Different species of animals display disparate behaviors that are produced by underlying neural circuits in the brains of each animal. To understand how different behaviors may have evolved, it is necessary to compare how the neural circuits in closely related species differ. The objective of this project is to address three fundamental questions about the evolution of neural circuits underlying behavior: 1) How do similar nervous systems produce different behaviors? 2) Can the same neurons in different species have similar functions even though the behaviors of the animals differ? 3) How do nervous systems in animals of different lineages produce the same behavior? This study addresses these questions by examining phylogenetic changes in identified homologous neurons in nudibranch mollusks, also known as sea slugs. Nudibranchs have simple nervous systems with individually identifiable neurons that underly three different types of locomotor behavior: crawling and two types of swimming: some sea slugs swim by lateral body flexions and others swim by dorsal/ventral body flexions. The divergent swimming behaviors arose independently multiple times in different nudibranch lineages. Studying phylogenetic differences in the functions and properties of identified neurons underlying locomotion will help determine how the behaviors changed during the evolutionary history of these sea slugs and will also provide understanding of how behaviorally relevant neural circuits can change in any creature. Closely-related nudibranchs can exhibit divergent behaviors that are often associated with species-differences in the properties and connections of the underlying neurons. This project compares the neurophysiological properties and synaptic connections of homologous neurons that produce different behaviors in four closely-related species: Tritonia diomedea (a dorsal/ventral swimmer), Melibe leonina and Dendronotus iris (both lateral swimmers), and Tochuina tetraquetra (a non-swimmer). This part of the project will correlate neurophysiology with behavior to determine which features of the neurons or their circuit connections are functionally important. The functions of the neurophysiological properties then will be tested directly using an electrophysiological technique called dynamic clamp to artificially transform the membrane and synaptic properties of homologous neurons. If the properties of neurons can be electrically transformed so their activity more closely resembles that of the homologous neurons in other species and swim behavior typical of that species is produced, then it would be strong evidence that those neural properties play a causal role in the production of behavior. Despite large differences in the behaviors of some closely-related nudibranchs, there likely will be underlying similarities in the functions of identified neurons. The second aim of the project is to look for conserved behavioral functions of homologous neurons in species with divergent behaviors. This will provide a basis for understanding the shared organization of the neural circuits, which forms the foundation upon which the derived behaviors are built. Distantly-related nudibranchs can also display similar behaviors. The phylogenetic distribution of swim behaviors suggests that they arose independently multiple times. The third aim of this project is to test whether independent evolution of the same motor behavior was caused by convergent or parallel evolution. The functions of homologous neurons in nudibranchs of different lineages that exhibit the same swimming behavior will be tested. The species pairs to be examined are Aphelodoris antillensis and Tritonia diomedea, distantly related dorsal /ventral swimmers, and Flabellina iodinea and Melibe leonina, distantly related lateral swimmers. If homologous neurons came to be used in the same way, for the same purpose, independently in different lineages, then it would indicate that the similarity in the swimming behavior arose through parallel evolution. This would suggest that components of neural circuits are like building blocks that can be taken apart and reassembled in the same way. Alternatively, if it is found that the behaviors resemble each other because of convergent evolution, then it would indicate that there are multiple configurations of nervous systems that can produce the same behavioral output. The project is designed to involve undergraduate students in the research plan. Specific mechanisms are in place to enhance the participation of historically under-represented ethnic groups. Plans have been made to use this project as a tool to teach about animal diversity and evolution in secondary schools using Georgia State University's Bio-Bus and to develop public exhibits on sea slugs at the new Georgia Aquarium in Atlanta.
