Abstract
Females of two click beetle species, Cardiophorus tenebrosus and C. edwardsi (Coleoptera: Elateridae), produce methyl (3R,6E)-2,3-dihydrofarnesoate as their sex pheromone. We had serendipitously discovered that males of both species were also strongly attracted to (R)-fuscumol acetate ((E)-6,10-dimethylundeca-5,9-dien-2-yl acetate), a known longhorned beetle (Coleoptera: Cerambycidae) pheromone, due to its structural similarities to the click beetle pheromone. To further investigate the specificity of the responses of Cardiophorus males, additional analogs with different chain lengths and structural relationships compared to the natural pheromone were synthesized and tested. In field and electroantennogram bioassays, only fuscumol propionate ((E)-6,10-dimethylundeca-5,9-dien-2-yl propionate) elicited strong responses from Cardiophorus males, indicating that they were able to distinguish chain length and spatial relationships between the structural elements. In field trials, C. tenebrosus males were attracted equally to the analog and their natural pheromone, but the pheromone elicited stronger antennal responses from males. In contrast, traps baited with fuscumol propionate caught approximately 26 times as many C. edwardsi males compared to traps baited with the natural pheromone, although the analog elicited significantly smaller antennal responses from C. edwardsi males. Thus, in terms of behavioral responses, fuscumol propionate appears to be acting as a hyperactive pheromone mimic, a phenomenon which has rarely been observed in insect semiochemistry.
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References
Advanced Chemistry Development (2019) ACD/Labs. Software V. 11.02. Toronto, ONT, Canada
Bengtsson M, Rauscher S, Arn H, Sun W-C, Prestwich GD (1990) Fluorine-substituted pheromone components affect the behavior of the grape berry moth. Experientia 46:1211–1213. https://doi.org/10.1007/BF01936940
Briggs GG, Cayley GR, Dawson GW, Griffiths DC, Macaulay EDM, Pickett JA, Pile MM, Wadhams LJ, Woodcock CM (1986) Some fluorine-containing pheromone analogs. Pestic Sci 17:441–448. https://doi.org/10.1002/ps.2780170415
Camps F, Fabriàs G, Gasol V, Guerrero A, Hernández R, Montoya R (1988) Analogs of the sex pheromone of processionary moth Thaumetopoea pityocampa: synthesis and biological activity. J Chem Ecol 14:1331–1346. https://doi.org/10.1007/BF01020138
Cardé RT, Roelofs WL (1977) Attraction of redbanded leafroller moths, Argyrotaenia velutinana, to blends of (Z)-and (E)-11-tridecenyl acetates. J Chem Ecol 3:143–149. https://doi.org/10.1007/BF00994141
Dawson GW, Mudd A, Pickett JA, Pile MM, Wadhams LJ (1990) Convenient synthesis of mosquito oviposition pheromone and a highly fluorinated analog retaining biological activity. J Chem Ecol 16:1779–1789. https://doi.org/10.1007/BF01020494
Eliyahu D, Mori K, Takikawa H, Leal WS, Schal C (2004) Behavioral activity of stereoisomers and a new component of the contact sex pheromone of female German cockroach, Blattella germanica. J Chem Ecol 30:1839–1848. https://doi.org/10.1023/B:JOEC.0000042405.05895.3a
El-Sayed AM (2019) The pherobase: database of pheromones and semiochemicals. https://www.pherobase.com/. Accessed 1 Nov 2019
Grant GG, Langevin D, Liska J, Kapitola P, Chong JM (1996) Olefin inhibitor of gypsy moth, Lymantria dispar, is a synergistic pheromone component of nun moth, L. monacha. Naturwissenschaften 83:328–830. https://doi.org/10.1007/BF01152217
Ho H-Y, Millar JG (2001) Identification and synthesis of a male-produced sex pheromone from the stink bug Chlorochroa sayi. J Chem Ecol 27:1177–1201. https://doi.org/10.1023/A:1010368013235
Hu D-H, He J, Zhou Y-W, Feng J-T, Zhang X (2012) Synthesis and field evaluation of the sex pheromone analogues to soybean pod borer Leguminivora glycinivorella. Molecules 17:12140–12150. https://doi.org/10.3390/molecules171012140
Lucas P, Renou M, Tellier F, Hammoud A, Audemard H, Descoins C (1994) Electrophysiological and field activity of halogenated analogs of (E, E)-8,10-dodecadienol, the main pheromone component, in the codling moth (Cydia pomonella L.). J Chem Ecol 20:489–503. https://doi.org/10.1007/BF02059592
Muraki Y, Taguri T, Yamakawa R, Ando T (2014) Synthesis and field evaluation of stereoisomers and analogues of 5-methylheptadecan-7-ol, an unusual sex pheromone component of the lichen moth, Miltochrista calamina. J Chem Ecol 40:250–258. https://doi.org/10.1007/s10886-014-0405-5
Pesenti C, Viani F (2004) The influence of fluorinated molecules (semiochemicals and enzyme substrate analogues) on the insect communication system. ChemBioChem 5:590–613. https://doi.org/10.1002/cbic.200300829
Renou M, Guerrero A (2000) Insect parapheromones in olfaction research and semiochemical-based pest control strategies. Annu Rev Entomol 45:605–630. https://doi.org/10.1146/annurev.ento.45.1.605
Riba M, Eizaguirre M, Sans A, Quero C, Guerrero A (1994) Inhibition of pheromone action in Sesamia nonagrioides by haloacetate analogues. Pestic Sci 41:97–103. https://doi.org/10.1002/ps.2780410205
Richter C, Schaepe K, Glorius F, Jan Ravoo B (2014) Tailor-made N-heterocyclic carbenes for nanoparticle stabilization. Chem Commun 50:3204–3207. https://doi.org/10.1039/C4CC00654B
Roelofs WL, Comeau A (1971) Sex pheromone perception: synergists and inhibitors for the red-banded leaf roller attractant. J Insect Physiol 17:435–448. https://doi.org/10.1007/BF00987721
SAS Institute Inc. (2019) SAS/STAT 9.4 user’s guide. Cary NC
Serrano JM, Collignon RM, Zou Y, Millar JG (2018) Identification of sex pheromones and sex pheromone mimics for two North American click beetle species (Coleoptera: Elateridae) in the genus Cardiophorus Esch. J Chem Ecol 44:327–338. https://doi.org/10.1007/s10886-018-0940-6
Solari P, Crnjar R, Frongia A, Sollai G, Secci F, Spiga M, Masala C, Liscia A (2007) Oxaspiropentane derivatives as effective sex pheromone analogues in the gypsy moth: electrophysiological and behavioral evidence. Chem Senses 32:755–763. https://doi.org/10.1093/chemse/bjm043
Sun Y, Meng Z, Chen P, Zhang D, Baunach M, Hertweck C, Li A (2016) A concise total synthesis of sespenine, a structurally unusual indole terpenoid from Streptomyces. Org Chem Front 3:368–374. https://doi.org/10.1039/C5QO00416K
Symonds MRE, Elgar MA (2008) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228. https://doi.org/10.1016/j.tree.2007.11.009
US EPA (2019) Estimation Programs Interface Suite™ for Microsoft® Windows, v 4.11. United States Environmental Protection Agency, Washington, DC, USA
Whittaker AM, Dong VM (2015) Nickel-catalyzed dehydrogenative cross-coupling: direct transformation of aldehydes into esters and amides. Angew Chem Int Ed 54:1312–1315. https://doi.org/10.1002/anie.201410322
Acknowledgements
We thank Stacy Hishinuma for providing access to field sites, Rebecca Schmidt-Jeffris and W. Rodney Cooper for assistance with statistics in SAS, and Sean Halloran and J. Steven McElfresh for assistance with field work. We also thank Ring Cardé, Teun Dekker, and John Hildebrand for helpful discussions concerning possible mechanisms.
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This work was funded in part by financial support from the Robert van den Bosch Scholarship to JMS, a UC Riverside Committee on Research grant to JGM, and funding from Hatch project CA-R*ENT-5181-H to JGM.
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JMS and JGM designed the research. JMS, YZ, and JGM conducted the chemical syntheses. JMS performed the experiments, analyzed the data, and wrote the first draft of the manuscript. All authors contributed to the final version of the manuscript.
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Serrano, J.M., Zou, Y. & Millar, J.G. Identification of a hyperactive pheromone analog in field tests of pheromone mimics for two click beetle species in the genus Cardiophorus (Coleoptera: Elateridae). Chemoecology 30, 297–304 (2020). https://doi.org/10.1007/s00049-020-00319-z
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DOI: https://doi.org/10.1007/s00049-020-00319-z