Trichobaris weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval performance

Abstract

Herbivorous insects use plant metabolites to inform their host plant selection for oviposition. These host-selection behaviours 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 those responsible for differences in offspring performance remain unknown for ecologically relevant interactions. Here, we examined the host-selection behaviours of two sympatric weevils, the Datura (Trichobaris compacta) and tobacco (T. mucorea) weevils in field and glasshouse experiments with transgenic host plants specifically altered in different components of their secondary metabolism. Adult females of both species strongly preferred to feed on D. wrightii rather than on N. attenuata leaves, but T. mucorea preferred to oviposit on N. attenuata, while T. compacta oviposited only on D. wrightii. These oviposition behaviours increased offspring performance: T. compacta larvae only survived in D. wrightii stems and T. mucorea larvae survived better in N. attenuata than in D. wrightii stems. Choice assays with nicotine-free, JA-impaired, and sesquiterpene-over-produced isogenic N. attenuata plants revealed that although half of the T. compacta larvae survived in nicotine-free N. attenuata lines, nicotine did not influence the oviposition behaviours of both the nicotine-adapted and nicotine-sensitive species. JA-induced sesquiterpene volatiles are key compounds influencing T. mucorea females' oviposition choices, but these sesquiterpenes had no effect on larval performance. We conclude that adult females are able to choose the best host plant for their offspring and use chemicals different from those that influence larval performance to inform their oviposition decisions.

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

“…The stems of N. attenuata are often attacked by herbivores, including stem borers (Diezel et al, 2011b;Lee et al, 2016), and are very important for plant fitness (Machado et al, 2016). We observed a strong up-regulation of defensive secondary metabolites in the stems in response to M. sexta attack (Fig.…”

“…unknown, jasmonate-dependent defenses (Diezel et al, 2011b;Lee et al, 2016). It is therefore possible that the IAA-triggered potentiation of jasmonate-dependent secondary metabolite accumulation in the stems may reduce the performance of stem feeders.…”

Strigolactone signaling regulates specialized metabolism in tobacco stems and interactions with stem-feeding herbivores

“…Alternatively, the red pigmentation may function as a visual indirect defense, functionally analogous to the volatile alarm calls that are so effective in attracting predators to herbivore-attacked N. attenuata plants [55]. In contrast, the functional significance of nicotine and other changes in pith secondary metabolism for weevil performance was characterized in this and previous publications [11,41,44], which provide insights into how natural selection has sculpted a skein of direct and indirect phytohormonal responses to attack from this native herbivore whose life is intimately entwined with that of its host.…”

“…Neonate larvae then burrow through the petioles into the pith of the RSJ, where they feed endophytically inside stems. At 2 or 3 weeks postinoculation (wpi), when larvae in wild-type (WT) stems are typically in the penultimate instar [44], stems were carefully split open, larvae were retrieved, and larval biomass was quantified. To first investigate the direct role of JAs in defense against T. mucorea, a transgenic line deficient in JA signaling, resulting from the silencing the JA biosynthetic gene, allene oxide cyclase (aoc) plants [45], was used for the larval performance assay.…”

Divergent host plant utilization by adults and offspring is related to intra‐plant variation in chemical defences

“…Maternal choice can vary between herbivore species and populations, where some may select either optimal or suboptimal diet choices for their offspring (Clark, Hartley, & Johnson, ; Friberg, Posledovich, & Wiklund, ; Garcia‐Robledo & Horvitz, ; Gripenberg, Mayhew, Parnell, & Roslin, ; Handley, Ekbom, & Ågren, ; Hufnagel, Schilmiller, Ali, & Szendrei, ). Alternatively, the inverse has been observed, where host plant dietary constraints on adults impacted reproduction and fitness, yet did not completely extend to negative impacts on brood performance (Lee et al, ; Scheirs, Bruyn, & Verhagen, ; Scheirs et al, ; Smith, Johnson, Davidowitz, & Bronstein, ). In some instances, such as in Trichobaris weevils, adult beetles avoid host plants that produce toxins (Lee et al, ), but these toxins have no apparent effect on juveniles infesting host plants.…”