Brain and antennal transcriptome changes are linked to colonization-mediated behavioral switch in an environmentally transmitted symbiosis

Many organisms engage in symbiosis with microbial partners that are not passed on directly to offspring but are acquired from the environment each generation. Hosts can minimize the risk of relying on such horizontal transmission of beneficial symbionts by engaging in specialized acquisition behaviors. Squash bugs, Anasa tristis, locate their Caballeronia symbiont through olfactory cues released from adult frass. After ingesting the symbiont, nymph behavior shifts from symbiont searching to host plant feeding. To begin to elucidate the underlying changes behind this behavioral switch, we generated transcriptomes from heads of second instar squash bugs that had recently acquired their symbiont and compared them to those of aposymbiotic controls. Inoculation with Caballeronia significantly impacted overall gene expression. Functional enrichment revealed significant changes in transporter and peptidase activity in response to symbiont colonization, suggesting a strong signaling cascade between midgut crypts and the brain. Given the role of olfaction in symbiont acquisition, we manually annotated odorant receptors and odorant binding proteins, two important gene families involved in olfaction. We identified one odorant receptor and two odorant binding proteins that responded to symbiont colonization. We then evaluated the phylogenetic relationship of all identified odorant receptors and odorant binding proteins to those of other hemipterans to identify functionally relevant clades. These results highlight the tight physiological coupling that can evolve between insects and their horizontally acquired microbial symbionts and will inform future research on microbially mediated changes in insect behavior.