Social Dominance and Serotonin Receptor Genes in Crayfish

Gene expression affects social behavior only through changes in the excitabilities of neural circuits that govern the release of the relevant motor programs. In turn, social behavior affects gene expression only through patterns of sensory stimulation that produce significant activation of relevant portions of the nervous system. In crayfish, social interactions between pairs of animals lead to changes in behavior that mark the formation of a dominance hierarchy. Those changes in behavior result from changes in the excitability of specific neural circuits. In the new subordinate, circuits for offensive behavior become less excitable and those for defensive behavior become more excitable. Serotonin, which is implicated in mechanisms for social dominance in many animals, modulates circuits for escape and avoidance responses in crayfish. The modulatory effects of serotonin on the escape circuits have been found to change with social dominance, becoming excitatory in dominant crayfish and inhibitory in subordinates. These changes in serotonin's effects on escape affect the synaptic response to sensory input of a single cell, the lateral giant (LG) command neuron for escape. Moreover, these changes occur over a 2‐week period and for the subordinate are reversible at any time following a reversal of the animal's status. The results have suggested that a persistent change in social status leads to a gradual change in the expression of serotonin receptors to a pattern that is more appropriate for the new status. To test that hypothesis, the expression patterns of crayfish serotonin receptors must be compared in dominant and subordinate animals. Two of potentially five serotonin receptors in crayfish have been cloned, sequenced, and pharmacologically characterized. Measurements of receptor expression in the whole CNS of dominant and subordinate crayfish have produced inconclusive results, probably because each receptor is widespread in the nervous system and is likely to experience opposite expression changes in different areas of the CNS. Both receptors have recently been found in identified neurons that mediate escape responses, and so the next step will be to measure their expression in these identified cells in dominant and subordinate animals.

Introduction

The struggle for survival and reproductive success that Darwin described is often most intense among members of the same species, all of whom are competing for the same resources within the same niche. This competition for food, shelter, and mating opportunities can become violent, but social animals have developed a variety of behavioral mechanisms to minimize violence. Among the most important of these is the social dominance hierarchy that is usually established through agonistic interactions. Once established, the hierarchy enables the participating animals to divide resources relatively peacefully, if unevenly (Wilson, 1975). This spares them from fighting and the chance of injury that for most animals in the wild leads directly to death.

The neural and neuroendocrine mechanisms that underlie social dominance are not well understood for any animal, in part because they include dynamic interactions within and between systems at all levels, from gene expression to social interactions (Fig. 1). These interactions form loops, such that cause and effect become indistinct. For example, a new social interaction (“World,” Fig. 1) will trigger sensory excitation, central activity, new motor patterns, and a behavioral response on a short timescale. The neural responses will also feed back to modify neural circuit function and structure through rapid mechanisms of plasticity and modify patterns of gene expression through slower mechanisms. New patterns of gene expression can promote structural changes through neurogenesis, synaptogenesis, apoptosis, or synapse elimination and functional changes through redistribution of receptors and ion channels, or through changes in second messenger cascades. These then alter circuit function and activity and so affect the animal's subsequent social behavior and experience.

Despite this complexity, some of the neurochemicals that appear to play significant roles in dominance behavior have been identified. Among the most prominent of these across phyla is serotonin (5‐hydroxytryptamine or 5‐HT) (Edwards 1997, Miczek 2002). In vertebrates, the correlation between dominance and serotonin is largely negative (Manuck 2006, Miczek 2006). In fish (Winberg et al., 1997) and monkeys (Fairbanks et al., 2004), levels of 5‐HT or its metabolite, 5‐HIAA, are lower in dominant animals than in subordinates. In crustaceans, an opposite trend was observed in shore crabs (Sneddon et al., 2000). In those animals, resting 5‐HT levels were found to be higher in the blood of winners than in losers, and 5‐HT levels increased more following a fight in winners than in losers. In crayfish, however, no differences in CNS levels of 5‐HT occurred between new dominant, subordinate, and control animals 24 hours after status differences were established (Panksepp et al., 2003).

The actions of serotonin are mediated through specific receptors that now number about 13 different types in vertebrates and 5 in arthropods (Manuck et al., 2006). Agonists of vertebrate 5‐HT_1A, 5‐HT_1B, and 5‐HT_2A receptors have been shown to reduce aggression in mammals (Miczek et al., 2002) and in some instances to promote social dominance status. At the same time, they also affect other patterns of motor behavior that, given the widespread distribution of both 5‐HT projections and 5‐HT receptors within nervous systems, is not surprising (Miczek 2006, Peeke 2000).

Only two of the estimated five or more 5‐HT receptors have been identified in crayfish, and their role in formation and maintenance of dominance hierarchies has only begun to be studied. However, much is known about the social dominance behavior of crayfish, and some of the neural circuits that mediate aspects of that behavior have been described, together with their modulation by 5‐HT. This unique knowledge base provides an opportunity that is missing in other animals to study the interaction between social status, neural circuits that mediate discrete aspects of social behavior, and the serotonergic modulation of those circuits and behavior.

Here we will describe what is known of dominance hierarchies in crayfish, the neural circuits that mediate relevant behavior patterns, and the roles of serotonin in modulating those circuits and behaviors. Finally, we will describe the two 5‐HT receptors that have recently been identified in crayfish, and the roles they may play in modulating neural circuits that control behavior patterns relevant to social dominance behavior.