Expression and localization of neuronal nitric oxide synthase in the brain and sensory tissues of the African cichlid fish Astatotilapia burtoni.

Nitric oxide (NO) produced by the enzyme neuronal nitric oxide synthase serves as an important neurotransmitter in the central nervous system that is involved in reproductive regulation, learning, sensory processing, and other forms of neural plasticity. Here, we map the distribution of nnos-expressing cells in the brain and retina of the cichlid fish Astatotilapia burtoni using in situ hybridization. In the brain, nnos-expressing cells are found from the olfactory bulbs to the hindbrain, including within specific nuclei involved in decision-making, sensory processing, neuroendocrine regulation, and the expression of social behaviors. In the retina, nnos-expressing cells are found in the inner nuclear layer, presumably in amacrine cells. We also used quantitative PCR to test for differences in nnos expression within the eye and olfactory bulbs of males and females of different reproductive states and social statuses. In the eye, males express more nnos than females, and socially dominant males express more nnos than subordinate males, but expression did not differ among female reproductive states. In the olfactory bulbs, dominant males had greater nnos expression than subordinate males. These results suggest a status-specific function for NO signaling in the visual and olfactory systems that may be important for sensory perception related to mating or territorial interactions to maintain the social hierarchy. The widespread distribution of nnos-expressing cells throughout the cichlid brain is similar to that in other teleosts, with some conserved localization patterns across vertebrates, suggesting diverse functions for this important neurotransmitter system.

Endocrine and neuroendocrine regulation of social status in cichlid fishes.

Position in a dominance hierarchy profoundly impacts group members' survival, health, and reproductive success. Thus, understanding the mechanisms that regulate or are associated with an individuals' social position is important. Across taxa, various endocrine and neuroendocrine signaling systems are implicated in the control of social rank. Cichlid fishes, with their often-limited resources of food, shelter, and mates that leads to competition, have provided important insights on the proximate and ultimate mechanisms related to establishment and maintenance of dominance hierarchies. Here we review the existing information on the relationships between endocrine (e.g., circulating hormones, gonadal and other tissue measures) and neuroendocrine (e.g., central neuropeptides, biogenic amines, steroids) systems and dominant and subordinate social rank in male cichlids. Much of the current literature is focused on only a few representative cichlids, particularly the African Astatotilapia burtoni, and several other African and Neotropical species. Many hormonal regulators show distinct differences at multiple biological levels between dominant and subordinate males, but generalizations are complicated by variations in experimental paradigms, methodological approaches, and in the reproductive and parental care strategies of the study species. Future studies that capitalize on the diversity of hierarchical structures among cichlids should provide insights towards better understanding the endocrine and neuroendocrine mechanisms contributing to social rank. Further, examination of this topic in cichlids will help reveal the selective pressures driving the evolution of endocrine-related phenotypic traits that may facilitate an individual's ability to acquire and maintain a specific social rank to improve survival and reproductive success.

Variation in the Sensory Space of Three-spined Stickleback Populations.

The peripheral sensory systems, whose morphological attributes help determine the acquisition of distinct types of information, provide a means to quantitatively compare multiple modalities of a species' sensory ecology. We used morphological metrics to characterize multiple sensory modalities-the visual, olfactory, and mechanosensory lateral line sensory systems-for Gasterosteus aculeatus, the three-spined stickleback, to compare how sensory systems vary in animals that evolve in different ecological conditions. We hypothesized that the dimensions of sensory organs and correlations among sensory systems vary in populations adapted to marine and freshwater environments, and have diverged further among freshwater lake-dwelling populations. Our results showed that among environments, fish differed in which senses are relatively elaborated or reduced. When controlling for body length, littoral fish had larger eyes, more neuromasts, and smaller olfactory tissue area than pelagic or marine populations. We also found differences in the direction and magnitude of correlations among sensory systems for populations even within the same habitat type. Our data suggest that populations take different trajectories in how visual, olfactory, and lateral line systems respond to their environment. For the populations we studied, sensory modalities do not conform in a predictable way to the ecological categories we assigned.

The Evolutionary Origin of Associative Learning.

Learning is a widespread ability among animals and, like physical traits, is subject to evolution. But how did learning first arise? What selection pressures and phenotypic preconditions fostered its evolution? Neither the fossil record nor phylogenetic comparative studies provide answers to these questions. Here, we take a novel approach by studying digital organisms in environments that promote the evolution of navigation and associative learning. Starting with a nonlearning sessile ancestor, we evolve multiple populations in four different environments, each consisting of nutrient trails with various layouts. Trail nutrients cue organisms on which direction to follow, provided they evolve to acquire and use those cues. Thus, each organism is tested on how well it navigates a randomly selected trail before reproducing. We find that behavior evolves modularly and in a predictable sequence, where simpler behaviors are necessary precursors for more complex ones. Associative learning is only one of many successful behaviors to evolve, and its origin depends on the environment possessing certain information patterns that organisms can exploit. Environmental patterns that are stable across generations foster the evolution of reflexive behavior, while environmental patterns that vary across generations but remain consistent for periods within an organism's lifetime foster the evolution of learning behavior. Both types of environmental patterns are necessary, since the prior evolution of simple reflexive behaviors provides the building blocks for learning to arise. Finally, we observe that an intrinsic value system evolves alongside behavior and supports associative learning by providing reinforcement for behavior conditioning.

Does humic acid alter visually and chemically guided foraging in stickleback fish?

Sensory systems function under the influence of multiple, interacting environmental properties. When environments change, so may perception through one or more sensory systems, as alterations in transmission properties may change how organisms obtain and use information. Humic acids, a natural and anthropogenically produced class of chemicals, have attributes that may change chemical and visual environments of aquatic animals, potentially with detrimental consequences on their ability to locate necessary resources. Here, we explore how environmental disturbance affects the way threespine sticklebacks (Gasterosteus aculeatus) use visual and olfactory information during foraging. We compared foraging behavior using visual, olfactory, and bimodal (visual and olfactory) information in the presence and absence of humic acids. We found evidence that humic acids reduced olfactory-based food detection. While visual perception was not substantially impaired by humic acids, the visual sense alone did not compensate for the loss of olfactory perception. These findings suggest that a suite of senses still may not be capable of compensating for the loss of information from individual modalities. Thus, senses may react disparately to rapid environmental change, and thereby push species into altered evolutionary trajectories.