- Author: Kathy Keatley Garvey
In newly published research in Ecology Letters, "Dispersal Enchances Beta Diversity in Nectar Microbes," Vannette and colleague Tadashi Fukami of Stanford University's Department of Biology, examined microbial communities inhabiting the nectar of the sticky monkeyflower, Mimulus auranticus, at the Jasper Ridge Biological Preserve in California's Santa Cruz Mountains.
The flower, in the family Phrymacease, is a native shrub common in chaparral and coastal scrub habitats of California and Oregon. It is primarily pollinated by Anna's hummingbird. Other common pollinators include bumble bees, carpenter bees, and thrips.
Dispersal is considered a key driver of beta diversity, which is “the variation in species composition among local communities,” Vannette said.
They are the first to publish work showing that increased dispersal can increase biodiversity.
In their experiment, they reduced natural rates of dispersal by eliminating multiple modes of microbial dispersal. “Specifically we focused in nectar-inhabiting bacteria and yeasts that are dispersed among flowers by wind, insects and birds,” they said. “We imposed dispersal limitation on individual flowers and quantified microbial abundance, species composition and microbial effects on nectar chemistry.”
This work has direct implications for conservation of many organisms in addition to bacteria and yeast, suggesting that preserving routes of dispersal among habitat patches may be important in the maintenance of biodiversity. In contrast to previous work showing that dispersal can homogenize communities or make them more similar, the published work demonstrates that dispersal can in some cases generate communities that are more different from each other. The authors hypothesize that this could be driven by priority effects, where early arriving species change the species that can establish within that habitat.
Why focus on nectar-inhabiting microbes? Previous work by Vannette and others shows that microbial activity in nectar can alter nectar chemistry and influence plant-pollinator interactions by altering nectar chemistry. In the Ecology Letters study, microbes were also found to change nectar chemistry, explaining ~50% of the variation in sugar composition in the field. This suggests that nectar-inhabiting bacteria and yeast can influence the nectar rewards available to pollinators in a natural setting.
More broadly, “Studying the role of microbes in the environment addresses one of the biggest mysteries in science,” Vannette says. In her current work, she and her lab are investigating how microbial communities form, change, and function in their interactions with insects and plants. They are also researching how microorganisms affect plant defense against herbivores and plant attraction to pollinators.
Vannette, a former postdoctoral fellow at Stanford, joined the UC Davis Department of Entomology and Nematology faculty as an assistant professor in 2015.
Vannette's research was funded by the Gordon and Betty Moore Foundation through the Life Sciences Research Fellowship. Stanford also funded the research through grants from the National Science Foundation, the Terman Fellowship, and the Department of Biology at Stanford University.
- Author: Kathy Keatley Garvey
- Evolution of floral signals and flower morphology
- Pollinator-drive speciation
- Evolution of floral mimicry
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- Author: Kathy Keatley Garvey
In newly published research in the journal Ecology, Vannette noted that floral nectar is produced by many plants to reward pollinators, but this sugary secretion often contains chemical compounds that are bitter tasting or toxic, and can deter pollinators. Plants including citrus (Citrus), tobacco (Nicotiana), milkweed (Asclepias), turtlehead (Chelone), Catalpa, and others produce nectar containing bioactive compounds, including deterrent or toxic compounds.
“This poses a paradox of toxic nectar: why are deterrent or harmful compounds present in a resource intended to attract pollinators?” she asked. “One hypothesis is that these compounds reduce microbial growth, which could otherwise spoil the nectar resource.”
Vannette, an assistant professor in the UC Davis Department of Entomology and Nematology, and her colleague Tadashi Fukami, associate professor at Stanford University, tested this hypothesis by growing yeasts and bacteria in sugar solutions spiked with a chemical compounds that are found in nectar.
“We examined effects on the growth of microbes isolated from nectar and non-nectar sources. Contrary to expectations, chemical compounds only weakly inhibited microbial growth in most cases. Interestingly, some microorganisms even grew better in the presence of plant compounds, like nicotine. But most surprising, we found that microbial growth in nectar reduced nectar toxicity, decreasing the concentration of chemical compounds in some nectar solutions.”
Microbial effects on nectar, in turn, increased consumption of nectar containing chemical compounds by honey bee pollinators, she said. “We found that microorganisms in nectar can both reduce the concentration of some plant compounds in nectar and increase consumption of nectar that does contain these compounds. This indicates that although ‘toxic nectar' does not strongly inhibit microbial growth in nectar, microbes modify the palatability of nectar to pollinators, which can change foraging behaviors and may reduce selection on this trait in nectar.”
The paper, exploring the effects of nectar-inhabiting microbes on chemical compounds found in nectar and nectar consumption by pollinators, “demonstrates that the compounds in nectar—such as on citrus blossoms--do not inhibit microbial growth, Vannette said. “However, yeasts and bacteria that grow in nectar can modify the effects of plant chemical compounds on pollinator foraging and nectar consumption..”
In her abstract, Vannette wrote “Secondary metabolites that are present in floral nectar have been hypothesized to enhance specificity in plant-pollinator mutualism by reducing larceny by non-pollinators, including microorganisms that colonize nectar. However, few studies have tested this hypothesis. Using synthetic nectar, we conducted laboratory and field experiments to examine the effects of five chemical compounds found in nectar on the growth and metabolism of nectar-colonizing yeasts and bacteria, and the interactive effects of these compounds and nectar microbes on the consumption of nectar by pollinators.”
“In most cases, focal compounds inhibited microbial growth, but the extent of these effects depended on compound identity, concentration, and microbial species. Moreover, most compounds did not substantially decrease sugar metabolism by microbes, and microbes reduced the concentration of some compounds in nectar. Using artificial flowers in the field, we also found that the common nectar yeast Metschnikowia reukaufii altered nectar consumption by small floral visitors, but only in nectar containing catalpol. This effect was likely mediated by a mechanism independent of catalpol metabolism. Despite strong compound-specific effects on microbial growth, our results suggest that the secondary metabolites tested here are unlikely to be an effective general defense mechanism for preserving nectar sugars for pollinators. Instead, our results indicate that microbial colonization of nectar could reduce the concentration of secondary compounds in nectar and, in some cases, reduce deterrence to pollinators.”
The research, “Nectar Microbes Can Reduce Secondary Metabolites in Nectar and Alter Effects on Nectar Consumption by Pollinators,” appears on the Ecology website, http://onlinelibrary.wiley.com/doi/10.1890/15-0858.1/full
The research was funded by the Gordon and Betty Moore Foundation, the National Science Foundation, and Stanford University.
Future work will examine how microbial modification of nectar traits influences floral attractiveness, how microbial growth may modify the specificity of plant-pollinator interactions, and if microbial effects vary among plant species.
Vannette, a former postdoctoral fellow at Stanford University, joined the UC Davis Department of Entomology and Nematology in September 2015. “I am interested in understanding and predicting how microbial communities influence interactions between plants and insects,” she said. “In the Vannette lab (in Briggs Hall), we use tools and concepts from microbial ecology, chemical ecology, and community ecology to better understand the ecology and evolution of interactions among plants, microbes and insects."
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Ecology journal research paper
- Author: Kathy Keatley Garvey
The paper on bee immunity and toxin metabolism was published Nov. 9 in Scientific Reports, part of the Nature Publishing Group.
“First, the results suggest that forager bees may use antimicrobial peptides—short sequences of amino acids with general activity-- to reduce microbial growth in stored food resources,” said Rachel Vannette of the UC Davis Department of Entomology and Nematology. “This would be a largely unrecognized way that bees protect honey and potentially other stored resources from microbial spoilage. Second, this work shows that forager bees produce toxin-degrading enzymes in nectar-processing tissues.”
“This may allow forager bees to degrade many different kinds of compounds in nectar, before it is stored,” Vannette said. “Bees also vary in their ability to do this—foragers have a greater ability to degrade a variety of compounds than nurses. This may have implications for hive health and management.”
"Nice paper,” said Gene Robinson, director of the Institute for Genomic Biology and Swanlund Chair of Entomology, University of Illinois at Urbana-Champaign, who was not involved in the research. “It had been well known that the division of labor in a honey bee colony is supported by extensive differences in brain gene expression between bees that perform different jobs. This new research shows nicely that this genomic differentiation extends beyond the brain; different complements of active genes in a variety of tissues make each bee better suited for the job it needs to perform."
The journal article, titled “Forager Bees (Apis mellifera) Highly Express Immune and Detoxification Genes in Tissues Associated with Nectar Processing,” is the work of senior author/assistant professor Brian Johnson of the UC Davis Department of Entomology and Nematology, and co-authors Abbas Mohamed, graduate student researcher in the Johnson lab and a member of the Pharmacology and Toxicology Group, and assistant professor Vannette, who joined the UC Davis Department of Entomology this fall after serving a postdoctoral fellowship at Stanford University. At Stanford, Vannette examined the role of nectar chemistry in community assembly of yeasts and plant-pollinator interactions.
Johnson, whose research interests include animal behavior, evolution, theoretical biology and genomics, recently began long-term research on the honey bee immune system and the causes and consequences of economically important diseases /syndromes such as colony collapse disorder.
Mohamed, who has researched honey bees since 2011, is currently focusing on pesticide detoxification as a part of his master's degree research. "Honey bees have always fascinated me,” Mohamed said, “and there is nothing more exciting than to be at the edge of discovery, learning new things, and contributing to the field of our understanding of these amazing creatures.”
The team plans to follow up with functional assays to examine the potential of these gene products to (1) reduce microbial growth and (2) degrade a variety of natural and synthetic compounds.
The abstract:
“Pollinators, including honey bees, routinely encounter potentially harmful microorganisms and phytochemicals during foraging. However, the mechanisms by which honey bees manage these potential threats are poorly understood. In this study, we examine the expression of antimicrobial, immune and detoxification genes in Apis mellifera and compare between forager and nurse bees using tissue-specific RNA-seq and qPCR. Our analysis revealed extensive tissue-specific expression of antimicrobial, immune signaling, and detoxification genes. Variation in gene expression between worker stages was pronounced in the mandibular and hypopharyngeal gland (HPG), where foragers were enriched in transcripts that encode antimicrobial peptides (AMPs) and immune response. Additionally, forager HPGs and mandibular glands were enriched in transcripts encoding detoxification enzymes, including some associated with xenobiotic metabolism. Using qPCR on an independent dataset, we verified differential expression of three AMP and three P450 genes between foragers and nurses. High expression of AMP genes in nectar-processing tissues suggests that these peptides may contribute to antimicrobial properties of honey or to honey bee defense against environmentally-acquired microorganisms. Together, these results suggest that worker role and tissue-specific expression of AMPs, and immune and detoxification enzymes may contribute to defense against microorganisms and xenobiotic compounds acquired while foraging.”
- Author: Kathy Keatley Garvey
“I am interested in understanding and predicting how microbial communities influence interactions between plants and insects,” she said. “In the Vannette lab (in Briggs Hall), we use tools and concepts from microbial ecology, chemical ecology, and community ecology to better understand the ecology and evolution of interactions among plants, microbes and insects."
A native of Hudsonville, Mich., Vannette received her bachelor of science degree in biology with honors at Calvin College, Grand Rapids, Mich., and her doctorate in ecology and evolutionary biology from the University of Michigan, in 2011. Her dissertation was entitled “Whose Phenotype Is It Anyway? The Complex Role of Species Interactions and Resource Availability in Determining the Expression of Plant Defense Phenotype and Community Consequences.”
In her PhD research, she examined how variation in nutrient availability and plant associations with mycorrhizal fungi belowground influenced defense chemistry in milkweed plants and the performance of a specialist herbivore (Danaus plexippus). She found that resource-based tradeoffs can in part explain plant allocation to antiherbivore defense and mycorrhizal fungi. This work also describes that plant genotypes vary in their investment in defense and associations with belowground fungi.
As a Stanford University postdoctoral fellow, funded by a life sciences research fellowship, Vannette examined the community ecology of plant-associated microorganisms. Using diverse systems, she studied the assembly of microbial communities, microbial response to anthropogenic changes like habitat fragmentation, and microbial effects on plant-pollinator interactions.
- Community ecology of plant-associated microbial communities. She explored what mechanisms shape the structure and function of microbial communities associated with plants, and how to assemble mechanisms to better understand functions, including the effects on insect herbivores and pollinators. She also researched how ants influence microbial community structure and nectar characteristics in coffee agroecosystems.
- Nectar ecology. Knowing that yeasts and bacteria are common inhabitants of flowers, and attain high densities in floral nectar, she researched how these microbes influence plants and pollinators, the mechanisms involved, and evolutionary ecology of these interactions. She also studied how nectar constituents influence pollinator foraging and health.
- Influence of anthropogenic changes on plant-microbe (insect) interactions. She researched how fragmentation affects fungal community composition in the rhizosphere of Meterosideros polymorpha, a species of flowering evergreen tree in the myrtle family. She also studied elevated carbon dioxide changes plant-microbe-insect interactions, and researched the effects of mycorrhizal fungi on plant defense and plant-herbivore interactions.
The National Wildlife Research Foundation featured Vannette's research on monarchs and milkweed in its March 11, 2013 piece on “Catering to Butterfly Royalty." The article, by author Doreen Cubie, focused on Vannette's research as a graduate student at the University of Michigan. Vannette and advisor Mark Hunter studied five common species of milkweeds, the host plant for monarchs. They found that climate change may disrupt the chemistry of milkweeds, and encouraged gardeners to help the monarchs by planting more of these critical host plants.
Vannette and Hunter grew the plants in open-air chambers, “exposing them to elevated amounts of carbon dioxide designed to mimic Earth's atmosphere in the future,” wrote Cubie. “Although most of the plants grew slightly larger, the composition of plant leaves changed dramatically. Most of the milkweed families decreased their production of toxins, some by as much as 50 percent. The extra carbon dioxide exposure toughened the leaves, a problem for the caterpillars.
Last March Vannette was an invited speaker on the ecology and evolution of the microbiome at the University of Michigan Early Career Scientists' symposium in Ann Arbor, Mich.
Among her recent publications:
- Co-author of “Plant-Derived Variation in the Composition of Aphid Honeydew and its Effects on Colonies of Aphid-Tending Ants,” published in November 2014 in the journal Ecology and Evolution.
- Lead author of “Genetic Variation in Plant Below-Ground Response to Elevated CO2 and Two Herbivore Species,” published in July 2014 in Plant Soil.
- Co-author of “Honey Bees Avoid Nectar Colonized by Three Bacterial Species, but not by a Yeast Species, Isolated from the Bee Gut,” published in a January 2014 edition of PLOS ONE.
- Lead author of “Historical Contingency in Species Interactions: Towards Niche-Based Predictions,” published November 2013 in Ecology Letters. (Recommended by the Faculty of 1000)