Trade-offs between cost of ingestion and rate of intake drive defensive toxin use

Abstract

Animals that ingest toxins can become unpalatable and even toxic to predators and parasites through toxin sequestration. Because most animals rapidly eliminate toxins to survive their ingestion, it is unclear how populations transition from susceptibility and toxin elimination to tolerance and accumulation as chemical defence emerges. Studies of chemical defence have generally focused on species with active toxin sequestration and target-site insensitivity mutations or toxin-binding proteins that permit survival without necessitating toxin elimination. Here, we investigate whether animals that presumably rely on toxin elimination for survival can use ingested toxins for defence. We use the A4 and A3 Drosophila melanogaster fly strains from the Drosophila Synthetic Population Resource (DSPR), which respectively possess high and low metabolic nicotine resistance among DSPR fly lines. We find that ingesting nicotine increased A4 but not A3 fly survival against Leptopilina heterotoma wasp parasitism. Further, we find that despite possessing genetic variants that enhance toxin elimination, A4 flies accrued more nicotine than A3 individuals, likely by consuming more medium. Our results suggest that enhanced toxin metabolism can allow greater toxin intake by offsetting the cost of toxin ingestion. Passive toxin accumulation that accompanies increased toxin intake may underlie the early origins of chemical defence.

Keywords: bioaccumulation; chemical defence; enemy-free space; multi-trophic selection; xenobiotic metabolism.

Figure 1.

(a) Nicotine concentration–survival curve for DSPR A3 and A4 Drosophila melanogaster. Data are normalized by maximum survival of each strain on control food. Vertical dashed lines represent LC50 of each strain.

Figure 2.

(a) Nicotine consumption significantly decreased survival in unparasitized A3 and A4 Drosophila melanogaster flies. Nicotine consumption increased survival of parasitized A4 but not A3 flies. (b) Nicotine consumption by A4 and A3 flies significantly decreased Leptopilina heterotoma developmental success. (c) Nicotine consumption reduced A3 but not A4 adult body mass. (d) Nicotine-fed A3 and A4 flies accumulated nicotine and its metabolic byproduct cotinine across developmental stages. Asterisks indicate significant differences; n.s., not significant.