Immunological dependence of plant-dwelling animals on the medicinal properties of their plant substrates: a preliminary test of a novel evolutionary hypothesis

Abstract

We present preliminary evidence for a novel evolutionary hypothesis, i.e., that animals living on plants high in antimicrobial secondary metabolites could, via drift or selection, evolve weakened immune defenses and an immunological dependence on the antimicrobial properties of their plant substrate and/or the volatile mix in the air surrounding their plant. Animals experience immunological stress during developmental transitions, so we evaluated our hypothesis by testing for an effect of plant substrate on hatching success in the jumping spider Lyssomanes viridis, a species that constructs its egg sacs on Liquidambar styraciflua leaves. Compared with other sympatric species, L. styraciflua is known to be high in potent volatile broad-spectrum antimicrobial compounds, most notably, the monoterpene terpinen-4-ol, a well-studied antimicrobial agent known from tea tree oil. We found that L. viridis experience higher hatching success on L. styraciflua than on other sympatric species or plastic substrate controls and that L. viridis has a chemically mediated preference for this plant. In contrast to other spiders’ compact, densely woven egg sacs, L. viridis’ egg sacs are sparsely woven and the eggs widely spaced, maximizing the eggs’ surface area exposed to volatiles coming off the leaf. Similar architectures exist in distantly related taxa, suggesting convergent evolution. Our theoretical framework and preliminary results open up an unexplored frontier—the possibility that any number of plant-dwelling species may depend upon on the antimicrobial properties of the plant tissues they inhabit.