A Model of Behavioral Evolution from Genotype to Phenotype

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The evolution of behavior relies on changes at the level of the genome, yet few vertebrate behaviors can be traced directly to specific gene sequences. In this project, the research team will use a naturally-occurring animal model, the white-throated sparrow, to connect behavior with gene sequence in a concrete way. In this species, 50% of the birds have an unusual chromosome that makes them more aggressive. The chromosome is therefore an excellent tool for understanding how individual variation in gene expression contributes to variation in behavior. The team recently showed that animals with the unusual chromosome have higher expression of a type of steroid receptor in some areas of the brain. Here, the research group determines the genetic mechanisms, at the molecular level, that cause some birds to express more of these receptors than others. In so doing, the team demonstrates how responsiveness to steroid hormones is encoded in the genome. The work lends itself well to education and outreach because it illustrates basic biological concepts in a common backyard bird. Thus, it serves to integrate multiple units of a typical biology course in a way that is accessible to students. High school teachers are recruited to participate in the research and to develop lesson plans about genetics, hormones, brain anatomy, and social behavior. The PI also mentors high school students, undergraduates, and graduate students in the lab. More than 75% of the PI's mentees at Emory have been underrepresented minorities or women. The evolution of behavior relies on changes at the level of the genome, yet few vertebrate behaviors can be traced directly to genetic sequences. In the white-throated sparrow (Zonotrichia albicollis), a chromosomal inversion segregates with an aggressive behavioral phenotype, offering a rare opportunity to connect genes and behavior in a concrete way. The inversion has captured the gene ESR1, which encodes estrogen receptor alpha (ERalpha). The research team recently showed that the local expression of ERalpha in the brain depends on the presence or absence of the inversion and that variation in ERalpha expression predicts the effect of genotype on territorial aggression. The research group uses in vitro reporter assays, bisulfite sequencing, and allele-specific quantitative PCR to identify the genetic and epigenetic mechanisms that contribute to variation in expression of ERalpha. The effects of selective ERalpha ligands on aggressive behavior in animals of each genotype is used to determine whether variation in ERalpha expression and function is causal for variation in territorial aggression. Because the team uses tissue from behaviorally characterized, free-living animals, the molecular and behavioral levels are integrated in the same animals to allow novel connections. The results provide an interdisciplinary, integrated model of how genetic change leads to phenotypic change. The work lends itself well to education and outreach because it illustrates basic biological concepts in a common backyard bird.