Abstract
Background Nicotiana attenuata is attacked by larvae of both specialist (Manduca sexta) and generalist (Spodoptera exigua) lepidopteran herbivores in its native habitat. Nicotine is one of N. attenuata's important defenses. M. sexta is highly nicotine tolerant; whether cytochrome P450 (CYP)-mediated oxidative detoxification and/or rapid excretion is responsible for its exceptional tolerance remains unknown despite five decades of study. Recently, we demonstrated that M. sexta uses its nicotine-induced CYP6B46 to efflux midgut-nicotine into the hemolymph, facilitating nicotine exhalation that deters predatory wolf spiders (Camptocosa parallela). S. exigua's nicotine metabolism is uninvestigated.Methodology/Principal FindingsWe compared the ability of these two herbivores to metabolize, tolerate and co-opt ingested nicotine for defense against the wolf spider. In addition, we analyzed the spider's excretion to gain insights into its nicotine metabolism. Contrary to previous reports, we found that M. sexta larvae neither accumulate the common nicotine oxides (cotinine, cotinine N-oxide and nicotine N-oxide) nor excrete them faster than nicotine. In M. sexta larvae, ingestion of nicotine as well as its oxides increases the accumulation of CYP6B46 transcripts. In contrast, S. exigua accumulates nicotine oxides and exhales less (66%) nicotine than does M. sexta. Spiders prefer nicotine-fed S. exigua over M. sexta, a preference reversed by topical or headspace nicotine supplementation, but not ingested or topically-coated nicotine oxides, suggesting that externalized nicotine but not the nicotine detoxification products deter spider predation. The spiders also do not accumulate nicotine oxides.ConclusionsNicotine oxidation reduces S. exigua's headspace-nicotine and renders it more susceptible to predation by spiders than M. sexta, which exhales unmetabolized nicotine. These results are consistent with the hypothesis that generalist herbivores incur costs of detoxification, which include the ecological costs of greater predation risks, in addition to the previously demonstrated energetic, physiological and metabolic costs.
Highlights
Plant defense chemicals hamper insect herbivores’ growth and reproduction
Since we could not detect any nicotine oxide in our previous work, a study in which we discovered a novel function of the midgut expressed and nicotineinduced CYP6B46, we hypothesized that in the M. sexta strain of our laboratory culture, one or more oxidation steps could be inactive or absent
We examined the frass of field-collected Manduca spp. larvae feeding on native plants and administered each nicotine oxide separately to M. sexta larvae and analyzed whether the additional oxidized products of the pathway could be recovered from hemolymph and frass
Summary
The ingestion of allelochemicals can enhance herbivore survivorship in nature, when they are co-opted for defense against natural enemies [1,2]. Such defensive co-option requires a balance between detoxification and tolerance mechanisms. Specialists by means of their evolved resistance and tolerance mechanisms are thought to co-opt host defenses, while generalists are thought to detoxify them, frequently at great energetic, metabolic and physiological costs [6,7,8,9]. Different herbivores’ cooption mechanisms against a common xenobiotic have been studied and compared [16,17,18]; the empirical evidence on the ecological consequences of co-option, especially to other herbivores of the same host remains sparse.
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