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A pheromone from cuticular hydrocarbons regulates mating behavior in the hoverfly Eupeodes corollae
Wenbiao Liu, Chenxi Cai, Jinan Wu, Bing Wang

State Key Laboratory for Biology of Plant Diseases and Insect PestsInstitute of Plant ProtectionChinese Academy of Agricultural SciencesBeijing 100193, China

 Highlights 

Eupeodes corollae mating peaked at 5 days post-emergence, with the highest copulation/success rates, shortest male latency, and stable duration.

l Two cuticular pheromones, (Z)-9-tricosene and n-tricosane, evoked strong electrophysiological responses in both sexes of E. corollae.

l (Z)-9-tricosene acts as a dual attractant for both sexes of E. corollae and stimulates male courtship behavior.

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摘要  

交配行为作为昆虫繁衍的重要环节,有助于后代种群的延续。表皮碳氢化合物(Cuticular Hydrocarbons, CHCs是调控昆虫交配行为的一类重要化学信号分子。然而,目前对天敌昆虫大灰优蚜蝇(Eupeodes corollae)的交配行为及其CHCs的化学通讯机制仍缺乏系统研究。本研究通过行为验系统解析大灰优蚜蝇的交配动态,利用气相色谱-质谱联用技术(GC-MS鉴定大灰优蚜蝇雌虫CHCs组成,并采用气相色谱-触角电位联用技术(GC-EAD)和触角电位技术(EAG筛选触角活性组分进一步通过行为试验测定活性组分对其行为选择及交配的调控作用。结果表明,大灰优蚜蝇交配过程划分为五个行为阶段:定向、近、振翅、爬背和求偶。其中,5日龄个体展现出最高的求偶率和交配成功率,同时雄虫求偶前所用搜寻时间最短,求偶持续时间稳定。表皮化合物分析显示,雌雄个体CHCs呈现单态性化学特征,其中顺-9-二十三烯和正二十三烷均能显著引起雌、雄虫触角电生理反应。行为试验表明,顺-9-二十三烯对大灰优蚜蝇雌、雄个体均有显著吸引作用,并能有效调控雄虫求偶行为。以上研究不仅为深入解析食蚜蝇化学通讯机制提供了新视角,更为开发基于信息素的行为调控技术提供了科学依据,对实现害虫防控具有重要应用价值



Abstract  

Mating behavior is crucial for most insects, as it is closely tied to reproduction and population growth and relies heavily on chemical communication via cuticular hydrocarbons (CHCs) between individuals. However, little is known about the mating behavior of Eupeodes corollae, a natural enemy insect, and how CHCs help it communicate. In this study, we performed a behavioral assay of the mating process of hoverfly E. corollae. The cuticular hydrocarbons of both male and female hoverflies were identified by gas chromatography-mass spectrometry (GC-MS). The electrophysiological activities of these compounds on the antennae of hoverflies were further determined by gas chromatography coupled with electroantennogram detection (GC-EAD) and electroantennogram (EAG). The effects of these compounds on the behavioral selection and mating of hoverflies were also determined. The results showed that the mating process of hoverflies was divided into five stages: orientation, approaching, wing fanning, mounting, and copulation. Fifth-aged individuals exhibited the highest copulation and mating success rates, the shortest male latency, and stable mating duration. The results of the determination of cuticular compounds showed that the CHCs of male and female hoverflies exhibited sexually monomorphic chemical profiles, and two compounds (Z)-9-tricosene and n-tricosane could cause significant electrophysiological responses in both male and female hoverflies. Behavioral bioassay results showed that (Z)-9-tricosene can significantly induce the attraction response of male and female E. corollae and can effectively regulate the courtship behavior of male E. corollae. This finding provides a new perspective for a deeper understanding of hoverflies’ chemical communication mechanism and a valuable scientific basis and potential application prospect for developing a pheromone-based behavior strategy to control pests.

Keywords:  pheromone       cuticular hydrocarbons              mating behavior              Eupeodes corollae              (Z)-9-tricosene  
Online: 11 April 2025  
Fund: 

This study was funded by the Natural Science Foundation of National Natural Science Foundation of China (32272621), the Key Project of Inter-Government International Science & Technology Innovation Cooperation (2019YFE0105800), Major special projects for green pest control (110202201017(LS-01)), and the Agricultural Science and Technology Innovation Program. 

About author:  Wenbiao Liu, E-mail: 82101221213@caas.cn; #Correspondence Bing Wang, E-mail: wangbing02@caas.cn

Cite this article: 

Wenbiao Liu, Chenxi Cai, Jinan Wu, Bing Wang. 2025. A pheromone from cuticular hydrocarbons regulates mating behavior in the hoverfly Eupeodes corollae. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.04.013

Abdel-Azim M M, Aldosari S A, Shukla P. 2019. Factors influencing mating behavior and success in the red palm weevil, Rhynchophorus ferrugineus Olivier (Coleoptera: Dryophthoridae). Neotropical Entomology, 48, 25-37.

Adams K, Roux O. 2024. No sexual pheromones in Anopheres mosquitoes? Current Opinion in Insect Science, 64, 101227.

Adams K L, Sawadogo S P, Nignan C, Niang A, Paton D G, Robert Shaw W, South A, Wang J, Itoe M A, Werling K, Dabiré R K, Diabaté A, Catteruccia F. 2021. Cuticular hydrocarbons are associated with mating success and insecticide resistance in malaria vectors. Communications Biology, 4, 911.

Agrawal S, Safarik S, Dickinson M. 2014. The relative roles of vision and chemosensation in mate recognition of Drosophila melanogaster. The Journal of Experimental Biology, 217, 2796-2805.

Andres-Bragado L, Sprecher S G. 2019. Mechanisms of vision in the fruit fly. Current Opinion in Insect Science, 36, 25-32.

Anholt R R H, O’Grady P, Wolfner M F, Harbison S T. 2020. Evolution of reproductive behavior. Genetics, 214, 49-73.

Antony C, Davis T L, Carlson D A, Pechine J M, Jallon J M. 1985. Compared behavioral responses of male Drosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs. Journal of Chemical Ecology, 11, 1617–1629.

Antony C, Jallon J M. 1982. The chemical basis for sex recognition in Drosophila melanogaster. Journal of Insect Physiology, 28, 873–880.

Baker C A, Clemens J, Murthy M. 2019. Acoustic pattern recognition and courtship songs: insights from insects. Annual Review of Neuroscience, 42, 129-147.

Bartelt R J, Schaner A M, Jackson L L. 1985. cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. Journal of Chemical Ecology, 11, 1747–1756. 

Benelli G, Kavallieratos N G, Donati E, Giunti G, Stefanini C, Canale A. 2016. Singing on the wings! Male wing fanning performances affect female willingness to copulate in the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae). Insect Science, 23, 603-611.

Benelli G, Ricciardi R, Romano D, Cosci F, Stefanini C, Lucchi A. 2020. Wing-fanning frequency as a releaser boosting male mating success-high-speed video analysis of courtship behavior in Campoplex capitator, a parasitoid of Lobesia botrana. Insect Science, 27, 1298-1310.

Billeter J C, Wolfner M F. 2018. Chemical cues that guide female reproduction in Drosophila melanogaster. Journal of Chemical Ecology, 44, 750-769.

Blomquist G J, Ginzel M D. 2021. Chemical ecology, biochemistry, and molecular biology of insect hydrocarbons. Annual Review of Entomology66, 45-60.

Butterworth F M. 1969. Lipids of Drosophila: a newly detected lipid in the male. Science, 163, 1356-1357.

Butterworth N J, Wallman J F, Drijfhout F P, Johnston N P, Keller P A, Byrne P G. 2020. The evolution of sexually dimorphic cuticular hydrocarbons in blowflies (Diptera: Calliphoridae). Journal of Evolution Biology, 33, 1468-1486.

Carlson D A, Mayer M S, Silhacek D L, James J D, Beroza M, Bierl B A. 1971. Sex attractant pheromone of the house fly: isolation, identification and synthesis. Science, 174, 76-78.

Carpita A, Canale A, Raffaelli A, Saba A, Benelli G, Raspi A. 2012. (Z)-9-tricosene identified in rectal gland extracts of Bactrocera oleae males: first evidence of a male-produced female attractant in olive fruit fly. Naturwissenschaften, 99, 77-81.

Chen Y, Zhang Y, Ai S, Xing S, Zhong G, Yi X. 2023. Female semiochemicals stimulate male courtship but dampen female sexual receptivity. Proceedings of the National Academy of Sciences of the United States of America, 120, e2311166120.

Chung H, Carroll S B. 2015. Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. BioEssays, 37, 822-830.

De Beer C J, Venter G J, Vreysen M J. 2015. Determination of the optimal mating age of colonised Glossina brevipalpis and Glossina austeni using walk-in field cages in South Africa. Parasites & Vectors, 8, 467.

Díaz V, Giudice A, Palladini A, Moyano A, Castillo G, Pérez- Staples D, Abraham S. 2024. Male and female age affects the reproductive potential of two tephritid flies. Ethology, 130, e13506.

Dunn L, Lequerica M, Reid C R, Latty T. 2020. Dual ecosystem services of syrphid flies (Diptera: Syrphidae): pollinators and biological control agents. Pest Management Science, 76, 1973–1979.

Dweck H K, Ebrahim S A, Thoma M, Mohamed A A, Keesey I W, Trona F, Lavista-Llanos S, Svatoš A, Sachse S, Knaden M, Hansson B S. 2015. Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 112, E2829-E2835.

Ebrahim S A M, Dweck H K M, Weiss B L, Carlson J R. 2023. A volatile sex attractant of tsetse flies. Science, 379, eade1877.

Ehlers S, Schulz S. 2023. The scent chemistry of butterflies. Natural Product Reports, 40, 794-818.

Faal H, Silk P J, Mayo P D, Teale S A. 2021. Courtship behavior and identification of a sex pheromone in Ibalia leucospoides (Hymenoptera: Ibaliidae), a larval parasitoid of Sirex noctilio (Hymenoptera: Siricidae). Peer J, 9, e12266.

Favoreto A L, Domingues M M, Serrão J E, Ribeiro M F, Silva C A D, Zanuncio J C, Wilcken C F. 2021. Courtship, mating behavior, and ovary histology of the nymph parasitoid Psyllaephagus bliteus (Hymenoptera: Encyrtidae). Journal of Insect Science, 21, 16.

Ferveur J F. 1991. Genetic control of pheromones in Drosophila simulans. I. Ngbo, a locus on the second chromosome. Genetics, 128, 293-301.

Ferveur J F. 1997. The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. BioEssays, 19, 353-358.

Funaro C F, Böröczky K, Vargo E L, Schal C. 2018. Identification of a queen and king recognition pheromone in the subterranean termite Reticulitermes flavipes. Proceedings of the National Academy of Sciences of the United States of America, 115, 3888-3893

Groot T, Dekker T, Heckel D G. 2016. The genetic basis of pheromone evolution in moths. Annual Review of Entomology, 61, 99-117.

Guo H, Mo B T, Li G C, Li Z L, Huang L Q, Sun Y L, Dong J F, Smith D P, Wang C Z. 2022. Sex pheromone communication in an insect parasitoid, Campoletis chlorideae Uchida. Proceedings of the National Academy of Sciences of the United States of America, 119, e2215442119.

Li H, Wyckhuys K A G, Wu K. 2023. Hoverflies provide pollination and biological pest control in greenhouse-grown horticultural crops. Frontiers in Plant Science, 14, 111838.

Li X L, Li D D, Cai X Y, Cheng D F, Lu Y Y. 2024. Reproductive behavior of fruit flies: courtship, mating, and oviposition. Pest Management Science, 80, 935-952.

Lin C C, Prokop-Prigge K A, Preti G, Potter C J. 2015. Food odors trigger Drosophila males to deposit a pheromone that guides aggregation and female oviposition decisions. Elife, 4, e08688.

Liu W B, Li H M, Wang G R, Cao H Q, Wang B. 2023. Conserved odorant receptor, EcorOR4, mediates attraction of mated female Eupeodes corollae to 1-octen-3-ol. Journal of Agricultural and Food Chemistry, 71, 1837-1844.

Menzel F, Blaimer B B, Schmitt T. 2017. How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait. Proceeding Biological Science, 284, 20161727.

Menzel F, Morsbach S, Martens J H, Räder P, Hadjaje S, Poizat M, Abou B. 2019. Communication versus waterproofing: the physics of insect cuticular hydrocarbons. The Journal of Experimental Biology, 222, jeb210807.

Moerkens R, Boonen S, Wäckers F L, Pekas A. 2021. Aphidophagous hoverflies reduce foxglove aphid infestations and improve seed set and fruit yield in sweet pepper. Pest Management Science, 77, 2690-2696.

Müller M J, Mendonça M P, Oliveira I R, de Oliveira L P, Valente V L, Valiati V H. 2012. Courtship behavior of Zaprionus indianus (Gupta) (Diptera: Drosophilidae) from populations colonizing South America, Neotropical Entomology, 41, 112-120.

Nojima T, Rings A, Goodwin S F. 2018. Drosophila courtship: Love is not blind. Current Biology, 28, R840-R842.

Pérez-Staples D, Abraham S. 2023. Postcopulatory behavior of Tephritid flies. Annual Review of Entomology, 48, 89-108.

Prathibha M, Krishna M S. 2010. Greater mating success of middle-aged females in D. ananassae. Zoological Studies, 49, 805-814.

Revadi S, Lebreton S, Witzgall P, Anfora G, Dekker T, Becher P G. 2015. Sexual behavior of Drosophila suzukii. Insects, 6, 183-196.

Rizvi S A H, George J, Reddy G V P, Zeng X N, Guerrero A. 2021. Latest developments in insect sex pheromone research and its application in agricultural pest management. Insects, 12, 484.

Smith A A, Liebig J. 2017. The evolution of cuticular fertility signals in eusocial insect. Current Opinion in Insect Science, 22, 79-84.

Snellings Y, Herrera B, Wildemann B, Beelen M, Zwarts L, Wenseleers T, Callaerts P. 2018. The role of cuticular hydrocarbons in mate recognition in Drosophila suzukii. Scientific Reports, 8, 4996.

Sokolowski M B. 2001. Drosophila: genetics meets behaviour. Nature Reviews Genetics, 2, 879-890.

Somashekar K, Krishna M S, Hegde S N, Jayaramu S C. 2011. Effects of age on female reproductive success in Drosophila bipectinate. Journal of Insect Science, 1, 132.

Tao Y X, Shan S, Dewer Y, Wang S N, Khashaveh A, Li R J, Zhang Y J. 2023. n-octyl acrylate is a candidate sex pheromone component involved in courtship in parasitoid wasp Microplitis mediator. Insect Science, 31, 1200-1210.

Triana M F, Melo N. 2024. Dynamics of Aedes aegypti mating behaviour. Current Opinion in Insect Science, 65, 101237.

Wang G, Vega-Rodríguez J, Diabate A, Liu J, Cui C, Nignan C, Dong L, Li F, Ouedrago C O, Bandaogo A M, Sawadogo P S, Maiga H, Alves E Silva T L, Pascini T V, Wang S, Jacobs-Lorena M. 2021. Clock genes and environmental cues coordinate Anopheles pheromone synthesis, swarming, and mating. Science, 371, 411-415.

Wicker-Thomas C. 2007. Pheromonal communication involved in courtship behavior in Diptera. Journal of Insect Physiology, 53, 1089-1100.

Wurrf J, Pokomy T, Wittbrodt J, Millar J G, Ruther J. 2020. Cuticular hydrocarbons as contact sex pheromone in the parasitoid wasp Urolepis rufipesFrontiers in Ecology and Evolution, 8, 180.

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