Ecological context, sensory inputs, and the internal physiological state are integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between four phenotypes. Two are determined by social status and two are identified by the principle body coloration (yellow or blue). When socially dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behaviors. Subordinate (SUB) males decrease predation risk by adopting cryptic coloration and schooling behavior. Yellow males are more conspicuous than blue males, and DOMs and more conspicuous than SUBs, which means that yellow DOMs are most likely to be seen by predators. We therefore hypothesized that DOMs, yellow DOMs in particular, would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs than SUBs. When testing the same males after social change, yellow DOMs respond at a higher rate than yellow SUBs but blue males do not show plasticity. Electrophysiological recordings from the Mauthner cells (Mcells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons presynaptic to the M-cell was significantly reduced in DOMs. Using behavioral tests, intracellular recordings, and single-cell molecular analysis, immunohistochemistry and in-situ hybridization, I show here that serotonin modulates this socially regulated plasticity via the 5-HT receptor subtype 2 (HTR2A). Specifically, SUBs display increased sensitivity to pharmacological blockade of HTR2A compared with DOMs in both startle-escape behavior and electrophysiological properties of the M-cell. These receptors, however, are not expressed in the Mauthner neurons, but in the inhibitory interneurons that regulate the Mcell’s membrane properties. I show a role for 5-HT in modulating startle plasticity and increase our understanding of the neural basis of behavioral plasticity. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit. / text

Cichlid fishes from the East African Rift lakes Victoria, Tanganyika and Malawi represent a preeminent example of replicated and rapid evolutionary radiation. In this single natural system, numerous morphological (eg. jaw and tooth shape, color patterns, visual sensitivity), behavioral (eg. bower-building) and physiological (eg. development, neural patterning) phenotypes have emerged, much akin to a mutagenic screen. This dissertation encompasses three studies that seek to decipher the underpinnings of such rapid evolutionary diversification, investigated via the genetic variation in East African cichlids. We generated a valuable cichlid genomic resource of five low-coverage Lake Malawi cichlid genomes, from which the general properties of the genome were characterized. Nucleotide diversity of Malawi cichlids was low at 0.26%, and a sample genotyping study found that biallelic polymorphisms segregate widely throughout the Malawi species flock, making each species a mosaic of ancestrally polymorphic genomes. A second genotyping study expanded our evolutionary analysis to cover the entire East African cichlid radiation, where we found that more than 40% of single nucleotide polymorphisms (SNPs) were ancestral polymorphisms shared across multiple lakes. Bayesian analysis of genetic structure in the data supported the hypothesis that riverine species had contributed significantly to the genomes of Malawi cichlids and that Lake Malawi cichlids are not monophyletic. Both genotyping studies also identified interesting loci involved in important sensory as well as developmental pathways that were well differentiated between species and lineages. We also investigated cichlid genetic variation in relation to the evolution of microRNA regulation, and found that divergent selection on miRNA target sites may have led to differential gene expression, which contributed to the diversification of cichlid species. Overall, the patterns of cichlid genetic variation seem to be dominated by the phenomena of extensive sharing of ancestral polymorphisms. We thus believe that standing genetic variation in the form of ancestrally inherited polymorphisms, as opposed to variations arising from new mutations, provides much of the genetic diversity on which selection acts, allowing for the rapid and repeated adaptive radiation of East African cichlids.