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Sherry is at the Dept of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C2, Lucia F. Jacobs is at the Dept of Biology, University of Utah, Salt Lake City, UT84112, USA, and Steven J. C. 6aulin is at the Dept of Anthropology, University of Pittsburgh, Pittsburgh, PA 15260, USA. Spatialmemory andadaptive specialization of the hippocampus David F. Sherry, Lucia F. Jacobs and Steven J. C. Gaulin The hippocampus plays an important role in spatial memory and spatial cognition in birds and mammals. Natural selection, sexual selection and artificial selec- tion have resulted in an increase in the size of the hippocampus in a remarkably diverse group of animals that rely on spatial abilities to solve ecologically important problems. Food-storing birds remember the locations of large numbers of scattered caches. P olygyn- ous male voles traverse large home ranges in search of mates. Kangaroo rats both cachefood and exhibit a sex difference in home range size. In all of these species, an increase in the size of the hippocampus is associated with superior spatial ability. Artificial selection for homing ability has produced a comparable increase in the size of the hippocampus in homing pigeons, com- pared with other strains of domestic pigeon. Despite differences among these animals in their histories of selection and the genetic backgrounds on which selec- tion has acted, there is a common relationship between relative hippocampal size and spatial ability. Natural selection produces changes in behavior and in the brain that make animals better adapted to the environment in which they live. However, identifying evolutionary adaptations and attributing them unam- biguously to the action of natural selection is not always easy. The vertebrate brain provides a good example. Its structure has changed enormously over an evolutionary timespan, but it can be difficult to determine precisely what selective forces have acted on it, and which of its features are adaptations and which are non-adaptive consequences of evolutionary change. Comparative methods exist, however, for dis- covering whether a seemingly adaptive feature occurs consistently in the presence of the same selective pressure 1, and these techniques can be used to analyse evolutionary change in the brain. If a particu- lar neuroanatomical feature occurs in different animals exposed to the same selective pressure, and is better accounted for by this selective pressure than by the phylogenetic relations among the species, then it is reasonable to conclude that the feature is indeed an adaptation - the result of convergent evolution in response to natural selection. This review is primarily concerned with adaptive modifications of the hippocampus that occur in food- storing birds and polygynous male rodents, and with similar modifications produced by artificial selection in domesticated pigeons. Memory and the hippocampus in food-storing birds Black-capped chickadees, and most other chick- adees and tits in the family Paridae, store food in cache sites scattered through their home range. They store only one food item per cache and never reuse the same cache site. They can create several hundred caches of seeds, nuts and invertebrate prey in a typical winter's day, and retrieve their stored food after a few days by remembering the precise spatial locations of their caches, as shown in a variety of experimental studies (for recent reviews see Refs 2, 3). Cache recovery by black-capped chickadees is disrupted by aspiration lesions of the hippocampus, without any obvious effect on caching, feeding or other behavior4 (Fig. 1). Birds possess a hippocampal complex, comprising the hippocampus and area para- hippocampalis, that has little anatomical resemblance to the mammalian hippocampus (Fig. 2). However, the avian hippocampal complex is homologous with the mammalian hippocampus both ontogenetically5 and neuroanatomically 6'7. Hippocampal lesions in chickadees also disrupt their ability to solve spatial problems unrelated to food storing, and produce deficits in working memory 8 on both spatial and non- spatial tasks. Comparative studies. In addition to chickadees, two other groups of passerine birds regularly store food: nuthatches (in the family Sittidae) and jays (in the family Corvidae). Comparison of the size of the hippocampus in North American representatives of these three food-storing families with that of the hippocampus in ten non-food-storing North American families and subfamilies shows that food storers possess a hippocampus more than twice the size expected for birds of their telencephalon size and body weight 9 (Fig. 3). A similar comparison of European representatives of the three food-storing 298 © 1992, Elsevier Science Publishers Ltd, (UK) TINS, Vol. 15, No. 8, 1992