The Role of Gene Co-option in the Evolution of Sap-Feeding Insect Endosymbioses (Hemiptera: Sternorrhyncha)

Symbiosis, the tightly co-evolved partnership between different species, fundamentally influences the evolutionary trajectory of the interacting species. However, with the help of emerging genomic resources, the mechanisms by which symbiotic partners are integrated into a functional organism are only just beginning to be revealed. As a system in which to investigate the mechanisms of host/symbiont integration, sap-feeding insects, which rely on intracellular symbionts for nutrient provisioning, benefit from growing genomic resources and a solid foundation resulting from years of research on the pea aphid, Acyrthosiphon pisum. At the core of the relationship between A. pisum and its endosymbiont Buchnera aphidicola is amino acid metabolism and exchange, and previous research suggests that amino acid exchange is mediated by amino acid transporters that were co-opted to operate in a symbiotic context. Inspired by recent discoveries in A. pisum, I use sap-feeding insects of the hemipteran suborder Sternorrhyncha to investigate the role of co-option of amino acid transporters in host/symbiont integration. In four chapters, I examine co-option with gene duplication and co-option in a single-copy amino acid transporter. Using microarray and RNA-seq data in the first three data chapters, I found support for both symbiotic and non-symbiotic traits driving the retention of duplicate amino acid transporters both at the level of the suborder Sternorrhyncha and at the level of the family Aphididae. Further, co-option of duplicate amino acid transporters to the symbiotic interface involved expression evolution, and possibly functional evolution as well. In the fourth data chapter, I combined gene annotation, expression analysis, and functional characterization to investigate the evolutionary mechanism by which the single-copy A. pisum glutamine transporter ApGLNT1 was co-opted to be a key regulator of amino acid metabolism in A, pisum. Using electrophysiology, I functionally characterized ApGLNT1 orthologs from other sap-feeding and non sap-feeding insects. I discovered that ApGLNT1 is functionally conserved, indicating that ApGLNT1 evolved its role in symbiosis within its ancestral functional constraints. Together, these four studies indicate that co-option has played a role in metabolic integration of sternorrhynchan endosymbioses by recruiting amino acid transporters to operate in the novel context of symbiosis