Abstract
The genus Depressaria (Lepidoptera: Depressariidae) mostly comprises specialist herbivores with varying capacity for detoxification of defensive phytochemistry. Depressaria depressana, a Eurasian moth recently introduced into North America, is a family-level specialist of the Apiaceae, whose hosts include more than a dozen species in multiple tribes; Depressaria radiella is a super-specialist of Eurasian origin that feeds exclusively on species in the genera Pastinaca and Heracleum throughout its native and introduced range. In eastern North America, it feeds upon Pastinaca sativa, an invasive European species, and Heracleum maximum, a native species. We determined 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. We also compared gravimetric estimates of feeding 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 feeding efficiencies revealed that D. depressana exhibited highest efficiencies consuming Daucus carota; moreover, this species survived to pupation consuming fruits of Zizia aurea, an apiaceous species native to North America. Our preliminary phylogenetic analysis, building on an earlier morphological analysis, incorporates mitochondrial cytochrome oxidase subunit 1 data from the BOLD database and revealed that the presence or absence of furanocoumarins is not a strong predictor of species-level evolution in Depressaria.
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Notes
ECI = biomass gain/diet ingested. Biomass gain represents the converted dry weight of the larva at 0 h minus the dry weight of the larva at 24 h. Diet ingested represents the diet dry weights at 0 h minus diet dry weights at 24 h. ECD = biomass gain/(consumption – frass). Consumption represents converted dry weights of the diet at 0 h minus the dry weights of the food at 24 h. RGR = biomass gain/larval mass. RCR = consumption/larval mass. Larval mass represents the converted dry weights of the larvae at 0 h.
References
Ali JG, Agrawal AA (2012) Specialist versus generalist herbivores and plant defense. Trends Plant Sci 17:293–302. https://doi.org/10.1016/j.tplants.2012.02.006
Bauri AK, Foro S, Nguyen Do NQ (2016) Crystal structure of a photobiologically active furanocoumarin from Artemisia reticulata. Acta Crystallogr e: Crystallogr Commun 72:463–466. https://doi.org/10.1107/S2056989016003303
Berenbaum MR (1981) Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae: Plant chemistry and community structure. Ecology 62:1254–1266. https://doi.org/10.2307/1937290
Berenbaum MR (1983) Coumarins and caterpillars: A case for coevolution. Evolution 37:163–179. https://doi.org/10.2307/2408184
Berenbaum MR (1990) Evolution of specialization in insect-umbellifer associations. Ann Rev Entomol 35:319–342. https://doi.org/10.1146/annurev.en.35.010190.001535
Berenbaum MR (1991) Comparative processing of allelochemicals in the Papilionidae (Lepidoptera). Arch Insect Biochem Physiol 17:213–221. https://doi.org/10.1002/arch.940170405
Berenbaum MR (1995) Phototoxicity of plant secondary metabolites: Insects and mammalian perspectives. Arch Insect Biochem Physiol 29:119–134. https://doi.org/10.1002/arch.940290294
Berenbaum MR, Favret C, Schuler MA (1996) On defining “key innovations” in an adaptive radiation: Cytochrome P450S and Papilionidae. Am Naturalist 148:S139–S155. https://doi.org/10.1086/285907
Berenbaum MR, Zangerl AR (1991) Acquisition of a native hostplant by an introduced oligophagous herbivore. Oikos 62:153–159. https://doi.org/10.2307/3545260
Berenbaum MR, Zangerl AR (1992) Genetics of physiological and behavioral resistance to host furanocoumarins in the parsnip webworm. Evolution 46:1373–1384. https://doi.org/10.1111/j.1558-5646.1992.tb01130.x
Berenbaum MR, Zangerl AR (1998) Chemical phenotype matching between a plant and its insect herbivore. Proc Natl Acad Sci U S A 95:13743–13748. https://doi.org/10.1073/pnas.95.23.13743
Berenbaum MR, Zangerl AR (2006) Parsnip webworms and host plants at home and abroad: Trophic complexity in geographic mosaic. Ecology 87:3070–3081. https://doi.org/10.1890/0012-9658(2006)87[3070:PWAHPA]2.0.CO;2
Berenbaum MR, Zangerl AR, Lee K (1989) Chemical barriers to adaptation by a specialist herbivore. Oecologia 80:501–506. https://doi.org/10.1007/BF00380073
Berenbaum MR, Zangerl AR, Nitao JK (1986) Constraints on chemical coevolution; Wild parsnips and the parsnip webworm. Evolution 40:1215–1228. https://doi.org/10.2307/2408949
Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci U S A 91:6491–6495. https://doi.org/10.1073/pnas.91.14.6491
Bouckaert R, Drummond A (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Ecol Biol 17:42. https://doi.org/10.1186/s12862-017-0890-6
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, de Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Drummond AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15:e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Bruni R, Barreca D, Protti M, Brighenti V, Righetti L, Anceschi L, Mercolini L, Benvenuti S, Gattuso G, Pellati F (2019) Botanical sources, chemistry, analysis, and biological activity of furanocoumarins of pharmaceutical interest. Molecules 24:2163. https://doi.org/10.3390/molecules24112163
Bucheli SR, Passoa S, Wenzel JW (2010) A phylogenetic test of Ehrlich and Raven’s theory of escape and radiation in insects that feed on toxic plants, based on Nearctic Depressaria moths (Gelechioidea: Elachistidae: Depressariinae), with discussion of the evolution of genitalia. Entomol Am 116:1–24. https://doi.org/10.1664/10-RA-009.1
Buchner P, Sumpich J (2018) Faunistic records of Agonopterix and Depressaria from continental Spain, and updated checklist (Lepidoptera:Depressariidae). SHIL Rev 46:681–94
Calla B, Wu WY, Dean CAE, Schuler MA, Berenbaum MR (2020) Substrate-specificity of cytochrome P450-mediated detoxification as an evolutionary strategy for specialization on furanocoumarin-containing hostplants: CYP6AE89 in parsnip webworms. Insect Mol Biol 29:112–123. https://doi.org/10.1111/imb.12612
Carroll MJ (2003) Effects of dietary lutein on the parsnip webworm, Depressaria pastinacella (Lepidoptera: Elachistidae). Dissertation, University of Illinois Urbana-Champaign
Clarke JF (1941) Revision of the North American moths of the family Oecophoridae: With descriptions of new genera and species. Proc US Nat Mus 90:33–286. https://doi.org/10.5479/si.00963801.90-3107.33
Clarke JF (1952) Host Relationships of moths of the genera Depressaria and Agonopterix: With descriptions of new species. Smithson Misc Collect 117:1–20
Crankshaw DL, Hetnarski K, Wilkinson CF (1979) Purification and characterization of NADPH-cytochrome C reductase from the midgut of the southern armyworm (Spodoptera eridania). Biochem J 181:593–605. https://doi.org/10.1042/bj1810593
Dhar P, Heckler I, Garcia A, Santos J (2014) Phytochemical analysis and extraction/isolation and characterization of a new furanocoumarin from Heracleum maximum. Planta Med 80:PD65. https://doi.org/10.1055/s-0034-1382486
Ehrlich PR, Raven PH (1964) Butterflies and Plants: A study in coevolution. Evolution 18:586–608. https://doi.org/10.1111/j.1558-5646.1964.tb01674.x
Harrison T, Dean CAE, Parks K, Berenbaum MR (2016) Depressaria depressana (Fabricius) (Depressariidae), new to the Midwestern USA. J Lepid Soc 70:169–173. https://doi.org/10.18473/lepi.70i2.a15
Hodges RW (1974) The moths of America North of Mexico. England, London
Huemer P (1998) Endemische Schmetterlinge der Alpen–ein Überblick (Lepidoptera). Stapfia 55:229–256
Iglesias C, Sinobas J, Varés L (2002) Hasenfussia erinaceella (Staudinger, 1870)(Lepidoptera, Depressaridae), un taladro del cardo 28:103–106
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Krone W (1911) Neubeschreibungen einiger arten und varietäten von microlepidopteren. Jahresbericht Des Wiener Entomologischen Vereins 21:39–42
Landry JF, Nazari V, Dewaard JR, Mutanen M, Lopez-Vaamonde C, Huemer P, Hebert PD (2013) Shared but overlooked: 30 species of Holarctic Microlepidoptera revealed by DNA barcodes and morphology. Zootaxa 3749:1–93. https://doi.org/10.11646/zootaxa.3749.1.1
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. https://doi.org/10.1093/molbev/mss020
Loxdale HD, Harvey JA (2016) The ‘generalism’ debate: misinterpreting the term in the empirical literature focusing on dietary breadth in insects. Biol J Linnean Soc 119:265–282. https://doi.org/10.1111/bij.12816
Mao W, Berhow MA, Zangerl AR, Mcgovern J, Berenbaum MR (2006) Cytochrome P450-mediated metabolism of xanthotoxin by Papilio multicaudatus. J Chem Ecol 32:523–536. https://doi.org/10.1007/s10886-005-9018-3
McKenna DD, Berenbaum MR (2003) A field investigation of Depressaria (Elachistidae) host plants and ecology in the Western United States. J Lepid Soc 57:36–42
Nitao JK, Berenbaum MR (1988) Laboratory rearing of the parsnip webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae). Ann Entomol Soc Am 81:485–487. https://doi.org/10.1093/aesa/81.3.485
Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey J (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67. https://doi.org/10.1080/10635150490264699
O’Neil T, Johnson JA, Webster D, Gray CA (2013) The Canadian medicinal plant Heracleum maximum contains antimycobacterial diynes and furanocoumarins. J Ethnopharmacol 147:232–237. https://doi.org/10.1016/j.jep.2013.03.009
Opler PA, Powell JA (1996) Moths of Western North America. 4.Distribution of "Oecophoridae"(sense of Hodges 1983) of Western NorthAmerica. Dissertation, Colorado State University
Ottenlips MV, Feist MA, Mansfield DH, Plunkett GM, Buerki S, Smith JF (2020) Evolutionary origins of three rare alpine-endemic species of Lomatium (Apiaceae) in the Wallowa and Elkhorn Mountains of Northeastern Oregon. Int J Plant Sci 181:748–765.https://doi.org/10.1086/709373
Ovsyannikova EI, Grichanov IYa (2021) Depressaria depressana (F.) - Purple Carrot-seed Moth. Interactive Agricultural Ecological Atlas of Russia and Neighboring Countries. Economic Plants and their Diseases, Pests and Weeds. http://www.agroatlas.ru/en/content/pests/Depressaria_depressana/index.html. Accessed 28 March 2021
Palm E (1989) [Oecophoridae (Lepidoptera) of Northern Europe – with special reference to Denmark]. Stenstrup, Denmark, pp.247 [in Danish]
Passoa SC (1995) Larval and pupal systematics of Nearctic Amphisbatinae and Depressariinae (Lepidoptera: Oecophoridae). Dissertation, University of Illinois, Urbana-Champaign.
Petschenka G, Halitschke R, Züst T, Roth A, Stiehler S, Tenbusch L, Hartwig C, Moreno Gámez JF, Trusch R, Deckert J, Chalušová K (2022) Sequestration of defenses against predators drives specialized host plant associations in preadapted milkweed bugs (Heteroptera: Lygaeinae). Am Nat 199:E211-228. https://doi.org/10.1086/719196
Requena E, Joaquim J, De-Gregorio P (2014) Contribució al coneixement del gènere Depressaria Haworth, 1812 a Catalunya i Espanya (Lepidoptera: Depressariidae). Butll Soc Cat Lep 105:13–30
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Ratnasingham S, Hebert PD (2007) BOLD: The Barcode of Life data system (http://www.barcodinglife.org). Mol Ecol Notes 7:355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
Rothwell EM, Holeski LM (2020) Phytochemical defences and performance of specialist and generalist herbivores: a meta-analysis. Ecol Entomol 45:396–405. https://doi.org/10.1111/een.12809
Sarker SD, Nahar L (2017) Progress in the chemistry of naturally occurring coumarins. Prog Chem Org Nat Prod 106:241–304. https://doi.org/10.1007/978-3-319-59542-9_3
Scriber JM, Feeny P (1979) Growth of Herbivorous Caterpillars in Relation to Feeding Specialization and to the Growth Form of Their Food Plants. Ecology 60:829–850. https://doi.org/10.2307/1936618
Smilanich AM, Fincher RM, Dyer LA (2016) Does plant apparency matter? Thirty years of data provide limited support but reveal clear patterns of the effects of plant chemistry on herbivores. New Phytol 210:1044–1057. https://doi.org/10.2307/newphytologist.210.3.1044
Sperling FA, Feeny P (1995) Umbellifer and composite feeding in Papilio: Phylogenetic frameworks and constraints on caterpillars. In: Scriber JM, Tsubaki Y, Lederhouse RC (eds) Swallowtail Butterflies: Their Ecology and Evolutionary Biology. Scientific Publishers, Gainesville, pp 299–306
Stamatakis A (2014) RAxML version 8: A Tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Thompson JN, Price PW (1977) Plant plasticity, phenology, and herbivore dispersion: wild parsnip and the parsnip webworm. Ecology 58:1112–1119. https://doi.org/10.2307/1936931
Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Phys 5:229–288. https://doi.org/10.1016/S0065-2806(08)60230-1
Walsingham Lord T De G (1881) On some North-American Tineidae. P Zool Soc London 1881:301–325
Wieser C, Huemer P (1997) Bemerkenswerte Nachweise von Schmetterlingen aus Kärnten (Lepidoptera). na
Yu Y, Blair C, He X (2020) RASP 4: Ancestral state reconstruction tool for multiple genes and characters. Mol Biol Evol 37:604–606. https://doi.org/10.1093/molbev/msz257
Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evol 57: 806–815. https://doi.org/10.1111/j.0014-3820.2003.tb00292.x
Zobel AM, Brown SA (1990) Dermatitis-inducing furanocoumarins on leaf surfaces of eight species of rutaceous and umbelliferous plants. J Chem Ecol 16:693–700. https://doi.org/10.1007/BF01016480
Zobel AM, March RE (1993) Autofluorescence reveals different histological localizations of furanocoumarins in fruit of some umbelliferae and leguminosae. Ann Bot 71:251–255.https://doi.org/10.1006/anbo.1993.1032
Acknowledgements
We thank Jack Easley for assistance with field work in Illinois, Drs. Ling-Hsiu Liao and Bernarda Calla for help with midgut bioassay preparations, and Dr. James Whitfield for advice on phylogenetic analyses.
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The work reported in this manuscript was supported by funds associated with the Swanlund Endowed Chair awarded to May Berenbaum.
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The research was conceived by CAED and MRB, fieldwork was conducted by CAED, midgut bioassays and HPLC analysis were performed by CAED and WYW, gravimetric estimates of performance were calculated by CAED, phylogenetic analysis was conducted by CAED and AK, and the manuscript was drafted by CAED and revised by AK, WYW, and MRB.
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Dean, C.A.E., Katz, A.D., Wu, WY. et al. Degree of Dietary Specialization on Furanocoumarin-Containing Hostplants in a Newly Invasive Web Building Caterpillar. J Chem Ecol 48, 850–866 (2022). https://doi.org/10.1007/s10886-022-01389-9
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DOI: https://doi.org/10.1007/s10886-022-01389-9