Abstract
Cuticular compounds (CCs) that cover the surface of insects primarily serve as protection against entomopathogens, harmful substances, and desiccation. However, CCs may also have secondary signaling functions. By studying the role of CCs in intraspecific interactions, we may advance our understanding of the evolution of pheromonal communication in insects. We previously found that the gregarious parasitoid, Cotesia glomerata (L.), uses heptanal as a repellent pheromone to help avoid mate competition among sibling males, whereas another cuticular aldehyde, nonanal, is part of the female-produced attractive sex pheromone. Here, we show that the same aldehydes have different pheromonal functions in a related solitary parasitoid, Cotesia marginiventris (Cresson). Heptanal enhances the attractiveness of the female’s sex pheromone, whereas nonanal does not affect a female’s attractiveness. Hence, these common aldehydes are differentially used by the two Cotesia species to mediate, synergistically, the attractiveness of the main constituents of their respective sex pheromones. The specificity of the complete sex pheromone blend is apparently regulated by two specific, less volatile compounds, which evoke strong electroantennographic (EAG) responses. This is the first demonstration that volatile CCs have evolved distinct pheromonal functions to aid divergent mating strategies in closely related species. We discuss the possibility that additional compounds are involved in attraction and that, like the aldehydes, they are likely oxidative products of unsaturated cuticular hydrocarbons.
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References
Bartelt RJ, Jones RL (1983) (Z)-10-nonadecenal: a pheromonally active air oxidation product of (Z,Z)-9,19 dienes in yellowheaded spruce sawfly. J Chem Ecol 9:1333–1341. https://doi.org/10.1007/bf00994802
Bartelt RJ, Cossé AA, Petroski RJ, Weaver DK (2002) Cuticular hydrocarbons and novel alkenediol diacetates from wheat stem sawfly (Cephus cinctus): natural oxidation to pheromone components. J Chem Ecol 28:385–405. https://doi.org/10.1023/A:1017994410538
Bates DM (2010) lme4: mixed-effects modeling with R. http://lme4.r-forge.r-project.org/book/. Accessed 25 September 2019
Blomquist GJ, Nelson DR, De Renobales M (1987) Chemistry, biochemistry, and physiology of insect cuticular lipids. Arch Insect Biochem 6:227–265. https://doi.org/10.1002/arch.940060404
Blows MW, Allan RA (1998) Levels of mate recognition within and between two Drosophila species and their hybrids. Am Nat 152:826–837. https://doi.org/10.1086/286211
Buellesbach J, Gadau J, Beukeboom LW, Echinger F, Raychoudhury R, Werren JH, Schmitt T (2013) Cuticular hydrocarbon divergence in the jewel wasp Nasonia: evolutionary shifts in chemical communication channels? J Evolution Biol 26:2467–2478. https://doi.org/10.1111/jeb.12242
Cuervo M, Rakosy D, Martel C, Schulz S, Ayasse M (2017) Sexual deception in the Eucera-pollinated Ophrys leochroma: a chemical intermediate between wasp-and Andrena-pollinated species. J Chem Ecol 43:469–479. https://doi.org/10.1007/s10886-017-0848-6
D’Alessandro M, Turlings TCJ (2005) In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30:739–753. https://doi.org/10.1093/chemse/bji066
Davison AC, Ricard I (2011) Comparison of models for olfactometer data. J Agr Biol Envir St 16:157–169. https://doi.org/10.1007/s13253-010-0042-6
Desurmont GA, Xu H, Turlings TC (2016) Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa. Plant Cell Environ 39:1920–1927. https://doi.org/10.1111/pce.12752
Fan YL, Rafaeli A, Gileadi C, Kubli E, Applebaum SW (1999) Drosophila melanogaster sex peptide stimulates juvenile hormone synthesis and depresses sex pheromone production in Helicoverpa armigera. J Insect Physiol 45:127–133. https://doi.org/10.1016/s0022-1910(98)00106-1
Gershman SN, Rundle HD (2016) Level up: the expression of male sexually selected cuticular hydrocarbons is mediated by sexual experience. Anim Behav 112:169–177. https://doi.org/10.1016/j.anbehav.2015.11.025
Gershman SN, Toumishey E, Rundle HD (2014) Time flies: time of day and social environment affect cuticular hydrocarbon sexual displays in Drosophila serrata. P Roy Soc B-Biol Sci 281:20140821. https://doi.org/10.1098/rspb.2014.0821
Gu H, Dorn S (2003) Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata. Anim Behav 66:259–264. https://doi.org/10.1006/anbe.2003.2185
Hatano E, Wada-Katsumata A, Schal C (2019) Environmental decomposition of cuticular hydrocarbons generates a volatile pheromone that guides insect social behavior. bioRxiv:773937. https://doi.org/10.1101/773937
Higgie M, Chenoweth S, Blows MW (2000) Natural selection and the reinforcement of mate recognition. Science 290:519–521. https://doi.org/10.1126/science.290.5491.519
Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: chemistry. University of Nebraska Press, Biochemistry and Biology, pp 179–226
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. https://doi.org/10.1146/annurev.ento.50.071803.130359
Ingleby FC (2015) Insect cuticular hydrocarbons as dynamic traits in sexual communication. Insects 6:732–742. https://doi.org/10.3390/insects6030732
Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289. https://doi.org/10.1111/j.1469-185X.2007.00009.x
Kather R, Martin SJ (2015) Evolution of cuticular hydrocarbons in the hymenoptera: a meta-analysis. J Chem Ecol 41:871–883. https://doi.org/10.1007/s10886-015-0631-5
Kühbandner S, Sperling S, Mori K, Ruther J (2012) Deciphering the signature of cuticular lipids with contact sex pheromone function in a parasitic wasp. J Exp Biol 215:2471–2478. https://doi.org/10.1242/jeb.071217
Lassance J et al (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486–489. https://doi.org/10.1038/nature09058
Lebreton S et al (2017) A Drosophila female pheromone elicits species-specific long-range attraction via an olfactory channel with dual specificity for sex and food. BMC Biol 15:88. https://doi.org/10.1186/s12915-017-0427-x
Mant J, Brändli C, Vereecken NJ, Schulz CM, Francke W, Schiestl FP (2005) Cuticular hydrocarbons as sex pheromone of the bee Colletes cunicularius and the key to its mimicry by the sexually deceptive orchid, Ophrys exaltata. J Chem Ecol 31:1765–1787. https://doi.org/10.1007/s10886-005-5926-5
Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161. https://doi.org/10.1007/s10886-009-9695-4
Michel-Salzat A, Whitfield JB (2004) Preliminary evolutionary relationships within the parasitoid wasp genus Cotesia (Hymenoptera: Braconidae: Microgastrinae): combined analysis of four genes. Syst Entomol 29:371–382. https://doi.org/10.1111/j.0307-6970.2004.00246.x
Niehuis O, Buellesbach J, Judson AK, Schmitt T, Gadau J (2011) Genetics of cuticular hydrocarbon differences between males of the parasitoid wasps Nasonia giraulti and Nasonia vitripennis. Heredity 107:61–70. https://doi.org/10.1038/hdy.2010.157
Niehuis O et al (2013) Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494:345–348. https://doi.org/10.1038/nature11838
Otte T, Hilker M, Geiselhardt S (2018) Phenotypic plasticity of cuticular hydrocarbon profiles in insects. J Chem Ecol 44:235–247. https://doi.org/10.1007/s10886-018-0934-4
Peso M, Elgar MA, Barron AB (2015) Pheromonal control: reconciling physiological mechanism with signalling theory. Biol Rev 90:542–559. https://doi.org/10.1111/brv.12123
Petfield D, Chenoweth SF, Rundle HD, Blows MW (2005) Genetic variance in female condition predicts indirect genetic variance in male sexual display traits. P Natl Acad Sci USA 102:6045–6050. https://doi.org/10.1073/pnas.0409378102
Rafaeli A, Gileadi C (1996) Down regulation of pheromone biosynthesis: cellular mechanisms of pheromonostatic responses. Insect Biochem Molec 26:797–807. https://doi.org/10.1016/S0965-1748(96)00029-X
Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn CE (2002) Evolution of moth sex pheromones via ancestral genes. P Natl Acad Sci USA 99:13621–13626. https://doi.org/10.1073/pnas.152445399
Ruther J (2013) Novel insights into pheromone-mediated communication in parasitic hymenopterans. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, pp 112–144
Schiestl FP, Ayasse M (2000) Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior. Behav Ecol Sociobiol 48:303–307. https://doi.org/10.1007/s002650000241
Scott D (1986) Sexual mimicry regulates the attractiveness of mated Drosophila melanogaster females. P Natl Acad Sci USA 83:8429–8433. https://doi.org/10.1073/pnas.83.21.8429
Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38:394–405. https://doi.org/10.1093/icb/38.2.394
Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409. https://doi.org/10.1007/s002650000311
Steiger S, Schmitt T, Schaefer HM (2010) The origin and dynamic evolution of chemical information transfer. P Roy Soc B-Biol Sci 278:970–979. https://doi.org/10.1098/rspb.2010.2285
Steinberg S, Dicke M, Vet LEM (1993) Relative importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoid Cotesia glomerata. J Chem Ecol 19:47–59. https://doi.org/10.1007/bf00987470
Steiner S, Mumm R, Ruther J (2007) Courtship pheromones in parasitic wasps: comparison of bioactive and inactive hydrocarbon profiles by multivariate statistical methods. J Chem Ecol 33:825–838. https://doi.org/10.1007/s10886-007-9265-6
Steinmetz I, Schmolz E, Ruther J (2003) Cuticular lipids as trail pheromone in a social wasp. P Roy Soc B-Biol Sci 270:385–391. https://doi.org/10.1098/rspb.2002.2256
Stökl J, Twele R, Erdmann DH, Francke W, Ayasse M (2007) Comparison of the flower scent of the sexually deceptive orchid Ophrys iricolor and the female sex pheromone of its pollinator Andrena morio. Chemoecology 17:231–233. https://doi.org/10.1007/s00049-007-0383-y
Swedenborg PD, Jones RL (1992) (Z)-4-Tridecenal, a pheromonally active air oxidation product from a series of (Z, Z)-9, 13 dienes in Macrocentrus grandii Goidanich (Hymenoptera: Braconidae). J Chem Ecol 18:1913–1931. https://doi.org/10.1007/BF00981916
Symonds MRE, Elgar MA (2004) The mode of pheromone evolution: evidence from bark beetles. P Roy Soc B-Biol Sci 271:839–846. https://doi.org/10.1098/rspb.2003.2647
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
Tagawa J (1977) Localization and histology of the female sex pheromone-producing gland in the parasitic wasp, Apanteles glomeratus. J Insect Physiol 23:49–56. https://doi.org/10.1016/0022-1910(77)90108-1
Tagawa J (2000) Sex allocation and clutch size in the gregarious larval endoparasitoid wasp, Cotesia glomerata. Entomol Exp Appl 97:193–202. https://doi.org/10.1046/j.1570-7458.2000.00730.x
Tamò C, Roelfstra L, Guillaume S, Turlings TCJ (2006) Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy. J Anim Ecol 75:1091–1099. https://doi.org/10.1111/j.1365-2656.2006.01128.x
Thomas ML, Simmons LW (2011) Short-term phenotypic plasticity in long-chain cuticular hydrocarbons. P Roy Soc B-Biol Sci 278:3123–3128. https://doi.org/10.1098/rspb.2011.0159
Turlings T, Tumlinson J, Lewis W (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253. https://doi.org/10.1126/science.250.4985.1251
Van Oystaeyen A et al (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290. https://doi.org/10.1126/science.1244899
Van Wilgenburg E, Symonds MRE, Elgar MA (2011) Evolution of cuticular hydrocarbon diversity in ants. J Evolution Biol 24:1188–1198. https://doi.org/10.1111/j.1420-9101.2011.02248.x
van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagneres AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology, vol 11. Cambridge University Press, Cambridge, pp 222–243
Weiss I, Rössler T, Hofferberth J, Brummer M, Ruther J, Stökl J (2013) A nonspecific defensive compound evolves into a competition avoidance cue and a female sex pheromone. Nat Commun 4. https://doi.org/10.1038/ncomms3767
Wickham JD, Xu Z, Teale SA (2012) Evidence for a female-produced, long range pheromone of Anoplophora glabripennis (Coleoptera: Cerambycidae). Insect Sci 19:355–371. https://doi.org/10.1111/j.1744-7917.2012.01504.x
Wurdack M et al (2015) Striking cuticular hydrocarbon dimorphism in the mason wasp Odynerus spinipes and its possible evolutionary cause (Hymenoptera: Chrysididae, Vespidae). P Roy Soc B-Biol Sci 282:20151777. https://doi.org/10.1098/rspb.2015.1777
Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, Cambridge
Xu H, Turlings TCJ (2018) Plant volatiles as mate-finding cues for insects. Trends Plant Sci 23:100–111. https://doi.org/10.1016/j.tplants.2017.11.004
Xu H, Veyrat N, Degen T, Turlings TCJ (2014) Exceptional use of sex pheromones by parasitoids of the genus Cotesia: males are strongly attracted to virgin females, but are no longer attracted to or even repelled by mated females. Insects 5:499–512. https://doi.org/10.3390/insects5030499
Xu H, Desurmont G, Degen T, Zhou G, Laplanche D, Henryk L, Turlings TC (2017) Combined use of herbivore-induced plant volatiles and sex pheromones for mate location in braconid parasitoids. Plant Cell Environ 40:330–339. https://doi.org/10.1111/pce.12818
Xu H et al (2019) The combined use of an attractive and a repellent sex pheromonal component by a gregarious parasitoid. J Chem Ecol 45:559–569. https://doi.org/10.1007/s10886-019-01066-4
Yang K, Huang L-Q, Ning C, Wang C-Z (2017) Two single-point mutations shift the ligand selectivity of a pheromone receptor between two closely related moth species. Elife 6:e29100. https://doi.org/10.7554/eLife.29100.001
Acknowledgements
We would like to thank Dr. Gaylord Desurmont from the European Biological Control Laboratory, USDA, and Dr. Huijuan Guo from Institute of Zoology, Chinese Academy of Science for useful suggestions for the experimental designs. We also thank Dr. Gregory Röder from the University of Neuchâtel for his help with chemical analyses. The research was funded by the Fundamental Research Funds for the Central Universities (KYZ201920 and JCQY201904), as well as by a Eurocore project (EuroVol) from the European Science Foundation, funded by the Swiss National Science Foundation.
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H.X., G.Z., and T.T. designed experiments. H.X. and G.Z. preformed bioassays, and I.S., S.D., G.Z., H.X. and L.C. performed the electrophysiological analyses. H.X., G.Z. and L.C. did fractionation and chemical analyses. H.X. analyzed data and made the figures. H.X., T.D. and T.T. wrote the manuscript. All authors commented on the manuscript.
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Xu, H., Zhou, G., Dötterl, S. et al. Distinct Roles of Cuticular Aldehydes as Pheromonal Cues in Two Cotesia Parasitoids. J Chem Ecol 46, 128–137 (2020). https://doi.org/10.1007/s10886-019-01142-9
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DOI: https://doi.org/10.1007/s10886-019-01142-9