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Document Type

Open Access Dissertation

Degree Name

Doctor of Philosophy (PhD)

Degree Program

Organismic and Evolutionary Biology

Year Degree Awarded

2018

Month Degree Awarded

February

First Advisor

Lynn Adler

Second Advisor

Anne Averill

Third Advisor

Ana Caicedo

Fourth Advisor

Peter Alpert

Subject Categories

Entomology | Evolution | Integrative Biology | Medicinal-Pharmaceutical Chemistry | Parasitology

Abstract

Background: Nectar and pollen are rich in phytochemicals, some of which can reduce disease in pollinators, including agriculturally important honey and bumble bees. Floral phytochemicals could influence the ecological and evolutionary relationships between plants, their pollinators, and parasites that cause pollinator disease. Antiparasitic effects of phytochemicals could be exploited to ameliorate pollinator disease and decline, and thereby sustain pollinator-dependent agricultural production. However, prior studies showed variable effects of phytochemicals on infection in live bees, where differences in bee genotype, abiotic conditions, and parasite strain could influence results.

Approach: I used cell cultures of the intestinal trypanosome parasite of bumble bees, Crithidia bombi, to (1) describe how resistance to 9 floral phytochemicals varied among 4 parasite strains, (2) describe the antiparasitic effect of phytochemical combinations, and (3) test for evolution of resistance to individual phytochemicals and a two-phytochemical blend.

Results:

(1) Resistance to floral phytochemicals: C. bombi showed striking resistance to the phenolics gallic acid, caffeic acid, and chlorogenic acid at levels beyond those found in nectar and pollen; literature searches showed that C. bombi resistance to these compounds exceeded that of bloodstream trypanosomes by several orders of magnitude. Phytochemical resistance varied among C. bombi isolates, indicating that medicinal effects of phytochemicals are dependent on parasite strain. Thymol and eugenol inhibited growth at concentrations below the toxicity thresholds of bees. Inhibitory concentrations of thymol were similar to those found in Thymus vulgaris nectar, indicating that medicinal effects of phytochemicals on pollinator disease are ecologically relevant, and could be achieved through strategic planting of phytochemical-rich flowers.

(2) Synergistic effects of combined phytochemicals: Thymol and eugenol had synergistic effects against 3 of 4 C. bombi strains—inhibition of parasites exposed to phytochemical combinations was stronger than predicted based on the activities of isolated phytochemicals. Synergy between phytochemicals suggests that phytochemical combinations may have greater antiparasitic potential in comparison to single phytochemicals. Synergistic phytochemical combinations in diverse floral landscapes could allow pollinators to self-medicate without toxicity, thereby ameliorating diseases that contribute to pollinator decline.

(3) Evolution of resistance to phytochemicals: Resistance of C. bombi increased under single and combined phytochemical exposure, without any associated cost of reduced growth under phytochemical-free conditions. After six weeks’ exposure, phytochemical concentrations that initially inhibited growth by >50%, and exceeded concentrations in floral nectar, had minimal effects on evolved parasite lines. Unexpectedly, a two-phytochemical combination did not impede resistance evolution compared to single compounds. These results demonstrate that repeated phytochemical exposure, which could occur in homogeneous floral landscapes or with therapeutic phytochemical treatment of managed hives, can cause rapid evolution of resistance in a pollinator parasite. Evolved resistance could diminish the antiparasitic value of phytochemical ingestion, weakening an important natural defense against infection.

Conclusion: These results show the potential of phytochemical-rich flowers to directly ameliorate pollinator infection, a recognized contributor to bee decline. Results also suggest benefits of diverse landscapes for pollinator health. Phytochemically complex mixtures in diverse floral landscapes could synergistically inhibit parasite growth and curtail the evolution of phytochemical resistance in parasites, thereby optimizing the medicinal effects of phytochemicals on bees. Deliberate planting of high-phytochemical crops and hedgerow species could reduce the effects of disease on bee populations, thereby benefitting agricultural production.

Comments

Published, typeset pdfs are available at DOI's:

10.1038/srep37087

10.1111/jeb.13002

10.1002/ece3.2794

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