Genomic contributions to the evolution of behavior [electronic resource]
Keywords: Biology.

Behavior is a key component of animal life and is central to the survival, life history, and diversification of species. Behavior is also the main output of the nervous system and, as such, is a reflection of the various biological capacities possessed by animal taxa. Developing an integrative understanding of animal behavior is crucial for addressing diverse topics biology including, but not limited to, unlocking how brains work (including our own, in both sickness and health), outlining the process of speciation, and developing tools for the conservation of natural animal populations. Despite this we still know little about how behavior is regulated by biology, be it through evolutionary time or within the span of an individual's lifetime. Part of the difficulty in doing has been due a historical paucity of behavioral model systems that display both extreme phenotypic diversity but are suitable for study in the laboratory. To this end I worked to develop the bower (mating nest) building cichlid fish of Lake Malawi as a system for understanding the evolution of behavior across biological levels, from genome sequence variation through to ecological constraints on behavior. First, I used a combination of novel and previously published data to explore the macroevolutionary, ecological, and morphological contexts of bower diversity. I found distinct associations between depth of occurrence, functional jaw morphology, visual sensitivity, and behavioral sequence with the different types of bower architecture observed in Lake Malawi. Next, I used comparative neuroanatomical methods to discover that hindbrain volume and structure, specifically that of the vagal lobe, significantly vary with bower type across evolutionary time. I used genetic labels of neural activity to confirm that the hindbrain is functionally recruited by bower building and applied phylogenomic tests to demonstrate that bower building has led to an increase in hindbrain diversification among both Malawi and Tanganyika cichlids, likely driven by the process of natural selection. Third, in collaboration with Todd Streelman's lab, I combined whole-genome sequencing of 20 bower building Malawi cichlid species with whole brain RNA-seq of F1 hybrids between two species with divergent bower types to identify the genetic bases of bower building. I found that variation in bower building is associated with an extremely complex genetic architecture and that these differences likely exert their effect through context-dependent genetic regulation based on behavioral state. Finally, to expand my efforts and place my work with Malawi cichlids in context, I performed a meta-analysis of behavior genetic mapping using quantitative trait locus (QTL) methods. I collected over 1,000 QTL significantly associated with behavior and found that the effect of these QTL varied strongly with the type of behavior studied (with courtship and feeding behaviors being associated with particularly strong QTL). I corroborated this meta-analysis with a genome-wide analyses of 87 behavioral traits in a single diverse population of fruit flies. I foun that in this case too courtship and feeding behaviors tended to be associated with loci of high effect that were on average more heritable. This work demonstrates that the evolution of bower building has involved segregation across diverse biological phenomena and is associated with a surprisingly complex genetic basis. Furthermore, it suggests a novel role for gene regulation in behavior based on an animal's behavioral state. Finally, it provides the basis for future targeted and integrative studies of Malawi cichlid behavior with the intent of unlocking how behavior is accomplished across time and space.