Abstract
The larvae of several species in the hawk moth genus Hyles, including H. euphorbiae, feed on plants of the genus Euphorbia containing phorbol esters and are insensitive to addition of the standard phorbol ester, tetradecanoyl-phorbol-13-acetate (TPA) to their artificial diet. Specialised non-Euphorbia feeding larvae were sensitive, whereas polyphagous ones were insensitive if their natural food plant spectrum also includes Euphorbia. Larvae of Hippotion celerio, an out-group species with polyphagous larvae not using Euphorbia as food plants, were sensitive. A highly conserved sequence of the TPA binding site of the protein kinase C in H. euphorbiae and Hippotion celerio demonstrates that intoxication by phorbol esters is not avoided by preventing target binding. H. euphorbiae larvae showed no vitality loss after chemical destruction of their peritrophic matrix and subsequent TPA treatment. TPA fed larvae that had putatively piperonyl butoxide (PBO)-inhibited cytochrome P450 enzymes also showed no deficits, indicating that this is not the only detoxification pathway in H. euphorbiae. Based on these qualitative results, we postulate that proto-Hyles was polyphagous with the ability to use Euphorbia as food plants. The most ancestral Hyles species presumably remained polyphagous, with the ability to switch to the toxic food plants if necessary. Within the youngest, Palearctic radiation, the species specialised on non-Euphorbia plants subsequently lost detoxification abilities, albeit not to 100%. The species in South America, the origin of Hyles, can detoxify TPA, indicating this ability to be a plesiomorphic character state within the genus that enabled its adaptive radiation in the Palearctic, the distribution and diversity centre of Euphorbia.
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References
Aardema ML, Zhen Y, Andolfatto P (2012) The evolution of cardenolide resistant forms of Na+, K+ ATPase in Danainae butterflies. Mol Ecol 21:340–349
Ali H, Qaiser M (2009) The ethnobotany of Chitral valley, Pakistan with particular reference to medicinal plants. Pak J Bot 41:2009–2041
Ali R, Ali R, Jaimini A, Nishad DK, Mittal G, Chaurasia OP, Kumar R, Bhatnagar A, Singh SB (2012) Acute and sub acute toxicity and efficacy studies of Hippophae rhamnoides based herbal antioxidant supplement. Indian J Pharmacol 44:504–508
Angel P, Imagawa M, Chiu R, Stein B, Imbra RJ, Rahmsdorf HJ et al (1987) Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell 49:729–739
Attie M, Kitching IJ, Veslot J (2010) Patterns of larval hostplant usage among hawkmoths (Lepidoptera, Sphingidae) from La Réunion, with a comparison of the Mascarenes with other regions of the world. Rev Écol (Terre Vie) 65:3–44
Barth MB, Buchwalder K, Kawahara AY, Zhou X, Liu S, Krezdorn N, Rotter B, Horres R, Hundsdoerfer AK (2018) Functional characterization of the Hyles euphorbiae hawkmoth transcriptome reveals strong expression of phorbol ester detoxification and seasonal cold hardiness genes. Front Zool 15:20
Blumberg PM (1988) Protein kinase C as the receptor for the phorbol ester tumor promoters: sixth Rhoads memorial award lecture. Cancer Res 48:1–8
Brose N, Rosenmund C (2002) Move over protein kinase C, you’ve got company: alternative cellular effectors of diacylglycerol and phorbol esters. J Cell Sci 115:4399–4411
Bury NR, Schnell S, Hogstrand C (2014) Gill cell culture systems as models for aquatic environmental monitoring. J Exper Biol 217:639–650
Daniel F (1966) Eine Sphingidenausbeute aus Nepal (Lepidoptera). Ergebnisse des Forschungsunternehmens Nepal Himalaya. Khumbu Himal 1:176–181
Danner F, Eitschberger U, Surholt B (1998) Die Schwärmer der westlichen Palaearktis. Bausteine zu einer Revision (Lepidoptera: Sphingidae). Herbipoliana 4:1–368
De Freina J, Geck M (2014) Beitrag zur Hyles centralasiae-siehei-Artengruppe. Zur Biologie, Ökologie, Verbreitung und geographischen Variabilität von H. siehei (Püngeler, 1903) und Reinterpretation von Hyles svetlana Shovkoon, 2010 (Lepidoptera: Sphingidae). Entomol Z 124:67–95
Dobler S, Dalla S, Wagschal V, Agrawal AA (2012) Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. PNAS 109:13040–13045
Dove WE (1947) Piperonyl butoxide, a new and safe insecticide for the household and field. Am J Trop Med 27:339–345
Harbich H (1994) Erfahrungen bei der Aufzucht von Sphingidenraupen mit einem Kombinationsfutter (Lepidoptera: Sphingidae). Entomol Z 104:112–117
Hecker E (1968a) Cocarcenogeneic principles from the seed oil of Croton tiglium and from other Euphorbiaceae. Cancer Res 28:2338–2349
Hecker E (1968b) Cocarcenogenic substances from Euphorbiaceae. Planta Med Suppl, p 24
Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Ann Rev Entom 54:285–302
Holzinger F, Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch (Danaus plexippus): Role of an amino acid substitution in the ouabain binding site of Na+, K+-ATPase. J Chem Ecol 22:1921–1937
Holzinger F, Frick C, Wink M (1992) Molecular basis for the insensitivity of the Monarch (Danaus plexippus) to cardiac glycosides. FEBS Lett 314:477–480
Hundsdoerfer AK, Tshibangu JN, Wetterauer B, Wink M (2005) Sequestration of phorbol esters by aposematic larvae of Hyles euphorbiae (Lepidoptera: Sphingidae)? Chemoecology 15:261–267
Hundsdoerfer AK, Rubinoff D, Attié M, Wink M, Kitching IJ (2009) A revised molecular phylogeny of the globally distributed hawkmoth genus Hyles (Lepidoptera: Sphingidae), based on mitochondrial and nuclear DNA sequences. Mol Phyl Evol 52:852–865
Hundsdoerfer AK, Mende MB, Harbich HC, Pittaway AR, Kitching IJ (2011) Larval pattern morphotypes in the Western Palaearctic Hyles euphorbiae complex (Lepidoptera: Sphingidae: Macroglossinae). Insect Syst Evol 42:41–86
Hundsdoerfer AK, Päckert M, Kehlmaier C, Strutzenberger P, Kitching IJ (2017) Museum archives revisited: central Asiatic hawkmoths reveal exceptionally high late Pliocene species diversification (Lepidoptera, Sphingidae). Zool Scr 46:552–570
Kinsler S, Levi PE, Hodgson E (1990) Relative contributions of the cytochrome P450 and flavin-containing monooxygenases to the microsomal oxidation of phorate following treatment of mice with phenobarbital, hydrocortisone, acetone, and piperonyl butoxide. Pesticide Biochem Physiol 37:174–181
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Labeyrie E, Dobler S (2004) Molecular adaptation of Chrysochus leaf beetles to toxic compounds in their food plants. Mol Biol Evol 21:218–221
Leatherman D (2014) White-lined Sphinx Moth. Colorado Birds 48:312–315
Liu N, Li M, Gong Y, Liu F, Li T (2015) Cytochrome P450s—their expression, regulation, and role in insecticide resistance. Pesticide Biochem Physiol 120:77–81
Manojlovic B, Keresi T (1997) Previous studies of phytophagous insects for biological control of plants from the genus Euphorbia L. (Euphorbiales: Euphorbiaceae J St. Hill.). Zast Bilja 48:23–48
Mende MB, Bartel M, Hundsdoerfer AK (2016) A comprehensive phylogeography of the Hyles euphorbiae complex (Lepidoptera: Sphingidae) indicates a ‘glacial refuge belt’. Sci Rep 6:29527
Moss Rev MA (1912) II. On the Sphingidae of Peru. Transact Zool Soc London 20:73–134
Moulds MS (1998) New larval foodplants for Australian hawk moths (Lepidoptera: Sphingidae). Austral Entomol 25:13–22
Nishizuka Y (1984) The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308:693–698
Ohno S, Konno Y, Akita Y, Yano A, Suzuki K (1990) A point mutation at the putative ATP-binding site of protein kinase C alpha abolishes the kinase activity and renders it down-regulation-insensitive. J Biol Chem 265:6296–6300
Ojani R, Liu P, Fu X, Zhu J (2016) Protein kinase C modulates transcriptional activation by the juvenile hormone receptor methoprene-tolerant. Insect Biochem Mol Biol 70:44–52
Ott HH, Hecker E (1981) Highly irritant ingenane type diterpene esters from Euphorbia cyparissias L. Experientia 37:88–91
Pakpour N, Camp L, Smithers HM, Wang B, Tu Z, Nadler SA, Luckhart S (2013) Protein kinase C-dependent signaling controls the midgut epithelial barrier to malaria parasite infection in anopheline mosquitoes. PloS One 8:e76535
Parker PJ, Coussens L, Totty N, Rhee L, Young S, Chen E, Stabel S, Waterfield MD, Ullrich A (1986) The complete primary structure of protein kinase C—the major phorbol ester receptor. Science 233:853–859
Peirson JA, Riina R, Mayfield MH, Ferguson CJ, Urbatsch LE, Berry PE (2014) Phylogenetics and taxonomy of the New World leafy spurges, Euphorbia section Tithymalus (Euphorbiaceae). Bot J Linn Soc 175:191–228
Petschenka G, Wagschal V, Tschirnhaus MV, Donath A, Dobler S (2017) Convergently evolved toxic secondary metabolites in plants drive the parallel molecular evolution of insect resistance. Am Nat 190:S29–S43
Pittaway TA (2018) Sphingidae of the western palaearctic. http://tpittaway.tripod.com/sphinx/list.htm. Accessed 18 Sept 2018
Riina R, Peirson JA, Geltman DV, Molero J, Frajman B, Pahlevani A et al (2013) A worldwide molecular phylogeny and classification of the leafy spurges, Euphorbia subgenus Esula (Euphorbiaceae). Taxon 62:316–342
Rosenthal A, Rhee L, Yadegari R, Paro R, Ullrich A, Goeddel DV (1987) Structure and nucleotide sequence of a Drosophila melanogaster protein kinase C gene. EMBO J 6:433
Shi QW, Su XH, Kiyota H (2008) Chemical and pharmacological research of the plants in genus Euphorbia. Chem Rev 108:4295–4327
Ureta RE, Donoso RB (1956) Revisión de la familia Sphingidae (Lep. Het.) en Chile. Apart Bol Mus Nac Hist Nat 26:237–256
Vanselow KA, Samim C, Breckle SW (2016) Preserving a comprehensive vegetation knowledge base—an evaluation of four historical Soviet vegetation maps of the Western Pamirs (Tajikistan). PLoS One 11:e0148930
Wang P, Granados RR (2000) Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 30:135–143
Wang P, Granados RR (2001) Molecular structure of the peritrophic matrix (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Phys 47:110–118
Wink M, Theile V (2002) Alkaloid tolerance in Manduca sextra and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecol 12:29–46
Wink M, Koschmieder C, Sauerwein M, Sporer F (1997) Phorbol esters of Jatropha curcas—Biological activities and potential applications. In: Gübitz GM, Mittelbach M, Trabi M (eds) Biofuel and industrial products from Jatropha curcas. Dbv-Verlag Univ, Graz
Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P (2012) Parallel molecular evolution in an herbivore community. Science 337:1634–1637
Zu Y, Li C, Fu Y, Zhao C (2006) Simultaneous determination of catechin, rutin, quercetin kaempferol and isorhamnetin in the extract of sea buckthorn (Hippophae rhamnoides L.) leaves by RP-HPLC with DAD. J Pharmac Biomed Anal 41:714–719
Acknowledgements
Thanks go to Ben Barth, Franziska Bauer, Gerda Buder, Stephanie Fiedler, Christin Großmann, Richard Mally, Anja Rauh, Francesca Vegliante and especially Christian Schmidt for laboratory support in larval rearing. We sincerely thank Ian J. Kitching (London) and Tony Pittaway (Wallingford) for valuable discussions. The ‘Deutsche Forschungsgemeinschaft’ provided funding (DFG HU 1561/1–1, 1–2). The feeding experiments were carried out in the Molecular Laboratory, Senckenberg Dresden (SNSDML).
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Communicated by Günther Raspotnig.
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Hundsdoerfer, A.K., Buchwalder, K., O’Neill, M.A. et al. Chemical ecology traits in an adaptive radiation: TPA-sensitivity and detoxification in Hyles and Hippotion (Sphingidae, Lepidoptera) larvae. Chemoecology 29, 35–47 (2019). https://doi.org/10.1007/s00049-018-0274-4
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DOI: https://doi.org/10.1007/s00049-018-0274-4