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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.

SUBMITTER: Egan PA

PROVIDER: S-EPMC6169423 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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

Egan Paul A PA Adler Lynn S LS Irwin Rebecca E RE Farrell Iain W IW Palmer-Young Evan C EC Stevenson Philip C PC

Frontiers in plant science 20180926

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 ...[more]

PMID: 30319666

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Project description:BackgroundPollinating insects provide economically and ecologically valuable services, but are threatened by a variety of anthropogenic changes. The availability and quality of floral resources may be affected by anthropogenic land use. For example, flower-visiting insects in agroecosystems rely on weeds on field edges for foraging resources, but these weeds are often exposed to agrochemicals that may compromise the quality of their floral resources.MethodsWe conducted complementary field and greenhouse experiments to evaluate the: (1) effect of low concentrations of agrochemical exposure on nectar and pollen quality and (2) relationship between floral resource quality and insect visitation. We applied the same agrochemcial treatments (low concentrations of fertilizer, low concentrations of herbicide, a combination of both, and a control of just water) to seven plant species in the field and greenhouse. We collected data on floral visitation by insects in the field experiment for two field seasons and collected pollen and nectar from focal plants in the greenhouse to avoid interfering with insect visitation in the field.ResultsWe found pollen amino acid concentrations were lower in plants exposed to low concentrations of herbicide, and pollen fatty acid concentrations were lower in plants exposed to low concentrations of fertilizer, while nectar amino acids were higher in plants exposed to low concentrations of either fertilizer or herbicide. Exposure to low fertilizer concentrations also increased the quantity of pollen and nectar produced per flower. The responses of plants exposed to the experimental treatments in the greenhouse helped explain insect visitation in the field study. The insect visitation rate correlated with nectar amino acids, pollen amino acids, and pollen fatty acids. An interaction between pollen protein and floral display suggested pollen amino acid concentrations drove insect preference among plant species when floral display sizes were large. We show that floral resource quality is sensitive to agrochemical exposure and that flower-visiting insects are sensitive to variation in floral resource quality.

Project description:Background and aimsPollinator landscapes, as determined by pollinator morphology/behaviour, can vary inter- or intraspecifically, imposing divergent selective pressures and leading to geographically divergent floral ecotypes. Assemblages of plants pollinated by the same pollinator (pollinator guilds) should exhibit convergence of floral traits because they are exposed to similar selective pressures. Both convergence and the formation of pollination ecotypes should lead to matching of traits among plants and their pollinators.MethodsWe examined 17 floral guild members pollinated in all or part of their range by Prosoeca longipennis, a long-proboscid fly with geographic variation in tongue length. Attractive floral traits such as colour, and nectar properties were recorded in populations across the range of each species. The length of floral reproductive parts, a mechanical fit trait, was recorded in each population to assess possible correlation with the mouthparts of the local pollinator. A multiple regression analysis was used to determine whether pollinators or abiotic factors provided the best explanation for variation in floral traits, and pollinator shifts were recorded in extralimital guild member populations.Key resultsNine of the 17 species were visited by alternative pollinator species in other parts of their ranges, and these displayed differences in mechanical fit and attractive traits, suggesting putative pollination ecotypes. Plants pollinated by P. longipennis were similar in colour throughout the pollinator range. Tube length of floral guild members co-varied with the proboscis length of P. longipennis.ConclusionsPollinator shifts have resulted in geographically divergent pollinator ecotypes across the ranges of several guild members. However, within sites, unrelated plants pollinated by P. longipennis are similar in the length of their floral parts, most probably as a result of convergent evolution in response to pollinator morphology. Both of these lines of evidence suggest that pollinators play an important role in selecting for certain floral traits.

Project description:BackgroundAnimal pollination supports agricultural production for many healthy foods, such as fruits, vegetables, nuts, and legumes, that provide key nutrients and protect against noncommunicable disease. Today, most crops receive suboptimal pollination because of limited abundance and diversity of pollinating insects. Animal pollinators are currently suffering owing to a host of direct and indirect anthropogenic pressures: land-use change, intensive farming techniques, harmful pesticides, nutritional stress, and climate change, among others.ObjectivesWe aimed to model the impacts on current global human health from insufficient pollination via diet.MethodsWe used a climate zonation approach to estimate current yield gaps for animal-pollinated foods and estimated the proportion of the gap attributable to insufficient pollinators based on existing research. We then simulated closing the "pollinator yield gaps" by eliminating the portion of total yield gaps attributable to insufficient pollination. Next, we used an agriculture-economic model to estimate the impacts of closing the pollinator yield gap on food production, interregional trade, and consumption. Finally, we used a comparative risk assessment to estimate the related changes in dietary risks and mortality by country and globally. In addition, we estimated the lost economic value of crop production for three diverse case-study countries: Honduras, Nepal, and Nigeria.ResultsGlobally, we calculated that 3%-5% of fruit, vegetable, and nut production is lost due to inadequate pollination, leading to an estimated 427,000 (95% uncertainty interval: 86,000, 691,000) excess deaths annually from lost healthy food consumption and associated diseases. Modeled impacts were unevenly distributed: Lost food production was concentrated in lower-income countries, whereas impacts on food consumption and mortality attributable to insufficient pollination were greater in middle- and high-income countries with higher rates of noncommunicable disease. Furthermore, in our three case-study countries, we calculated the economic value of crop production to be 12%-31% lower than if pollinators were abundant (due to crop production losses of 3%-19%), mainly due to lost fruit and vegetable production.DiscussionAccording to our analysis, insufficient populations of pollinators were responsible for large present-day burdens of disease through lost healthy food consumption. In addition, we calculated that low-income countries lost significant income and crop yields from pollinator deficits. These results underscore the urgent need to promote pollinator-friendly practices for both human health and agricultural livelihoods. https://doi.org/10.1289/EHP10947.

Project description:Background and aimsStudies of local floral adaptation in response to geographically divergent pollinators are essential for understanding floral evolution. This study investigated local pollinator adaptation and variation in floral traits in the rewarding orchid Gymnadenia odoratissima, which spans a large altitudinal gradient and thus may depend on different pollinator guilds along this gradient.MethodsPollinator communities were assessed and reciprocal transfer experiments were performed between lowland and mountain populations. Differences in floral traits were characterized by measuring floral morphology traits, scent composition, colour and nectar sugar content in lowland and mountain populations.Key resultsThe composition of pollinator communities differed considerably between lowland and mountain populations; flies were only found as pollinators in mountain populations. The reciprocal transfer experiments showed that when lowland plants were transferred to mountain habitats, their reproductive success did not change significantly. However, when mountain plants were moved to the lowlands, their reproductive success decreased significantly. Transfers between populations of the same altitude did not lead to significant changes in reproductive success, disproving the potential for population-specific adaptations. Flower size of lowland plants was greater than for mountain flowers. Lowland plants also had significantly higher relative amounts of aromatic floral volatiles, while the mountain plants had higher relative amounts of other floral volatiles. The floral colour of mountain flowers was significantly lighter compared with the lowland flowers.ConclusionsLocal pollinator adaptation through pollinator attraction was shown in the mountain populations, possibly due to adaptation to pollinating flies. The mountain plants were also observed to receive pollination from a greater diversity of pollinators than the lowland plants. The different floral phenotypes of the altitudinal regions are likely to be the consequence of adaptations to local pollinator guilds.

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

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

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