in the structure and size of the hippocampus. The costs of for- aging can be also decreased by migration to better forag- ing conditions or by food-storing, both of which decrease the temporal heterogeneity of food resources. Both of these latter strategies are associated with increased hip- pocampal structure: for food-storing birds, this increase is a seasonal phenomenon. Thus not only behavior, but also learning ability and even brain structures in adult animals, may be phenotypically plastic in response to the changing demands of the environment. Introduction To every thing there is a season, und a time to everypurpose under the heaven. -Ecclesiustes, 3.1 Behavior and neural structure evolve in response to changing environments, not static ones. When interac- tions between the environment and the genotype result Received 19 December 1995; accepted 18 March 1996. This paper was originally presented at a symposium titled Finding Food: Newoethological Aspem ofForaging. The symposium was held at the University of Massachusetts, Amherst, from 6 to 8 October 1995. in a variety of phenotypes, this is called ‘phenotypic plas- ticity’ or “the ability of a single genotype to produce more than one alternative form of morphology, physio- logical state, and/or behavior in response to environ- mental conditions.” (West-Eberhard, 1989). The pheno- type includes “all aspects of an organism other than the genotype, from the enzyme products of the genes to learned behaviors and the effects of disease.” (West-Eb- erhard, 1989). Thus questions of plasticity in behavior and neural structure, usually addressed by the discipline of cognitive neuroscience, or the neural basis of cognitive abilities, may be seen as an example of phenotypic plas- ticity, and fit into the larger framework of evolutionary processes. Behavior is perhaps the most plastic of phenotypic traits, and as such has long been seen as a unique agent of evolutionary change (Wcislo, 1989). The neural bases of behavior, in contrast, are usually considered to be a constraint on the range of behaviors, tethering them to the information-processing capacity of a species’ prede- termined brain size and structure. The idea that both be- havior and brain can change in response to environmen- tal challenge is relatively new. It was first recognized in the extraordinary ability of forebrain nuclei in canaries to add new neurons in advance of the annual breeding season. This dramatic example of adult neurogenesis in response to photoperiod revolutionized our perception of adult brain plasticity (Nottebohm, 1981). Yet it can also be seen simply as phenotypic plasticity: a change in brain phenotype in response to changes in the environ- ment. Environmental cues trigger a change in the brain structure, which is correlated with an increase in behav- ioral plasticity, i.e., the ability to produce nuptial adver- tisement song. The production of song in turn creates more changes in the environment, as females arrive, at- tracted by the song, and as their arrival initiates the breeding process. The production of offspring, and the 92