Crop Domestication Alters Floral Reward Chemistry With Potential Consequences for Pollinator Health

Abstract

Crop domestication can lead to weakened expression of plant defences, with repercussions for herbivore and pathogen susceptibility. However, little is known about how domestication alters traits that mediate other important ecological interactions in crops, such as pollination. Secondary metabolites, which underpin many defence responses in plants, also occur widely in nectar and pollen and influence plant-pollinator interactions. Thus, domestication may also affect secondary compounds in floral rewards, with potential consequences for pollinators. To test this hypothesis, we chemically analysed nectar and pollen from wild and cultivated plants of highbush blueberry (Vaccinium corymbosum L.), before conducting an artificial diet bioassay to examine pollinator-pathogen interactions. Our results indicated that domestication has significantly altered the chemical composition of V. corymbosum nectar and pollen, and reduced pollen chemical diversity in cultivated plants. Of 20 plant metabolites identified in floral rewards, 13 differed significantly between wild and cultivated plants, with a majority showing positive associations with wild compared to cultivated plants. These included the amino acid phenylalanine (4.5 times higher in wild nectar, 11 times higher in wild pollen), a known bee phagostimulant and essential nutrient; and the antimicrobial caffeic acid ester 4-O-caffeoylshikimic acid (two times higher in wild nectar). We assessed the possible biological relevance of variation in caffeic acid esters in bioassays, using the commercially available 3-O-caffeoylquinic acid. This compound reduced Bombus impatiens infection by a prominent gut pathogen (Crithidia) at concentrations that occurred in wild but not cultivated plants, suggesting that domestication may influence floral traits with consequences for bee health. Appreciable levels of genetic variation and heritability were found for most floral reward chemical traits, indicating good potential for selective breeding. Our study provides the first assessment of plant domestication effects on floral reward chemistry and its potential repercussions for pollinator health. Given the central importance of pollinators for agriculture, we discuss the need to extend such investigations to pollinator-dependent crops more generally and elaborate on future research directions to ascertain wider trends, consequences for pollinators, mechanisms, and breeding solutions.

Flowers and climate change: a metabolic perspective

“…Very little research is currently performed in order to ascertain the extent of these metabolic changes and how they affect pollinators’ behavior. Moreover, to our knowledge, no breeding strategies are currently being implemented that aim to increase pollination efficiency (beyond artificial pollination strategies), although recent studies have revealed that domestication alters floral chemistry and may jeopardize pollinator health (Egan et al ., ).…”

Pollen and vegetative secondary chemistry of three pollen‐rewarding lupines

“…In particular, many of the studies that have assessed pollen secondary chemistry have been limited to single species and single or few tissues, limiting the comparative value of these data (Kessler and Halitschke, ). Further, the majority of this work has focused on species that also provide other rewards, most commonly nectar (e.g., London‐Shafir et al., ; Cook et al., ; Egan et al., ). Such species are not strictly pollen rewarding and so may be expected to chemically defend their pollen.…”

Pollen Protein: Lipid Macronutrient Ratios May Guide Broad Patterns of Bee Species Floral Preferences

“…Additionally, although remaining high, there is substantial difference between the P:L values of Jalapeño and Marengo varieties of Capsicum annuum P:L values (Table S2). Crop domestication can reduce nectar and pollen defensive chemistry [82], but the effect of domestication on pollen nutritional chemistry and effect on pollinator attractiveness, pollination services, and health needs further investigation.…”