Pollinator selection against toxic nectar as a key facilitator of a plant invasion

Abstract

Plant compounds associated with herbivore defence occur widely in floral nectar and can impact pollinator health. We showed previously that Rhododendron ponticum nectar contains grayanotoxin I (GTX I) at concentrations that are lethal or sublethal to honeybees and a solitary bee in the plant's non-native range in Ireland. Here we further examined this conflict and tested the hypotheses that nectar GTX I is subject to negative pollinator-mediated selection in the non-native range, but that phenotypic linkage between GTX I levels in nectar and leaves acts as a constraint on independent evolution. We found that nectar GTX I experienced negative directional selection in the non-native range, in contrast to the native Iberian range, and that the magnitude and frequency of pollinator limitation indicated that selection was pollinator-mediated. Surprisingly, nectar GTX I levels were decoupled from those of leaves in the non-native range, which may have assisted post-invasion evolution of nectar without compromising the anti-herbivore function of GTX I (here demonstrated in bioassays with an ecologically relevant herbivore). Our study emphasizes the centrality of pollinator health as a concept linked to the invasion process, and how post-invasion evolution can be targeted toward minimizing lethal or sub-lethal effects on pollinators. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Sweet solutions: nectar chemistry and quality

“…Two South African examples are the dark phenolic-containing nectar of Aloe vryheidensis , which deters honeybees and sunbirds, but not generalist bulbuls, and the unpalatable nectar of a milkweed that is preferentially consumed by spider wasps [ 48 , 109 ]. Grayanotoxins in nectar of the invasive Rhododendron ponticum in the UK are toxic to honeybees but not to the main bumblebee pollinator Bombus terrestris [ 49 ]; geographical variation in the filtering function of these compounds has consequences for invasion biology [ 110 ]. Deterrence depends on concentrations of both sugar and toxin: honeybees and nectar-feeding birds are more tolerant to nicotine in artificial nectars of higher concentration [ 111 , 112 ].…”

Natural processes influencing pollinator health

“…However, Egan et al . [ 33 ] report that pollinators impose negative directional selection against grayanotoxin in nectar of invasive R. ponticum , which contrasts with selection patterns quantified in the species' native range, where this compound was under positive selection in nectar. Nectar concentrations were decoupled from those of leaves in the invasive but not the native range, which is likely to assist this species to evolve and facilitate visits by pollinators while simultaneously maintaining anti-herbivore defence.…”