The search for mates and food is mediated by volatile chemicals. Insects sense food odorants and sex pheromones through odorant receptors (ORs) and pheromone receptors (PRs), which are expressed in olfactory sensory neurons. Molecular phylogenetics of ORs, informed by behavioral and functional data, generates sound hypotheses for the identification of semiochemicals driving olfactory behavior. Studying orthologous receptors and their ligands across taxa affords insights into the role of chemical communication in reproductive isolation and phylogenetic divergence. The female sex pheromone of green budworm moth Hedya nubiferana (Lepidoptera, Totricidae) is a blend of two unsaturated acetates, only a blend of both elicits male attraction. Females produce in addition codlemone, which is the sex pheromone of another tortricid, codling moth Cydia pomonella. Codlemone also attracts green budworm moth males. Concomitantly, green budworm and codling moth males are attracted to the host plant volatile pear ester. A congruent behavioral response to the same pheromone and plant volatile in two tortricid species suggests co-occurrence of dedicated olfactory channels. In codling moth, one PR is tuned to both compounds, the sex pheromone codlemone and the plant volatile pear ester. Our phylogenetic analysis finds that green budworm moth expresses an orthologous PR gene. Shared ancestry, and high levels of amino acid identity and sequence similarity, in codling and green budworm moth PRs offer an explanation for parallel attraction of both species to the same compounds. A conserved olfactory channel for a sex pheromone and a host plant volatile substantiates the alliance of social and habitat signals in insect chemical communication. Field attraction assays confirm that in silico investigations of ORs afford powerful predictions for an efficient identification of behavior-modifying semiochemicals, for an improved understanding of the mechanisms of host plant attraction in insect herbivores and for the further development of sustainable insect control.

ChemTica Internacional Heredia Costa Rica

Corporación Colombiana de Investgación Agropecuaria Agrosavia Mosquera Colombia

Department to Plant Protection Biology Swedish University of Agricultural Sciences Alnarp Sweden

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Faculty of Health and Life Sciences Linnaeus University Kalmar Sweden

Molecular Ecology and Evolution Lab Department of Biology Lund University Lund Sweden

Plant Protection Institute CAR Budapest Hungary

See more in PubMed

Ansebo, L. , Ignell, R. , Löfqvist, J. , & Hansson, B. S. (2005). Responses to sex pheromone and plant odours by olfactory receptor neurons housed in sensilla auricillica of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). Journal of Insect Physiology, 51, 1066–1074. 10.1016/j.jinsphys.2005.05.003 PubMed DOI

Arguello, J. R. , Cardoso‐Moreira, M. , Grenier, J. K. , Gottipati, S. , Clark, A. G. , & Benton, R. (2016). Extensive local adaptation within the chemosensory system following Drosophila melanogaster's global expansion. Nature Communications, 7, 11855 10.1038/ncomms11855 PubMed DOI PMC

Arn, H. , Rauscher, S. , & Schmid, A. (1979). Sex attractant formulations and traps for the grape moth Eupoecilia ambiguella Hb. Mitteilungen Der Schweizer Entomologischen Gesellschaft, 52, 49–55.

Arn, H. , Schwarz, C. , Limacher, H. , & Mani, E. (1974). Sex attractant inhibitors of the codling moth Laspeyresia pomonella L. Experientia, 30, 1142–1144. 10.1007/BF01923655 PubMed DOI

Arn, H. , Städler, E. , & Rauscher, S. (1975). The electroantennographic detector ‐ a selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Zeitschrift Für Naturforschung, 30c, 722–725. 10.1515/znc-1975-11-1204 DOI

Bäckman, A.‐C. , Anderson, P. , Bengtsson, M. , Löfqvist, J. , Unelius, C. R. , & Witzgall, P. (2000). Antennal response of codling moth males, Cydia pomonella (L.) (Lepidoptera: Tortricidae), to the geometric isomers of codlemone and codlemone acetate. Journal of Comparative Physiology A, 186, 513–519. 10.1007/s003590000 PubMed DOI

Bäckman, A.‐C. , Bengtsson, M. , & Witzgall, P. (1997). Pheromone release by individual females of codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae). Journal of Chemical Ecology, 23, 807–815. 10.1023/B:JOEC.0000006412.16914.09 DOI

Baker, T. C. (2002). Mechanism for saltational shifts in pheromone communication systems. Proceedings of the National Academy of Science USA, 99, 13368–13370. 10.1073/pnas.222539799 PubMed DOI PMC

Bengtsson, J. M. , Gonzalez, F. , Cattaneo, A. M. , Montagne, N. , Walker, W. B. , Bengtsson, M. , … Witzgall, P. (2014). A predicted sex pheromone receptor of codling moth Cydia pomonella detects the plant volatile pear ester. Frontiers in Ecology Evolution, 2, 33 10.3389/fevo.2014.00033 DOI

Bengtsson, J. M. , Trona, F. , Montagne, N. , Anfora, G. , Ignell, R. , Witzgall, P. , & Jacquin‐Joly, E. (2012). Putative chemosensory receptors of the codling moth, Cydia pomonella, identified by antennal transcriptome analysis. PLoS One, 7(2), e31620 10.1371/journal.pone.0031620 PubMed DOI PMC

Bengtsson, M. , Jaastad, G. , Knudsen, G. , Kobro, S. , Bäckman, A.‐C. , Pettersson, E. , & Witzgall, P. (2006). Plant volatiles mediate attraction to host and non‐host plant in apple fruit moth, Argyresthia conjugella . Entomolgia Experimentalis Et Applicata, 118, 77–85. 10.1111/j.1570-7458.2006.00359.x DOI

Bengtsson, M. , Liljefors, T. , Hansson, B. S. , Löfstedt, C. , & Copaja, S. V. (1990). Structure‐activity relationships for chain‐shortened analogs of (Z)‐5‐decenyl acetate, a pheromone component of the turnip moth, Agrotis segetum . Journal of Chemical Ecology, 16, 667–684. 10.1007/BF01016478 PubMed DOI

Borrero‐Echeverry, F. , Bengtsson, M. , Nakamuta, K. , & Witzgall, P. (2018). Plant odour and sex pheromone are integral elements of specific mate recognition in an insect herbivore. Evolution, 72, 2225–2233. 10.1111/evo.13571 PubMed DOI PMC

Boughman, J. W. (2002). How sensory drive can promote speciation. Trends in Ecology and Evolution, 17, 571–577. 10.1016/S0169-5347(02)02595-8 DOI

Bradley, J. D. , Tremewan, W. G. , & Smith, A. (1979). British tortricoid moths. Tortricidae: Olethreutinae. London, UK: The Ray Society.

Braunschmid, H. , Mükisch, B. , Rupp, T. , Schäffler, I. , Zito, P. , Birtele, D. , & Dötterl, S. (2017). Interpopulation variation in pollinators and floral scent of the lady’s‐slipper orchid Cypripedium calceolus L. Arthropod‐Plant Interactions, 11, 363–379. 10.1007/s11829-017-9512-x DOI

Bruce, T. J. A. , & Pickett, J. A. (2011). Perception of plant volatile blends by herbivorous insects ‐ finding the right mix. Phytochemistry, 72, 1605–1611. 10.1016/j.phytochem.2011.04.011 PubMed DOI

Caballero‐Vidal, G. , Bouysset, C. , Grunig, H. , Fiorucci, S. , Montagné, N. , Golebiowski, J. , & Jacquin‐Joly, E. (2020). Machine learning decodes chemical features to identify novel agonists of a moth odorant receptor. Scientific Reports, 10(1), 1–9. 10.1038/s41598-020-58564-9 PubMed DOI PMC

Cao, D. , Liu, Y. , Wei, J. , Liao, X. , Walker, W. B. , Li, J. , & Wang, G. (2014). Identification of candidate olfactory genes in Chilo suppressalis by antennal transcriptome analysis. International Journal of Biological Science, 10, 846–860. 10.7150/ijbs.9297 PubMed DOI PMC

Cao, S. , Huang, T. , Shen, J. , Liu, Y. , & Wang, G. (2020). An orphan pheromone receptor affects the mating behavior of Helicoverpa armigera . Frontires in Physiology, 11, 413 10.3389/fphys.2020.00413 PubMed DOI PMC

Carde, A. M. , Baker, T. C. , & Carde, R. T. (1979). Identification of a four‐component sex pheromone of the female Oriental fruit moth, Grapholitha molesta (Lepidoptera: Tortricidae). Journal of Chemical Ecology, 5, 423–427. 10.1007/BF00987927 DOI

Carde, R. T. , & Minks, A. K. (1995). Control of moth pests by mating disruption: Successes and constraints. Annual Review of Entomology, 40, 559–585. 10.1146/annurev.en.40.010195.003015 DOI

Carson, R. (1962). Silent Spring. Boston, MA: Houghton Mifflin.

Cattaneo, A. M. , Gonzalez, F. , Bengtsson, J. M. , Corey, E. A. , Jacquin‐Joly, E. , Montagne, N. , … Bobkov, Y. V. (2017). Candidate pheromone receptors from the insect pest Cydia pomonella respond to pheromone and kairomone components. Scientific Reports, 7, 41105 10.1038/srep41105 PubMed DOI PMC

Chandler, D. , Bailey, A. S. , Tatchell, G. M. , Davidson, G. , Greaves, J. , & Grant, W. P. (2011). The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society of London B, 366, 1987–1998. 10.1098/rstb.2010.0390 PubMed DOI PMC

Chang, X. Q. , Nie, X. P. , Zhang, Z. , Zeng, F. F. , Lv, L. , Zhang, S. , & Wang, M. Q. (2017). De novo analysis of the oriental armyworm Mythimna separata antennal transcriptome and expression patterns of odorant‐binding proteins. Comparative Biochemistry and Physiology D, 22, 120–130. 10.1016/j.cbd.2017.03.001 PubMed DOI

Chepurwar, S. , Gupta, A. , Haddad, R. , & Gupta, N. (2019). Sequence‐based prediction of olfactory receptor responses. Chemical Senses, 44, 693–703. 10.1093/chemse/bjz078 PubMed DOI PMC

Chmiel, J. A. , Daisley, B. A. , Burton, J. P. , & Reid, G. (2019). Deleterious effects of neonicotinoid pesticides on Drosophila melanogaster immune pathways. MBio, 10, e01395‐19 10.1128/mBio.01395-19 PubMed DOI PMC

Clyne, P. J. , Warr, C. G. , Freeman, M. R. , Lessing, D. , Kim, J. , & Carlson, J. R. (1999). A novel family of divergent seven‐transmembrane proteins: Candidate odorant receptors in Drosophila . Neuron, 22, 327–338. 10.1016/S0896-6273(00)81093-4 PubMed DOI

Conchou, L. , Lucas, P. , Meslin, C. , Proffit, M. , Staudt, M. , & Renou, M. (2019). Insect odorscapes: From plant volatiles to natural olfactory scenes. Frontiers in Physiology, 10, 972 10.3389/fphys.2019.00972 PubMed DOI PMC

Corcoran, J. A. , Jordan, M. D. , Thrimawithana, A. H. , Crowhurst, R. N. , & Newcomb, R. D. (2015). The peripheral olfactory repertoire of the lightbrown apple moth, Epiphyas p ostvittana . PLoS One, 10, e0128596 10.1371/journal.pone.0128596 PubMed DOI PMC

Couto, A. , Alenius, M. , & Dickson, B. J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current Biology, 15, 1535–1547. 10.1016/j.cub.2005.07.034 PubMed DOI

De Fouchier, A. , Walker, W. B. , Montagne, N. , Steiner, C. , Binyameen, M. , Schlyter, F. , … Jacquin‐Joly, E. (2017). Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nature Communications, 8, 1–11. 10.1038/ncomms15709 PubMed DOI PMC

Deutsch, C. A. , Tewksbury, J. J. , Tigchelaar, M. , Battisti, D. S. , Merrill, S. C. , Huey, R. B. , & Naylor, R. L. (2018). Increase in crop losses to insect pests in a warming climate. Science, 361, 916–919. 10.1126/science.aat3466 PubMed DOI

Dietrich, M. (2003). Richard Goldschmidt: Hopeful monsters and other 'heresies'. Nature Reviews Genetics, 4, 68–74. 10.1038/nrg979 PubMed DOI

Dobritsa, A. A. , Van Naters, W. V. D. G. , Warr, C. G. , Steinbrecht, R. A. , & Carlson, J. R. (2003). Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron, 37, 827–841. 10.1016/S0896-6273(03)00094-1 PubMed DOI

Dong, J. , Song, Y. , Li, W. , Shi, J. , & Wang, Z. (2016). Identification of putative chemosensory receptor genes from the Athetis dissimilis antennal transcriptome. PLoS One, 11, e0147768 10.1371/journal.pone.0147768 PubMed DOI PMC

Du, L. , Zhao, X. , Liang, X. , Gao, X. , Liu, Y. , & Wang, G. (2018). Identification of candidate chemosensory genes in Mythimna separata by transcriptomic analysis. BMC Genomics, 19, 518 10.1186/s12864-018-4898-0 PubMed DOI PMC

El‐Sayed, A. M. (2019). The pherobase: database of pheromones and semiochemicals. www.pherobase.com

El‐Sayed, A. M. , Suckling, D. M. , Byers, J. A. , Jang, E. B. , & Wearing, C. H. (2009). Potential of “lure and kill” in long‐term pest management and eradication of invasive species. Journal of Economic Entomology, 102, 815–835. 10.1603/029.102.0301 PubMed DOI

El‐Sayed, A. , Unelius, R. C. , Liblikas, I. , Löfqvist, J. , Bengtsson, M. , & Witzgall, P. (1998). Effect of codlemone isomers on codling moth (Lepidoptera: Tortricidae) male attraction. Environmental Entomology, 27, 1250–1254. 10.1093/ee/27.5.1250 DOI

Evenden, M. L. , & Silk, P. J. (2016). The influence of Canadian research on semiochemical‐based management of forest insect pests in Canada. The Canadian Entomologist, 148, S170–S209. 10.4039/tce.2015.17 DOI

Feng, B. , Guo, Q. , Zheng, K. , Qin, Y. , & Du, Y. (2017). Antennal transcriptome analysis of the piercing moth Oraesia emarginata (Lepidoptera: Noctuidae). PLoS One, 12, e0179433 10.1371/journal.pone.0179433 PubMed DOI PMC

Fleischer, J. , Pregitzer, P. , Breer, H. , & Krieger, J. (2018). Access to the odor world: Olfactory receptors and their role for signal transduction in insects. Cellular and Molecular Life Sciences, 75, 485–508. 10.1007/s00018-017-2627-5 PubMed DOI PMC

Frerot, B. , Priesner, E. , & Gallois, M. (1979). A sex attractant for the green budworm moth, Hedya nubiferana . Zeitschrift Für Naturforschung, 34c, 1248–1252. 10.1515/znc-1979-1229 DOI

Gonzalez, F. , Bengtsson, J. M. , Walker, W. B. , Rodrigues Sousa, M. F. , Cattaneo, A. M. , Montagné, N. , … Bengtsson, M. (2015). A conserved odorant receptor detects the same 1‐indanone analogs in a tortricid and a noctuid moth. Frontires in Ecology and Evolution, 3, 131 10.3389/fevo.2015.00131 DOI

Gonzalez, F. , Sousa, M. , Conchou, L. , Walker, W. B. , Chakraborty, A. , Karlsson, M. , … Witzgall, P. (2020). An endophytic yeast odorant mediates codling moth attraction to apple (submitted).

Gonzalez, F. , Witzgall, P. , & Walker, W. B. (2016). Protocol for heterologous expression of insect odourant receptors in Drosophila . Frontiers in Ecology Evolution, 4, 24 10.3389/fevo.2016.00024 DOI

Gonzalez, F. , Witzgall, P. , & Walker, W. B. (2017). Antennal transcriptomes of three tortricid moths reveal putative conserved chemosensory receptors for social and habitat olfactory cues. Scientific Reports, 7, 41829 10.1038/srep41829 PubMed DOI PMC

Grabe, V. , Strutz, A. , Baschwitz, A. , Hansson, B. S. , & Sachse, S. (2015). Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster . Journal of Comparative Neurology, 523, 530–544. 10.1002/cne.23697 PubMed DOI

Gregg, P. C. , Del Socorro, A. P. , & Landolt, P. J. (2018). Advances in attract‐and‐kill for agricultural pests: Beyond pheromones. Annual Review of Entomology, 63, 453–470. 10.1146/annurev-ento-031616-035040 PubMed DOI

Hallem, E. A. , Ho, M. G. , & Carlson, J. R. (2004). The molecular basis of odor coding in the Drosophila antenna. Cell, 117, 965–979. 10.1016/j.cell.2004.05.012 PubMed DOI

Hathaway, D. O. , McGovern, T. P. , Beroza, M. , Moffitt, H. R. , McDonough, L. M. , & Butt, B. A. (1974). An inhibitor of sexual attraction of male codling moths to a synthetic sex pheromone and virgin females in traps. Environmental Entomology, 3, 522–524. 10.1093/ee/3.3.522 DOI

Jactel, H. , Verheggen, F. , Thiéry, D. , Escobar‐Gutiérrez, A. J. , Gachet, E. , & Desneux, N. , Neonicotinoids Working Group (2019). Alternatives to neonicotinoids. Environment International, 129, 423–429. 10.1016/j.envint.2019.04.045 PubMed DOI

Jia, X.‐J. , Wang, H.‐X. , Yan, Z.‐G. , Zhang, M.‐Z. , Wei, C.‐H. , Qin, X.‐C. , … Du, Y.‐L. (2016). Antennal transcriptome and differential expression of olfactory genes in the yellow peach moth, Conogethes punctiferalis (Lepidoptera: Crambidae). Scientific Reports, 6, 29067 10.1038/srep29067 PubMed DOI PMC

Jia, X. , Zhang, X. , Liu, H. , Wang, R. , & Zhang, T. (2018). Identification of chemosensory genes from the antennal transcriptome of Indian meal moth Plodia interpunctella . PLoS One, 13, e0189889 10.1371/journal.pone.0189889 PubMed DOI PMC

Jiang, X. J. , Guo, H. , Di, C. , Yu, S. , Zhu, L. , Huang, L. Q. , & Wang, C. Z. (2014). Sequence similarity and functional comparisons of pheromone receptor orthologs in two closely related Helicoverpa species. Insect Biochemistry and Molecular Biology, 48, 63–74. 10.1016/j.ibmb.2014.02.010 PubMed DOI

Jósvai, J. K. , Koczor, S. , & Tóth, M. (2016). Traps baited with pear ester and acetic acid attract both sexes of Hedya nubiferana (Lepidoptera: Tortricidae). Journal of Applied Entomology, 140, 81–90. 10.1111/jen.12216 DOI

Katoh, K. , Rozewicki, J. , & Yamada, K. D. (2019). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. 10.1093/bib/bbx108 PubMed DOI PMC

Khan, Z. R. , Midega, C. A. O. , Pittchar, J. O. , Murage, A. W. , Birkett, M. A. , Bruce, T. J. A. , & Pickett, J. A. (2014). Achieving food security for one million sub‐Saharan African poor through push‐pull innovation by 2020. Philosophical Transactions of the Royal Society B, 369, 20120284 10.1098/rstb.2012.0284 PubMed DOI PMC

Knight, A. L. , & Light, D. M. (2013). Adding microencapsulated pear ester to insecticides for control of Cydia pomonella (Lepidoptera: Tortricidae) in apple. Pest Management Science, 69, 66–74. 10.1002/ps.3363 PubMed DOI

Knight, A. , Light, D. , & Chebny, V. (2013). Monitoring codling moth (Lepidoptera: Tortricidae) in orchards treated with pear ester and sex pheromone combo dispensers. Journal of Applied Entomology, 137, 214–224. 10.1111/j.1439-0418.2012.01715.x DOI

Knight, A. L. , Mujica, V. , Herrera, S. L. , & Tasin, M. (2019). Addition of terpenoids to pear ester plus acetic acid increases catches of codling moth (Lepidoptera: Tortricidae). Journal of Applied Entomology, 143, 942–947. 10.1111/jen.12682 DOI

Knight, A. L. , Stelinski, L. L. , Hebert, V. , Gut, L. , Light, D. , & Brunner, J. (2012). Evaluation of novel semiochemical dispensers simultaneously releasing pear ester and sex pheromone for mating disruption of codling moth (Lepidoptera: Tortricidae). Journal of Applied Entomology, 136, 79–86. 10.1111/j.1439-0418.2011.01633.x DOI

Knudsen, G. K. , Bengtsson, M. , Kobro, S. , Jaastad, G. , Hofsvang, T. , & Witzgall, P. (2008). Discrepancy in laboratory and field attraction of apple fruit moth Argyresthia conjugella to host plant volatiles. Physiological Entomology, 33, 1–6. 10.1111/j.1365-3032.2007.00592.x DOI

Knudsen, G. K. , Norli, H. R. , & Tasin, M. (2017). The ratio between field attractive and background volatiles encodes host‐plant recognition in a specialist moth. Frontiers in Plant Science, 8, 2206 10.3389/fpls.2017.02206 PubMed DOI PMC

Knudsen, G. K. , & Tasin, M. (2015). Spotting the invaders: A monitoring system based on plant volatiles to forecast apple fruit moth attacks in apple orchards. Basic and Applied Ecology, 16, 354–364. 10.1016/j.baae.2015.03.006 DOI

Knudsen, J. T. , Tollsten, L. , & Bergström, L. G. (1993). Floral scents: A checklist of volatile compounds isolated by head‐space techniques. Phytochemistry, 33, 253–280. 10.1016/0031-9422(93)85502-I DOI

Koenig, C. , Hirsh, A. , Bucks, S. , Klinner, C. , Vogel, H. , Shukla, A. , … Grosse‐Wilde, E. (2015). A reference gene set for chemosensory receptor genes of Manduca sexta . Insect Biochemistry and Molecular Biology, 66, 51–63. 10.1016/j.ibmb.2015.09.007 PubMed DOI

Kovanci, O. B. (2015). Co‐application of microencapsulated pear ester and codlemone for mating disruption of Cydia pomonella . Journal of Pest Science, 88, 311–319. 10.1007/s10340-014-0619-x DOI

Krieger, J. , Gondesen, I. , Forstner, M. , Gohl, T. , Dewer, Y. , & Breer, H. (2009). HR11 and HR13 receptor‐expressing neurons are housed together in pheromone‐responsive sensilla trichodea of male Heliothis virescens . Chemical Senses, 34, 469–477. 10.1093/chemse/bjp010 PubMed DOI

Lebreton, S. , Borrero‐Echeverry, F. , Gonzalez, F. , Solum, M. , Wallin, E. , Hedenström, E. , … Witzgall, P. (2017). A Drosophila female pheromone elicits species‐specific long‐range attraction via an olfactory channel with dual specificity for sex and food. BMC Biology, 15, 88 10.1186/s12915-017-0427-x PubMed DOI PMC

Lemfack, M. C. , Gohlke, B. O. , Toguem, S. M. T. , Preissner, S. , Piechulla, B. , & Preissner, R. (2018). mVOC 2.0: A database of microbial volatiles. Nucleic Acids Research, 46, D1261–D1265. 10.1093/nar/gkx1016 PubMed DOI PMC

Li, G. , Du, J. , Li, Y. , & Wu, J. (2015). Identification of putative olfactory genes from the oriental fruit moth Grapholita molesta via an antennal transcriptome analysis. PLoS One, 10(11), e0142193 10.1371/journal.pone.0142193 PubMed DOI PMC

Light, D. M. (2016). Control and monitoring of codling moth (Lepidoptera: Tortricidae) in walnut orchards treated with novel high‐load, low‐density “meso” dispensers of sex pheromone and pear ester. Environmental Entomology, 45, 700–707. 10.1093/ee/nvw017 PubMed DOI

Light, D. M. , & Beck, J. J. (2012). Behavior of codling moth (Lepidoptera: Tortricidae) neonate larvae on surfaces treated with microencapsulated pear ester. Environmental Entomology, 41, 603–611. 10.1603/EN11273 PubMed DOI

Light, D. M. , & Knight, A. (2005). Specificity of codling moth (Lepidoptera: Tortricidae) for the host plant kairomone, ethyl (2E,4Z)‐2,4‐decadienoate: Field bioassays with pome fruit volatiles, analogue, and isomeric compounds. Journal of Agricultural and Food Chemistry, 53, 4046–4053. 10.1021/jf040431r PubMed DOI

Light, D. M. , & Knight, A. L. (2011). Microencapsulated pear ester enhances insecticide efficacy in walnuts for codling moth (Lepidoptera: Tortricidae) and navel orangeworm (Lepidoptera: Pyralidae). Journal of Economic Entomology, 104, 1309–1315. 10.1603/EC11058 PubMed DOI

Light, D. M. , Knight, A. L. , Henrick, C. A. , Rajapaska, D. , Lingren, B. , Dickens, J. C. , … Campbell, B. C. (2001). A pear‐derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.). Naturwissenschaften, 88, 333–338. (10.1007/s001140100243) PubMed

Liu, Z. , Smagghe, G. , Lei, Z. , & Wang, J. J. (2016). Identification of male‐and female‐specific olfaction genes in antennae of the Oriental fruit fly (Bactrocera dorsalis). PLoS One, 11, e0147783 (10.1371/journal.pone.0147783) PubMed PMC

Ljunggren, J. , Borrero‐Echeverry, F. , Chakraborty, A. , Lindblom, T. U. , Hedenström, E. , Karlsson, M. , … Bengtsson, M. (2019). Yeast volatomes differentially effect larval feeding in an insect herbivore. Appl Environm Microbiol, 85, e01761–e1819. 10.1128/AEM.01761-19 PubMed DOI PMC

Longing, S. D. , Peterson, E. M. , Jewett, C. T. , Rendon, B. M. , Discua, S. A. , Wooten, K. J. , … McIntyre, N. E. (2020). Exposure of foraging bees (Hymenoptera) to neonicotinoids in the U.S. southern high plains. Environmental Entomology. 10.1093/ee/nvaa003 PubMed DOI

Lu, P. F. , Wang, R. , Wang, C. Z. , Luo, Y. Q. , & Qiao, H. L. (2015). Sexual differences in electrophysiological and behavioral responses of Cydia molesta to peach and pear volatiles. Entomologia Experimentalis Et Applicata, 157, 279–290. 10.1111/eea.12362 DOI

McBride, C. S. , & Arguello, J. R. (2007). Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics, 177, 1395–1416. 10.1534/genetics.107.078683 PubMed DOI PMC

Menuz, K. , Larter, N. K. , Park, J. , & Carlson, J. R. (2014). An RNA‐seq screen of the Drosophila antenna identifies a transporter necessary for ammonia detection. PLoS Genetics, 10, e1004810 10.1371/journal.pgen.1004810 PubMed DOI PMC

Muench, D. , & Galizia, C. G. (2016). DoOR 2.0‐Comprehensive mapping of Drosophila melanogaster odorant responses. Scientific Reports, 6, 21841 10.1038/srep21841 PubMed DOI PMC

Najar‐Rodriguez, A. J. , Galizia, C. G. , Stierle, J. , & Dorn, S. (2010). Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant‐derived volatile mixtures. Journal of Experimental Biology, 213, 3388–3397. 10.1242/jeb.046284 PubMed DOI

Park, K. C. , Withers, T. M. , Suckling, D. M. , & Collaboration, B. B. B. (2015). Identification of olfactory receptor neurons in Uraba lugens (Lepidoptera: Nolidae) and its implications for host range. Journal of Insect Physiology, 78, 33–46. 10.1016/j.jinsphys.2015.04.010 PubMed DOI

Paterson, H. (1978). More evidence against speciation by reinforcement. South African Journal of Science, 74, 369–371.

Phelan, P. L. (1992). Evolution of sex pheromones and the role of assymetric tracking In Roitberg B. D., & Isman M. B. (Eds.), Insect chemical ecology: An evolutionary approach (pp. 265–314). New York, NY: Chapman and Hall.

Porcel, M. , Sjöberg, P. , Swiergiel, W. , Dinwiddie, R. , Rämert, B. , & Tasin, M. (2015). Mating disruption of Spilonota ocellana and other apple orchard tortricids using a multispecies reservoir dispenser. Pest Management Science, 71, 562–570. 10.1002/ps.3844 PubMed DOI

Ramdya, P. , & Benton, R. (2010). Evolving olfactory systems on the fly. Trends in Genetics, 26, 307–316. 10.1016/j.tig.2010.04.004 PubMed DOI

Rauscher, S. , Arn, H. , & Guerin, P. (1984). Effects of dodecyl acetate and Z‐10‐tridecenyl acetate on attraction of Eupoecilia ambiguella males to the main sex pheromone component, Z‐9‐Dodecenyl acetate. Journal of Chemical Ecology, 10, 253–264. 10.1007/BF00987853 PubMed DOI

Reddy, G. V. , & Guerrero, A. (2004). Interactions of insect pheromones and plant semiochemicals. Trends in Plant Science, 9, 253–261. 10.1016/j.tplants.2004.03.009 PubMed DOI

Reddy, G. V. , & Guerrero, A. (2010). New pheromones and insect control strategies. Vitamins and Hormones, 83, 493–519. 10.1016/S0083-6729(10)83020-1 PubMed DOI

Regier, J. C. , Brown, J. W. , Mitter, C. , Baixeras, J. , Cho, S. , Cummings, M. P. , & Zwick, A. (2012). A molecular phylogeny for the leafroller moths (Lepidoptera: Tortricidae) and its implications for classification and life history evolution. PLoS One, 7, e35574 10.1371/journal.pone.0035574 PubMed DOI PMC

Ridgway, R. L. , Silverstein, R. M. , & Inscoe, M. N. (1990). Behavior‐modifying chemicals for insect management: Applications of pheromones and other attractants. New York, NY: Marcel Dekker.

Robertson, H. M. (2019). Molecular evolution of the major arthropod chemoreceptor gene families. Annual Review of Entomology, 64, 227–242. 10.1146/annurev-ento-020117-043322 PubMed DOI

Rojas, V. , Jimenez, H. , Palma‐Millanao, R. , Gonzalez‐Gonzalez, A. , Machuca, J. , Godoy, R. , … Venthur, H. (2018). Analysis of the grapevine moth Lobesia botrana antennal transcriptome and expression of odorant‐binding and chemosensory proteins. Comparative Biochemistry and Physiology D, 27, 1–12. 10.1016/j.cbd.2018.04.003 PubMed DOI

Rosenthal, G. G. (2017). Mate choice: The evolution of sexual decision making from microbes to humans. Princeton, NJ: Princeton University Press.

Rouyar, A. , Deisig, N. , Dupuy, F. , Limousin, D. , Wycke, M. A. , Renou, M. , & Anton, S. (2015). Unexpected plant odor responses in a moth pheromone system. Frontiers in Physiology, 6, 148 10.3389/fphys.2015.00148 PubMed DOI PMC

Sánchez‐Gracia, A. , Vieira, F. , & Rozas, J. (2009). Molecular evolution of the major chemosensory gene families in insects. Heredity, 103, 208–216. 10.1038/hdy.2009.55 PubMed DOI

Schmidt, S. , Anfora, G. , Ioriatti, C. , Germinara, G. S. , Rotundo, G. , & De Cristofaro, A. (2007). Biological activity of ethyl (E, Z)‐2,4‐decadienoate on different tortricid species: Electrophysiological responses and field tests. Environmental Entomology, 36, 1025–1031. 10.1603/0046-225X(2007)36[1025:BAOEEO]2.0.CO;2 PubMed DOI

Schmidt, S. , Tomasi, C. , Pasqualini, E. , & Ioriatti, C. (2008). The biological efficacy of pear ester on the activity of granulosis virus for codling moth. Journal of Pest Science, 81, 29–34. 10.1007/s10340-007-0181-x DOI

Schorkopf, D. L. P. , Molnar, B. P. , Solum, M. , Larsson, M. C. , Millar, J. G. , Karpati, Z. , & Dekker, T. (2019). False positives from impurities result in incorrect functional characterization of receptors in chemosensory studies. Progress in Neurobiology, 181, 101661 10.1016/j.pneurobio.2019.101661 PubMed DOI

Seibold, S. , Gossner, M. M. , Simons, N. K. , Blüthgen, N. , Müller, J. , Ambarli, D. , … Weisser, W. W. (2019). Arthropod decline in grasslands and forests is associated with landscape‐level drivers. Nature, 574, 671–674. 10.1038/s41586-019-1684-3 PubMed DOI

Steinwender, B. , Thrimawithana, A. H. , Crowhurst, R. N. , & Newcomb, R. D. (2015). Pheromone receptor evolution in the cryptic leafroller species, Ctenopseustis obliquana and C. herana . Journal of Molecular Evolution, 80, 42–56. 10.1007/s00239-014-9650-z PubMed DOI

Stenberg, J. A. , Heil, M. , Åhman, I. , & Björkman, C. (2015). Optimizing crops for biocontrol of pests and disease. Trends in Plant Science, 20, 698–712. 10.1016/j.tplants.2015.08.007 PubMed DOI

Suckling, D. M. , Stringer, L. D. , Stephens, A. E. , Woods, B. , Williams, D. G. , Baker, G. , & El‐Sayed, A. M. (2014). From integrated pest management to integrated pest eradication: Technologies and future needs. Pest Management Science, 70, 179–189. 10.1002/ps.3670 PubMed DOI

Sutherland, O. R. W. , & Hutchins, R. F. N. (1972). α‐Farnesene, a natural attractant for codling moth larvae. Nature, 239, 170.

Tamiru, A. , Khan, Z. R. , & Bruce, T. J. (2015). New directions for improving crop resistance to insects by breeding for egg induced defence. Current Opinion in Insect Science, 9, 51–55. 10.1016/j.cois.2015.02.011 PubMed DOI

Tamura, K. , Stecher, G. , Peterson, D. , Filipski, A. , & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. 10.1093/molbev/mst197 PubMed DOI PMC

Tasin, M. , Bäckman, A.‐C. , Anfora, G. , Carlin, S. , Ioriatti, C. , & Witzgall, P. (2010). Attraction of female grapevine moth to common and specific olfactory cues from 2 host plants. Chemical Senses, 35, 57–64. 10.1093/chemse/bjp082 PubMed DOI

Tian, Z. , Sun, L. , Li, Y. , Quan, L. , Zhang, H. , Yan, W. , … Qiu, G. (2018). Antennal transcriptome analysis of the chemosensory gene families in Carposina sasakii (Lepidoptera: Carposinidae). BMC Genomics, 19, 544 10.1186/s12864-018-4900-x PubMed DOI PMC

Trona, F. , Anfora, G. , Balkenius, A. , Bengtsson, M. , Tasin, M. , Knight, A. , … Ignell, R. (2013). Neural coding merges sex and habitat chemosensory signals in an insect herbivore. Proceedings of the Royal Society B, 280, 20130267 10.1098/rspb.2013.0267 PubMed DOI PMC

Trona, F. , Anfora, G. , Bengtsson, M. , Witzgall, P. , & Ignell, R. (2010). Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella . Journal of Experimental Biology, 213, 4291–4303. 10.1242/jeb.047365 PubMed DOI

Varela, N. , Avilla, J. , Gemeno, C. , & Anton, S. (2011). Ordinary glomeruli in the antennal lobe of male and female tortricid moth Grapholita molesta (Busck)(Lepidoptera: Tortricidae) process sex pheromone and host‐plant volatiles. Journal of Experimental Biology, 214, 637–645. 10.1242/jeb.047316 PubMed DOI

Wagner, D. L. (2020). Insect declines in the Anthropocene. Annual Review of Entomology, 65, 457–480. 10.1146/annurev-ento-011019-025151 PubMed DOI

Walker, W. B. , Gonzalez, F. , Garczynski, S. F. , & Witzgall, P. (2016). The chemosensory receptors of codling moth Cydia pomonella ‐ expression in larvae and adults. Scientific Reports, 6, 23518 10.1038/srep23518 PubMed DOI PMC

Wan, F. , Yin, C. , Tang, R. , Chen, M. , Wu, Q. , Huang, C. , … Wang, G. (2019). A chromosome‐level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance. Nature Communications, 10, 1–14. 10.1038/s41467-019-12175-9 PubMed DOI PMC

Witzgall, P. , Bengtsson, M. , Buser, H. R. , Chambon, P. J. , Priesner, E. , Wildbolz, T. , & Arn, H. (1991). Sex pheromones of Spilonota ocellana and Spilonota laricana. Entomologia Experimentalis et Applicata, 60, 219–223. 10.1111/j.1570-7458.1991.tb01541.x DOI

Witzgall, P. , Bengtsson, M. , Rauscher, S. , Liblikas, I. , Bäckman, A.‐C. , Coracini, M. , … Löfqvist, J. (2001). Identification of further sex pheromone synergists in the codling moth, Cydia pomonella . Entomologia Experimentalis Et Applicata, 101, 131–141. 10.1046/j.1570-7458.2001.00898.x DOI

Witzgall, P. , Bengtsson, M. , Unelius, C. R. , & Löfqvist, J. (1993). Attraction of pea moth Cydia nigricana F. (Lepidoptera: Tortricidae) to female sex pheromone (E, E)‐8,10‐dodecadien‐1‐yl acetate, is inhibited by geometric isomers (E, Z), (Z, E) and (Z, Z). Journal of Chemical Ecology, 19, 1917–1928. 10.1007/BF00983796 PubMed DOI

Witzgall, P. , Chambon, J.‐P. , Bengtsson, M. , Unelius, C. R. , Appelgren, M. , Makranczy, G. , … Löfqvist, J. (1996). Sex pheromones and attractants in the Eucosmini and Grapholitini (Lepidoptera, Tortricidae). Chemoecology, 7, 13–23. 10.1007/BF01240633 DOI

Witzgall, P. , Kirsch, P. , & Cork, A. (2010). Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36, 80–100. 10.1007/s10886-009-9737-y PubMed DOI

Witzgall, P. , Stelinski, L. , Gut, L. , & Thomson, D. (2008). Codling moth management and chemical ecology. Annual Review of Entomology, 53, 503–522. 10.1146/annurev.ento.53.103106.093323 PubMed DOI

Witzgall, P. , Trematerra, P. , Liblikas, I. , Bengtsson, M. , & Unelius, C. R. (2010). Pheromone communication channels in tortricid moths: Lower specificity of alcohol vs. acetate geometric isomer blends. Bulletin of Entomological Research, 100, 225–230. 10.1017/S0007485309990186 PubMed DOI

Yamamuro, M. , Komuro, T. , Kamiya, H. , Kato, T. , Hasegawa, H. , & Kameda, Y. (2019). Neonicotinoids disrupt aquatic food webs and decrease fishery yields. Science, 366, 620–623. 10.1126/science.aax3442 PubMed DOI

Yang, S. , Cao, D. , Wang, G. , & Liu, Y. (2017). Identification of genes involved in chemoreception in Plutella xyllostella by antennal transcriptome analysis. Scientific Reports, 7, 1–16. 10.1038/s41598-017-11646-7 PubMed DOI PMC

Zeng, F.‐F. , Zhao, Z.‐F. , Yan, M.‐J. , Zhou, W. , Zhang, Z. , Zhang, A. , … Wang, M.‐Q. (2015). Identification and comparative expression profiles of chemoreception genes revealed from major chemoreception organs of the rice leaf folder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). PLoS One, 10, e0144267 10.1371/journal.pone.0144267 PubMed DOI PMC

Zhang, D. D. , & Löfstedt, C. (2015). Moth pheromone receptors: Gene sequences, function, and evolution. Frontiers in Ecology and Evolution, 3, 105 10.3389/fevo.2015.00105 DOI

Zhang, J. , Wang, B. , Dong, S. , Cao, D. , Dong, J. , Walker, W. B. , … Wang, G. (2015). Antennal transcriptome analysis and comparison of chemosensory gene families in two closely related noctuidae moths, Helicoverpa armigera and H. assulta . PLoS One, 10, e0117054 10.1371/journal.pone.0117054 PubMed DOI PMC

Zhang, S.‐F. , Liu, H.‐H. , Kong, X.‐B. , Wang, H.‐B. , Liu, F. , & Zhang, Z. (2017). Identification and expression profiling of chemosensory genes in Dendrolimus punctatus Walker. Frontiers in Physiology, 8, 471 10.3389/fphys.2017.00471 PubMed DOI PMC

Zhang, S. , Zhang, Z. , Wang, H. , & Kong, X. (2014). Antennal transcriptome analysis and comparison of olfactory genes in two sympatric defoliators, Dendrolimus houi and Dendrolimus kikuchii (Lepidoptera: Lasiocampidae). Insect Biochemistry and Molecular Biology, 52, 69–81. 10.1016/j.ibmb.2014.06.006 PubMed DOI

Zhang, Y.‐N. , Jin, J.‐Y. , Jin, R. , Xia, Y.‐H. , Zhou, J.‐J. , Deng, J.‐Y. , & Dong, S.‐L. (2013). Differential expression patterns in chemosensory and non‐chemosensory tissues of putative chemosensory genes identified by transcriptome analysis of insect pest the purple stem borer Sesamia inferens (Walker). PLoS One, 8, e69715 10.1371/journal.pone.0069715 PubMed DOI PMC