Comparative chemical ecology of invasive Depressaria species (Lepidoptera: Depressariidae) varying in hostplant specificity

Dean, Charles-Antoine Edouard

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https://hdl.handle.net/2142/115767 Copy

Description

Title

Comparative chemical ecology of invasive Depressaria species (Lepidoptera: Depressariidae) varying in hostplant specificity

Author(s)

Dean, Charles-Antoine Edouard

Issue Date

2022-04-20

Director of Research (if dissertation) or Advisor (if thesis)

Berenbaum, May R

Doctoral Committee Chair(s)

Berenbaum, May R

Committee Member(s)

• Whitfield, James B
• Dolezal, Adam G
• Calla, Bernarda

Department of Study

Entomology

Discipline

Entomology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• Herbivory
• Invasive
• Phytochemistry
• Coevolution
• Apiaceae, Depressariidae

Abstract

The purple carrot seed moth (Depressaria depressana) (Fabricius) (Lepidoptera: Depressariidae) is a newly invasive species in North America. This moth is of Eurasian origin and, unlike its well-studied congener the parsnip webworm (Depressaria radiella), it is a family-level specialist of the Apiaceae, utilizing more than a dozen species in multiple tribes within the family. By contrast, D. radiella is a superspecialist that feeds almost exclusively on species in the genera Pastinaca and Heracleum in Europe and in areas of introduction around the world. The presence of D. depressana in North America offers a unique opportunity to study the evolutionary and ecological mechanisms underlying the adaptation of a family specialist to a novel environment during the early stages of its colonization. Such an investigation can not only reveal the similarities and differences between biological invaders of divergent feeding strategies but can also provide insight into the dynamics of plant-insect interactions involving an introduced family specialist and chemically defended hosts that can provide a framework for management strategies for future invasive species that fill a similar ecological niche. In the first chapter of my dissertation, I investigated whether differences in furanocoumarin metabolism exist between D. depressana and two isolated populations of D. radiella feeding exclusively on either P. sativa or H. maximum. I also compared four gravimetric estimates of efficiency to assess D. depressana larval performance on different diets. Both populations of D. radiella metabolized furanocoumarins at a greater rate than D. depressana. Although there was no difference in rates of metabolism of linear furanocoumarins in the two populations of D. radiella, individuals collected from H. maximum metabolized angular furanocoumarins more rapidly. The gravimetric assessments of performance revealed that D. depressana exhibited highest efficiencies of conversion of ingested food when consuming D. carota; moreover, this species could survive consuming fruits of Zizia aurea, an apiaceous species native to North America. Lastly, I performed a preliminary phylogenetic analysis, building on an earlier analysis based on morphological characters, by adding data from the mitochondrial cytochrome oxidase subunit 1 (COI) barcoding gene. Results indicate that adaptation to furanocoumarins is not a strong predictor of species-level evolution in Depressaria. In the second chapter of my dissertation, I evaluated differences in physiological mechanisms of adaptation to phototoxic furanocoumarins in the two species of Depressaria. Earlier work revealed that D. radiella sequesters lutein, a carotenoid pigment, in response to UV light exposure and dietary furanocoumarins, apparently as a mechanism to reduce phototoxicity. Accordingly, I examined differences in expression of the ninaB gene in response to dietary -carotene, xanthotoxin, and B-carotene + xanthotoxin among D. radiella, a superspecialist feeder, D. depressana, a family-level specialist, and Trichoplusia ni, a broadly polyphagous herbivore. The ninaB enzyme is involved in the cleavage of carotenoids, which are pigments that aid in a broad array of biological functions, including ultraviolet light protection, vision, color pattern development, and antioxidant defenses. I found that, in all three species, ninaB is significantly downregulated across all three experimental diets relative to the unamended artificial diet control. However, there was no consistent pattern within each species across treatments. These results indicate that cleavage of B-carotene is downregulated in the presence of dietary furanocoumarins, but whether sequestration of unmodified -carotene either directly reduces toxicity of furanocoumarins or enhances the activity of detoxifying cytochrome P450 monooxygenase enzymes remains an open question. For the third chapter of my dissertation, I characterized the CYPome, or complete inventory of genes encoding cytochrome P450 monooxygenases, the principal Phase 1 detoxification enzymes utilized by most lepidopterans, in the D. depressana genome and evaluated the transcriptomic response of D. depressana to consumption of the linear furanocoumarin xanthotoxin and the angular furanocoumarin sphondin. The cytochrome P450 monooxygenases (P450s) involved in metabolism mediate detoxification of xenobiotics, including furanocoumarins, by catalyzing oxidation reactions whereby oxygen is added to lipophilic compounds to increase water solubility and excretion from the cell. In many specialist herbivores, detoxifying P450s have become highly specialized over evolutionary time and differences in susceptibility to furanocoumarins can potentially be explained by a diversity of P450s with narrow substrate specificities. I found that the D. depressana CYPome encompasses 76 P450 genes, including 7 Clan 2, 37 Clan 3, 24 Clan 4, and 11 mitochondrial clan P450s. This CYPome is the smallest of the seven lepidopteran species considered in this analysis. Transcriptomic responses to dietary xanthotoxin revealed striking widespread differential expression relative to the sphondin and control treatments. A Gene Ontology (GO) enrichment analysis revealed that upregulation was highest among genes involving DNA replication, transcription, and metabolic processes. The transcriptomic response to dietary sphondin was virtually nonexistent and a GO enrichment analysis was not conducted. For my fourth chapter, I assessed the genetic structure of invasive D. depressana populations across latitudinal and longitudinal gradients in the eastern United States by constructing haplotype networks using the mitochondrial COI and nuclear EF1α markers. This experiment allowed me to assess interpopulational diversity and gene flow across 301 individuals from 17 populations collected in 7 states. In my analysis, both markers exhibited high genetic diversity, which indicates high levels of gene flow, or, given the recency of its introduction, insufficient evolutionary time for localized adaptation to occur among populations of D. depressana. In the case of COI, few haplotypes were recovered and comparisons to European and Canadian populations did not reveal a likely source population. Conversely, many EF1α haplotypes were recovered in this experiment, which obscured any evaluation of dispersal routes across the continent. Geographic features, such as rivers and mountains, did not appear to obstruct gene flow across populations. Together my chapters provide a novel aspect to the plant-insect coevolutionary model first established by the parsnip webworm and wild parsnip system. As a newly invasive congener of the parsnip webworm, D. depressana maintains a greater diet breadth as a family-level specialist and therefore serves as a point of comparison to the superspecialist, D. radiella. My chapters examine the reciprocal selective pressure between plant phytochemistry and herbivore detoxification by broadening the understanding of the role that diet breath plays in the dynamics underlying invasion biology.

Graduation Semester

2022-05

Type of Resource

Thesis

Copyright and License Information

Copyright 2022 Charles-Antoine Dean

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