Genetic, molecular, and neuroendocrine basis of behavioral evolution in deer mice

Despite the extraordinary diversity of behavior across the animal kingdom, the genes and molecules that contribute to such natural diversity are largely unknown. In this thesis, I leverage the dramatic divergence in behavior between two closely related species of deer mice (genus Peromyscus) to investigate the genetic, cellular, and neuroendocrine basis of behavior. In chapter 2, I show that the monogamous oldfield mouse (Peromyscus polionotus subgriseus) has evolved a novel cell type in the adrenal gland that expresses the enzyme AKR1C18, which converts progesterone into 20α-hydroxyprogesterone (20α-OHP). I then demonstrate that 20α-OHP is more abundant in oldfield mice than in the closely-related promiscuous prairie deer mouse (P. maniculatus bairdii) and that it increases monogamous-typical parental behaviors when administered to both monogamous fathers. Using quantitative trait locus mapping in a cross between these species, I discover interspecific genetic variation that drives expression of the glycoprotein tenascin N and ultimately contributes to gain of adrenal AKR1C18 expression in oldfield mice. In chapter 3, I investigate the genetic architecture underlying the striking difference in exploratory behavior between prairie deer mice and oldfield mice. Through congenic fine-mapping, I identify a 15-Mb locus that strongly contributes to species differences in exploratory behavior. I then investigate the potential contributions of one of the 18 genes in the locus, Olfm4, which harbors cis-regulatory variants that drives its expression in the oldfield hypothalamus. Taken together, my research advances our understanding of the genetic and molecular causes that drive rapid behavioral divergence between species

Symbiont interactions with non-native hosts limit the formation of new symbioses

BACKGROUND: Facultative symbionts are common in eukaryotes and can provide their hosts with significant fitness benefits. Despite the advantage of carrying these microbes, they are typically only found in a fraction of the individuals within a population and are often non-randomly distributed among host populations. It is currently unclear why facultative symbionts are only found in certain host individuals and populations. Here we provide evidence for a mechanism to help explain this phenomenon: that when symbionts interact with non-native host genotypes it can limit the horizontal transfer of symbionts to particular host lineages and populations of related hosts. RESULTS: Using reciprocal transfections of the facultative symbiont Hamiltonella defensa into different pea aphid clones, we demonstrate that particular symbiont strains can cause high host mortality and inhibit offspring production when injected into aphid clones other than their native host lineage. However, once established, the symbiont's ability to protect against parasitoids was not influenced by its origin. We then demonstrate that H. defensa is also more likely to establish a symbiotic relationship with aphid clones from a plant-adapted population (biotype) that typically carry H. defensa in nature, compared to clones from a biotype that does not normally carry this symbiont. CONCLUSIONS: These results provide evidence that certain aphid lineages and populations of related hosts are predisposed to establishing a symbiotic relationship with H. defensa. Our results demonstrate that host-symbiont genotype interactions represent a potential barrier to horizontal transmission that can limit the spread of symbionts, and adaptive traits they carry, to certain host lineages

Additional file 1: of Symbiont interactions with non-native hosts limit the formation of new symbioses

Diagnostic symbiont species-specific primer sequences. (PDF 70 kb

Additional file 3: of Symbiont interactions with non-native hosts limit the formation of new symbioses

Survival, reproduction, and establishment of H. defensa strains in different host aphid clones. Aphids that have been cured of H. defensa have a “c” prior to the clone number. (PDF 85 kb

Additional file 2: of Symbiont interactions with non-native hosts limit the formation of new symbioses

Production of artificial infection treatments by microinjection of H. defensa-containing hemolymph from two donor aphid clones into three symbiont-free recipient aphid clones, named according to their host plant (L. pedunculatus, M. sativa, or O. spinosa), producing two native symbiont strain by host aphid clone associations (“native”) and four non-native associations (“non-native”), plus three control treatments of recipient clones injected with hemolymph from a single M. sativa clone that had been cured of H. defensa (“control”). (PDF 54 kb