Date of Award

5-10-2017

Degree Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Department

Neuroscience Institute

First Advisor

Paul S. Katz

Second Advisor

Charles Derby

Third Advisor

Laura Carruth

Fourth Advisor

William Walthall

Abstract

Serotonin (5-HT) receptors modulate neuronal and synaptic properties, altering the functional output of neural circuits. Changing the functions of a neural circuit can alter behavior. Over evolutionary time, species differences in neuromodulation could allow for species-specific behaviors to evolve. To investigate this idea, this dissertation compared neuromodulatory receptor gene expression underlying species-specific swimming behaviors in sea slugs.

The sea slug Tritonia diomedea (Mollusca, Gastropoda, Nudipleura, Nudibranchia), performs a rhythmic dorsal-ventral (DV) escape swim behavior. The behavior is controlled by a central pattern generator (CPG), composed of a small number of large, identifiable neurons. During swimming, 5-HT enhances the synaptic strength of a neuron in the swim CPG, called C2. In contrast, the nudibranch Hermissenda crassicornis does not swim in this manner. It has C2 homologues, and 5-HT is present, however, 5-HT does not modulate C2 synaptic strength. Pleurobranchaea californica, a Nudipleura species belonging to a sister clade of Nudibranchia, swims with DV flexions, although in this species swimming varies within individuals. 5-HT enhances Pleurobranchaea C2 homologue synaptic strength in swimming animals, only. Phylogenetic analysis showed that Tritonia and Pleurobranchaea independently evolved DV-swimming. Thus, there is a correlation between independently evolved swimming and serotonergic modulation of C2 homologues. It was hypothesized that 5-HT receptor differences in C2 neurons underlie species-specific swimming and modulation.

To test this hypothesis, 5-HT receptor genes were identified in each species. A total of seven receptor subtypes, from five gene families, were found to be expressed in the brains of each species. Using single-cell quantitative PCR (qPCR), 5-HT receptor expression profiles were determined in C2 homologues. Genes known as 5-HT2a and 5-HT7 were expressed in C2 homologues from Tritonia and swimming Pleurobranchaea, only. Single-neuron transcriptome sequencing verified these results. The expression profiles of neuromodulatory receptor genes in single, homologous neurons correlated with species-specific swimming and modulation. The results illustrate how differences in neuromodulatory gene expression may alter the functional output of homologous neural structures, shedding light on a means by which neuromodulation can alter the brain to facilitate the evolution of species-specific behaviors.

Evolution, Mollusc, Neuromodulation, Serotonin, Receptor, Behavior, Next-Generation Sequencing, Transcriptomics

DOI

https://doi.org/10.57709/10068106

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