Host selection behavior of a herbivorous insect, Trichobaris mucorea and defense responses of the host plant, Nicotiana attenuata

Abstract

Plant chemicals play important roles on host selection behaviors of herbivorous insects, especially females are able to recognize plant-producing chemicals to select their host plants and these host-selection behaviors are often consistent with the preference-performance hypothesis

females oviposit on hosts that maximize the performance of their offspring. However, the metabolites used for these oviposition choices and responsible for differences in offspring performance remain unknown for ecologically-relevant interactions. In this study, I examined host selection behaviors of two sympatric sibling species: Datura weevil, Trichobaris compacta and tobacco weevil, Trichobaris mucorea in the field and the glasshouse with transgenic host plants specifically altered in different components of their secondary metabolism. I found that both Trichobaris species adults were mainly observed in Datura wrightii growing in the Great Basin Desert of southwestern USA, but only T. mucorea larvae were colonized in the wild tobacco, Nicotiana attenuata growing the same area. In the glasshouse-experiments, both Trichobaris females strongly preferred to feed on D. wrightii rather than on N. attenuata, females of T. compacta oviposited only on D. wrightii but, T. mucorea females preferred to oviposit on N. attenuata. These oviposition behaviors increased their offspring performances which are larval survival and growth. Although the half of the T. compacta larvae survived in nicotine-free N. attenuata lines but, nicotine did not influence oviposition behaviors of T. compacta as well as T. mucorea. Jasmonic acid (JA)-induced sesquiterpene volatiles were key compounds influencing T. mucorea female oviposition choices, while these sesquiterpenes had no effect on larvae performance. I conclude that there is strong correlation between female oviposition preference and larval performance of two sibling Trichobaris species between D. wrightii and N. attenuata plants. Furthermore I verified that each level of host selection behavior such as female oviposition choice and offspring performance is affected by different plant secondary metabolites. To understand affecting factor of T. mucorea larvae performance on host plant defense response, I focused on host plant induced defense metabolite against T. mucorea larvae in stem tissue. When leaf-feeding insect herbivores attack, plants activate defense responses in both attacked as well as unattacked systemic leaves. These defense responses are largely regulated by herbivory-induced JA. Little is known about the defense responses of the stems or the role of JA signaling in these responses. I show here how the attack of T. mucorea larva, a tobacco stem weevil, triggers a defense response in the stems of N. attenuata plants. Female T. mucorea adults lay eggs on the stems of N. attenuata, and neonates burrow into the stems and feed on the pith. To examine this stem defense, firstly I established an herbivore performance assay, in which T. mucorea eggs were experimentally inoculated into N. attenuata stems. T. mucorea elicited high levels of JA and jasmonoyl-L-isoleucine in the pith of stem that have been attacked, as happens when chewing insects damage N. attenuata leaves. Chlorogenic acid (CGA) levels were highly increased in the pith of attacked stems in a JA-dependent manner, while the level of CGA in the attacked N. attenuata leaves is known to be unchanged. To test whether induced CGA confers resistance of the pith, I used a transgenic CGA-free N. attenuata plant that could not produce hydroxycinnamoyl quinate CoA transferase (NaHQT). In glasshouse and field experiments, T. mucorea larvae performed better in these NaHQT-silenced plants than on wild-type plants, indicating that the CGA in stems is a direct defense metabolite that plants produce to protect themselves against T. mucorea attack.