Aversion and attraction to harmful plant secondary compounds jointly shape the foraging ecology of a specialist herbivore

• Published in: Ecology and evolution Vol. 6; no. 10; pp. 3256 - 3268
• Main Authors: Humphrey, Parris T., Gloss, Andrew D., Alexandre, Nicolas M., Villalobos, Martha M., Fremgen, Marcella R., Groen, Simon C., Meihls, Lisa N., Jander, Georg, Whiteman, Noah K.
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.05.2016; John Wiley and Sons Inc
• Subjects: Arabidopsis thaliana; Aversion; Biosynthesis; Brassicaceae; Cardamine cordifolia; Detoxification; Drosophila; Drosophilidae; Feeding; Feeding trials; Foraging behavior; glucosinolate; Glucosinolates; Herbivores; Host plants; inducible defense; Insects; Jasmonic acid; Larvae; Larval development; Leaves; Mustard; Mustard oil; Mutants; Oils & fats; Original Research; oviposition; Plant species; Plant tissues; preference–performance; Scaptomyza nigrita; Specialization; Species; United States > US; inducible defense; glucosinolate; oviposition; Drosophila; jasmonic acid; preference–performance
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.2082

Most herbivorous insect species are restricted to a narrow taxonomic range of host plant species. Herbivore species that feed on mustard plants and their relatives in the Brassicales have evolved highly efficient detoxification mechanisms that actually prevent toxic mustard oils from forming in the bodies of the animals. However, these mechanisms likely were not present during the initial stages of specialization on mustard plants ~100 million years ago. The herbivorous fly Scaptomyza nigrita (Drosophilidae) is a specialist on a single mustard species, bittercress (Cardamine cordifolia; Brassicaceae) and is in a fly lineage that evolved to feed on mustards only in the past 10–20 million years. In contrast to many mustard specialists, S. nigrita does not prevent formation of toxic breakdown products (mustard oils) arising from glucosinolates (GLS), the primary defensive compounds in mustard plants. Therefore, it is an appealing model for dissecting the early stages of host specialization. Because mustard oils actually form in the bodies of S. nigrita, we hypothesized that in lieu of a specialized detoxification mechanism, S. nigrita may mitigate exposure to high GLS levels within plant tissues using behavioral avoidance. Here, we report that jasmonic acid (JA) treatment increased GLS biosynthesis in bittercress, repelled adult female flies, and reduced larval growth. S. nigrita larval damage also induced foliar GLS, especially in apical leaves, which correspondingly displayed the least S. nigrita damage in controlled feeding trials and field surveys. Paradoxically, flies preferred to feed and oviposit on GLS‐producing Arabidopsis thaliana despite larvae performing worse in these plants versus non‐GLS‐producing mutants. GLS may be feeding cues for S. nigrita despite their deterrent and defensive properties, which underscores the diverse relationship a mustard specialist has with its host when lacking a specialized means of mustard oil detoxification. Many specialists herbivores can subvert host plant defensive chemistry, allowing them to “feed with impunity” on plant tissues. But despite being a specialist herbivore, Scaptomyza nigrita lacks a specialized means of overcoming the toxic mustard oils of its Brassicacea host. Here, we show that this herbivore exhibits a behavioral strategy for mitigating host plant toxicity by avoiding high concentrations of mustard oil precursors where possible, even though these compounds themselves may be important for initiating host feeding.