Habitat complexity, brain, and behavior.

More complex brains and behaviors have arisen repeatedly throughout both vertebrate and invertebrate evolution. The challenge is to tease apart the forces underlying such change. In this review, I show how habitat complexity influences both brain and behavior in African cichlid fishes, drawing on examples from primates and birds where appropriate. These species groups share a number of similarities. They exhibit a considerable range of brain to body weight within their group. Often highly visual, the species show a diversity of habitat types, social systems, and cognitive abilities. Phylogenies are well established. In closely-related cichlid fishes from the monophyletic Ectodine clade of Lake Tanganyika, habitat complexity is directly correlated with social variables, including species richness, diversity, and abundance. Total brain size, telencephalic and cerebellar size are positively correlated with habitat complexity. Visual acuity and spatial memory are also enhanced in cichlids living in more complex environments. I speculate that species-specific neural effects of environmental complexity could be the consequence of the corresponding social changes. However, environmental and social forces affect brains differently. Environmental forces exert a broader effect on brain structures than social ones, suggesting either allometric expansion of the brain structures in concert with brain size and/or co-evolution of these structures. To advance our understanding of the mechanism by which habitat complexity affects brain and behavior will require the use of closely-related species, quantification of complexity, hypothesis testing restricting analysis to a single variable and path analyses to explore the order of importance of such variables. We will also need new experimental paradigms exploring the cognitive and survival value of brain and brain structure changes both in the laboratory and in the wild.

Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish.

Complex brains and behaviors have occurred repeatedly within vertebrate classes throughout evolution. What adaptive pressures drive such changes? Both environmental and social features have been implicated in the expansion of select brain structures, particularly the telencephalon. East African cichlid fishes provide a superb opportunity to analyze the social and ecological correlates of neural phenotypes and their evolution. As a result of rapid, recent, and repeated radiations, there are hundreds of closely-related species available for study, with an astonishing diversity in habitat preferences and social behaviors. In this study, we present quantitative ecological, social, and neuroanatomical data for closely-related species from the (monophyletic) Ectodini clade of Lake Tanganyikan cichlid fish. The species differed either in habitat preference or social organization. After accounting for phylogeny with independent contrasts, we find that environmental and social factors differentially affect the brain, with environmental factors showing a broader effect on a range of brain structures compared to social factors. Five out of seven of the brain measures show a relationship with habitat measures. Brain size and cerebellar size are positively correlated with species number (which is correlated with habitat complexity); the medulla and olfactory bulb are negatively correlated with habitat measures. The telencephalon shows a trend toward a positive correlation with rock size. In contrast, only two brain structures, the telencephalon and hypothalamus, are correlated with social factors. Telencephalic size is larger in monogamous species compared to polygamous species, as well as with increased numbers of individuals; monogamy is also associated with smaller hypothalamic size. Our results suggest that selection or drift can act independently on different brain regions as the species diverge into different habitats and social systems.

Mechanisms underlying reorganization of fractured tactile cerebellar maps after deafferentation in developing and adult rats.

Our previous studies showed that fractured tactile cerebellar maps in rats reorganize after deafferentation during development and in adulthood while maintaining a fractured somatotopy. Several months after deafferentation of the infraorbital branch of the trigeminal nerve, the missing upper lip innervation is replaced in the tactile maps in the granule cell layer of crus IIa. The predominant input into the denervated area is always the upper incisor representation. This study examined whether this reorganization was caused by mechanisms intrinsic to the cerebellum or extrinsic, i.e., occurring in somatosensory structures afferent to the cerebellum. We first compared normal and deafferented maps and found that the expansion of the upper incisor is not caused by a preexisting bias in the strength or abundance of upper incisor input in normal animals. We then mapped tactile representations before and immediately after denervation. We found that the pattern of reorganization observed in the cerebellum several months later is not caused by unmasking of a silent or weaker upper incisor representation. Both results indicate that the reorganization is not a result of subsequent growth or sprouting mechanism within the cerebellum itself. Finally, we compared postlesion maps in the cerebellum and the somatosensory cortex. We found that the upper incisor representation significantly expands in both regions and that this expansion is correlated, suggesting that reorganization in the cerebellum is a passive consequence of reorganization in afferent cerebellar pathways. This result has important developmental and functional implications.

Visual acuity, environmental complexity, and social organization in African cichlid fishes.

The authors studied the effects of habitat complexity and social organization on visual acuity in closely related cichlid fishes (the Ectodini clade). The authors quantified habitat complexity among sand, intermediate, and rock habitats using chromatic difference measures (intensity analysis). Visual acuity was measured behaviorally, using optomotor/optokinetic responses to rotating square-wave stimuli. The rock-dwelling Asprotilapia leptura exhibited the best visual ability, compared with the intermediate and sand-dwelling species, Xenotilapia spilotera and Xenotilapia flavipinnis. The authors then compared effects of social organization. The lek-forming, polygamous Enantiopus melanogenys showed better visual acuity than that of the pair-bonding, monogamous X. flavipinnis. The authors' results are the first to demonstrate that species-specific differences in visual acuity are associated with differences in both the physical and social environment.