PREOPTIC MECHANISMS OF SOCIAL BEHAVIOR PLASTICITY: GENETIC AND NEUROENDOCRINE REGULATION OF FISH ALTERNATIVE REPRODUCTIVE TACTICS

Abstract

A central challenge animals face is finding a mate and reproducing to pass on genes to offspring. Doing this often requires the performance of several related behaviors that may include territory defense, courtship, mating, and parental care. Individuals must perform these behaviors in a species- and context-appropriate manner or risk losing fitness. Together, hormones and the brain act to coordinate these social behaviors. Due to the extreme degree of intrasexual variation they express, species with alternative reproductive tactics make excellent models for investigating the neuroendocrine mechanisms underlying plasticity in reproductive behavior. I have worked with one of these species, the plainfin midshipman fish (Porichthys notatus), to investigate the role of a neuroendocrine center of the brain, the preoptic area-anterior hypothalamus (POA-AH), in regulating alternative spawning tactics and reproductive-related behaviors. Midshipman males develop into either of two fixed alternate morphs: type I males which may engage in courtship or cuckoldry and type II males which engage in cuckoldry only. These alternate morphs, coupled with type I male behavioral flexibility, have allowed me to better understand how POA-AH function is influenced both by developmental history and behavioral context. I have examined the role of the POA-AH in these tactics at the level of gene expression, neuroanatomy, and neural activity during behavior. First, I used RNA-sequencing to identify that during spawning type I males engaged in the cuckolding tactic had a more similar pattern of transcript expression in the POA-AH to cuckolding type II males than to courting type I males. This revealed that current behavioral tactic was more strongly associated with POA-AH transcript expression than was developmental morph. Additionally, I was able to identify a small set of differentially expressed transcripts involved in hormone signaling that included the neuropeptide galanin, which has an established role in mating, and is a marker for neurons that control parental care behaviors. Next, I found that the anatomy of galanin-expressing neurons is highly sexually polymorphic, with subtle differences between male morphs but extreme differences between males and females. Their location in the POA-AH and projection patterns make them well positioned to influence social behaviors, especially male-specific behaviors. Finally, I investigated the activity of these neurons during spawning and related behaviors, using phosphorylated S6 protein to label galanin-expressing cells that had recently been active. I found that these neurons are active in courting type I males during spawning, but not cuckolders of either morph or females. Additionally, this activity was not explained by courtship vocalization, care for eggs, or defense against cuckolders during spawning. Taken together, these results indicate that galanin is a regulator of male midshipman courtship tactic during spawning and appears to play a conserved role among vertebrates in behaviors contributing to individual fitness.