Abstract
Phytophagous insects locate suitable hosts through volatile compounds. Polyphagous species face a particular challenge because their hosts emit diverse chemical profiles, yet their olfactory strategies remain unclear. A long-standing assumption suggests that these insects respond primarily to compounds shared across hosts. Here we show that olfactory responses of various polyphagous fruit fly species (Tephritidae) are instead tuned to species-specific fruit compounds from 28 host fruits. This tuning translates into a behavioural preference for species-specific over shared fruit compounds, but only at low doses. Previously, response probability in the same species had been reported to be tuned to shared fruit compounds. To reconcile these observations, we propose a working hypothesis, supported by a computational model: an inverse relationship between olfactory response amplitude and probability may have evolved under the ecological need to detect and discriminate hosts. Together, these results highlight how polyphagous Tephritidae balance detection and discrimination through finely tuned olfactory mechanisms. This insight not only advances our understanding of host selection in polyphagous insects but also has potential applications for ecological management and pest control strategies.
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Data availability
Data have been deposited in a long term repository service: CIRAD Dataverse, V1 (https://doi.org/10.18167/DVN1/T3XUXW)64.
Code availability
The code used for modelling has been deposited in a long term repository service: CIRAD Dataverse, V1 (https://doi.org/10.18167/DVN1/T3XUXW, CIRAD Dataverse, V1)64.
References
Schoonhoven, L. M., van Loon, J. J. A. & Dicke, M. Insect-Plant Biology 2nd edn (Oxford University Press, 2005).
Cardé, R. T. & Willis, M. A. Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 34, 854–866 (2008).
Bruce, T. J. A., Wadhams, L. J. & Woodcock, C. M. Insect host location: a volatile situation. Trends Plant Sci. 10, 269–274 (2005).
Bruce, T. J. A. & Pickett, J. A. Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry 72, 1605–1611 (2011).
Siderhurst, M. S. & Jang, E. B. Cucumber volatile blend attractive to female melon fly, Bactrocera cucurbitae (Coquillett). J. Chem. Ecol. 36, 699–708 (2010).
Cunningham, J. P. Can mechanism help explain insect host choice? J. Evol. Biol. 25, 244–251 (2012).
Pan, H. et al. Volatile fragrances associated with flowers mediate host plant alternation of a polyphagous mirid bug. Sci. Rep. 5, 1–11 (2015).
Biasazin, T. D., Larsson Herrera, S., Kimbokota, F. & Dekker, T. Translating olfactomes into attractants: shared volatiles provide attractive bridges for polyphagy in fruit flies. Ecol. Lett. 22, 108–118 (2019).
Cunningham, J. P., Carlsson, M. A., Villa, T. F., Dekker, T. & Clarke, A. R. Do fruit ripening volatiles enable resource specialism in polyphagous fruit flies. J. Chem. Ecol. 42, 931–940 (2016).
Gripenberg, S., Mayhew, P. J., Parnell, M. & Roslin, T. A meta-analysis of preference-performance relationships in phytophagous insects. Ecol. Lett. 13, 383–393 (2010).
Lauciello, N., Mille, C. G., Hafsi, A., Jacob, V. & Duyck, P. Comparative adult preference–larval performance relationship between a specialist and a generalist tephritid: implication for predicting field host-range. Ecol Evol 14, e70170 (2024).
Charlery De La Masselière, M., Facon, B., Hafsi, A. & Duyck, P. F. Diet breadth modulates preference-performance relationships in a phytophagous insect community. Sci. Rep. 7, 16934 (2017).
Cooley, S. S., Prokopy, R. J., McDonald, P. T. & Wong, T. T. Y. Learning in oviposition site selection by Ceratitis capitata flies. Entomol. Exp. Appl. 40, 47–51 (1986).
Cunningham, J. P., West, S. A. & Zalucki, M. P. Host selection in phytophagous insects: a new explanation for learning in adults. Oikos 95, 537–543 (2001).
Cunningham, J. P., Jallow, M. F. A., Wright, D. J. & Zalucki, M. P. Learning in host selection in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Anim. Behav. 55, 227–234 (1998).
Starkie, M. L. et al. A comprehensive phylogeny helps clarify the evolutionary history of host breadth and lure response in the Australian Dacini fruit flies (Diptera: Tephritidae). Mol. Phylogenet Evol. 172, 107481 (2022).
Clarke, A. R. Why so many polyphagous fruit flies (Diptera: Tephritidae)? A further contribution to the ‘generalism’ debate. Biol. J. Linn. Soc. 120, 245–257 (2016).
He, J., Chen, K., Jiang, F. & Pan, X. Host shifts in economically significant fruit flies (Diptera: Tephritidae) with high degree of polyphagy. Ecol. Evol. 11, 13692–13701 (2021).
Moquet, L., Payet, J., Glenac, S. & Delatte, H. Niche shift of tephritid species after the oriental fruit fly (Bactrocera dorsalis) invasion in La Réunion. Divers. Distrib. 27, 109–129 (2021).
Hassani, I. M. et al. Invasion by Bactrocera dorsalis and niche partitioning among tephritid species in Comoros. Bull. Entomol. Res. 106, 749–758 (2016).
Dominiak, B. C. & Hoskins, J. L. Managing oriental fruit fly, Bactrocera dorsalis (Hendel): prioritising host plants using the host reproduction number. Int. J. Trop. Insect Sci. 45, 1249–1275 (2025).
Manoukis, N. C., Cha, D. H., Collignon, R. M. & Shelly, T. E. Terminalia larval host fruit reduces the response of Bactrocera dorsalis (Diptera: Tephritidae) adults to the male lure methyl eugenol. J. Econ. Entomol. 111, 1644–1649 (2018).
Segura, D., Vera, M. T. & Cladera, J. L. Host utilization by the mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). In Proc. 6th International Fruit Fly Symposium 83–90 (IAEA, 2002).
de, C. harlery et al. Changes in phytophagous insect host ranges following the invasion of their community: long-term data for fruit flies. Ecol. Evol. 7, 5181–5190 (2017).
Ramiaranjatovo, G., Reynaud, B. & Jacob, V. Triple electroantennography captures the range and spatial arrangement of olfactory sensory neuron response on an insect antenna. J. Neurosci. Methods 390, 109842 (2023).
Williams, J. & Ringsdorf, A. Human odour thresholds are tuned to atmospheric chemical lifetimes. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190274 (2020).
Andersson, M. N., Schlyter, F., Hill, S. R. & Dekker, T. What reaches the antenna? How to calibrate odor flux and ligand-receptor affinities. Chem. Senses 37, 403–420 (2012).
Geervliet, J. B. F., Vet, L. E. M. & Dicke, M. Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula. Entomol. Exp. Appl. 73, 289–297 (1994).
Beck, J. J., Higbee, B. S., Merrill, G. B. & Roitman, J. N. Comparison of volatile emissions from undamaged and mechanically damaged almonds. J. Sci. Food Agric. 88, 1363–1368 (2008).
Meiners, T. Chemical ecology and evolution of plant-insect interactions: a multitrophic perspective. Curr. Opin. Insect Sci. 8, 1–7 (2015).
El Hadi, M. A. M., Zhang, F. J., Wu, F. F., Zhou, C. H. & Tao, J. Advances in fruit aroma volatile research. Molecules 18, 8200–8229 (2013).
Dweck, H. K. M. et al. The olfactory logic behind fruit odor preferences in larval and adult Drosophila. Cell Rep. 23, 2524–2531 (2018).
Bernays, E. A. Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev. Entomol. 46, 703–727 (2001).
Niven, J. E. & Laughlin, S. B. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211, 1792–1804 (2008).
Cunningham, J. P., Carlsson, M. A., Villa, T. F., Dekker, T. & Clarke, A. R. Do fruit ripening volatiles enable resource specialism in polyphagous fruit flies? J. Chem. Ecol. 42, 931–940 (2016).
Paoli, M. et al. Minute impurities contribute significantly to olfactory receptor ligand studies: tales from testing the vibration theory. eNeuro 4, 1–10 (2017).
Schorkopf, D. L. P. et al. False positives from impurities result in incorrect functional characterization of receptors in chemosensory studies. Prog. Neurobiol. 181, 7 (2019).
Scala, A., Allmann, S., Mirabella, R., Haring, M. A. & Schuurink, R. C. Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 14, 17781–17811 (2013).
Jaenike, J. On optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 14, 350–356 (1978).
Cunningham, J. P. & West, S. A. How host plant variability influences the advantages to learning: a theoretical model for oviposition behaviour in Lepidoptera. J. Theor. Biol. 251, 404–410 (2008).
Joachim-Bravo, I. S., Fernandes, O. A., De Bortoli, S. A. & Zucoloto, F. S. Oviposition behavior of Ceratitis capitata wiedemann (Diptera: Tephritidae): association between oviposition preference and larval performance in individual females. Neotrop. Entomol. 30, 559–564 (2001).
Liu, H., Chen, Z. S., Zhang, D. J. & Lu, Y. Y. BdorOR88a modulates the responsiveness to methyl eugenol in mature males of Bactrocera dorsalis (Hendel). Front. Physiol. 9, 1–17 (2018).
Dhillon, M. K., Singh, R., Naresh, J. S. & Sharma, H. C. The melon fruit fly, Bactrocera cucurbitae: a review of its biology and management. J. Insect Sci. 5, 40 (2005).
Kambura, C. et al. Composition, host range and host suitability of vegetable-infesting tephritids on cucurbits cultivated in Kenya. Afr. Entomol. 26, 379–397 (2018).
Mcquate, G. T., Follett, P. A., Liquido, N. J. & Sylva, C. D. Assessment of navel oranges, clementine tangerines, and rutaceous fruits as hosts of Bactrocera cucurbitae and Bactrocera latifrons (Diptera: Tephritidae). Int. J. Insect Sci. 7, IJIS.S20069 (2015).
Vayssières, J. F., Rey, J. Y. & Traoré, L. Distribution and host plants of Bactrocera cucurbitae in West and Central Africa. Fruits 62, 391–396 (2007).
Virgilio, M., De Meyer, M., White, I. M. & Backeljau, T. African Dacus (Diptera: Tephritidae: molecular data and host plant associations do not corroborate morphology based classifications. Mol. Phylogenet. Evol. 51, 531–539 (2009).
Jacob, V. et al. Current source density mapping of antennal sensory selectivity reveals conserved olfactory systems between tephritids and Drosophila. Sci. Rep. 7, 1–13 (2017).
Agelopoulos, N. et al. Exploiting semiochemicals in insect control. Pestic. Sci. 55, 225–235 (1999).
Hafsi, A. et al. Host plant range of a fruit fly community (Diptera: Tephritidae): does fruit composition influence larval performance? BMC Ecol. 16, 40 (2016).
Jacob, V. Current source density analysis of electroantennogram recordings: a tool for mapping the olfactory response in an insect antenna. Front. Cell. Neurosci. 12, 1–19 (2018).
Myrick, A. J. & Baker, T. C. Increasing signal-to-noise ratio in gas chromatography-electroantennography using a deans switch effluent chopper. J. Chem. Ecol. 44, 111–126 (2018).
Pluskal, T., Castillo, S., Villar-Briones, A. & Orešič, M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 11, 395 (2010).
Ni, Y., Su, M., Qiu, Y., Jia, W. & Du, X. ADAP-GC 3.0: improved peak detection and deconvolution of co-eluting metabolites from GC/TOF-MS data for metabolomics studies. Anal. Chem. 88, 8802–8811 (2016).
US EPA. Estimation Programs Interface SuiteTM for Microsoft® Windows, v.4.11. United States Environmental Protection Agency, (Washington, DC, 2012). https://www.epa.gov/tsca-screening-tools/epi-suitetm-estimation-program-interface.
Manion, J. A. et al. NIST Chemical Kinetics Database, NIST Standard Reference Database 17, Version 7.0 (Web Version), Release 1.6.8, Data Version 2015.09 https://kinetics.nist.gov/ (National Institute of Standards and Technology, 20899–8320).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org (2020).
van den Berg, R. A., Hoefsloot, H. C. J., Westerhuis, J. A., Smilde, A. K. & van der Werf, M. J. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genom. 7, 1–15 (2006).
Grace, S. C. & Hudson, D. A. Processing and visualization of metabolomics data-using R, 67–94 (Intech, 2016).
Jost, L. Partitioning diversity into independent alpha and beta components. Ecology 88, 2427–2439 (2007).
Abouheif, E. A method for testing the assumption of phylogenetic independence in comparative data. Evol. Ecol. Res 1, 895–909 (1999).
Pavoine, S., Ollier, S., Pontier, D. & Chessel, D. Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theor. Popul. Biol. 73, 79–91 (2008).
Ronquist, F. et al. Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
Jacob, V., Ramiaranjatovo, G., Charlery de la Masselière, M. & Duyck, P. F. “Volatile profiles of 28 fruit species and Tephritidae antennal responses: Chemical, EAG and Modeling Data”, https://doi.org/10.18167/DVN1/T3XUXW, CIRAD Dataverse, V1 (2026).
Acknowledgements
The authors would like to thank Serge Glenac and Jim Payet for collecting and rearing the insects. The authors greatly acknowledge the Plant Protection Platform for their technical support (3P, IBISA). This research was conducted within the frameworks of the research platform ‘Biocontrôle et épidémio-surveillance végétale en Ocean Indien’ (https://www.dp-biocontrole-oi.org/) and the UMT BAT ’Biocontrôle en Agriculture Tropicale’. This work was co-funded by the European Union and the Région Réunion. L’Europe s’engage à La Réunion avec le FEDER (European Regional Development Fund ERDF 2024-1248-005756). It was also funded by the Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD) and the French Ministry of Agriculture, as part of the research project GEMDOTIS (Ecophyto II 2018) and ATTRACTIS (Ecophyto II 2023).
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G.R., M.C.M., P.F.D. and V.J. designed the study. G.R. collected the EAG/EAD and behavioural data and analysed all the data. M.C.M. collected the GC–MS data. V.J. contributed to data analysis and did the modelling. T.D., S.L.H. contributed to designing the behavioural tests. P.F.D., B.R. and V.J. supervised the work. G.R., V.J. wrote the manuscript. All authors edited the manuscript.
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Ramiaranjatovo, G., Charlery de la Masselière, M., Dekker, T. et al. Olfaction in fruit flies (Tephritidae) balances detection and discrimination of host fruits. Commun Biol (2026). https://doi.org/10.1038/s42003-026-09751-3
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DOI: https://doi.org/10.1038/s42003-026-09751-3
