Rhythmic biosynthesis of sex pheromone modulates the calling and mating behaviors of Tuta absoluta (Lepidoptera: Gelechiidae)

Minglei Luo , Liang Huang , Furong Gui , Arnó Judit , Peng Han , Fanghao Wan , Guifen Zhang , Cong Huang , Yibo Zhang

New Plant Protection ›› 2025, Vol. 2 ›› Issue (4) : e70030

PDF
New Plant Protection ›› 2025, Vol. 2 ›› Issue (4) :e70030 DOI: 10.1002/npp2.70030
ORIGINAL PAPER
Rhythmic biosynthesis of sex pheromone modulates the calling and mating behaviors of Tuta absoluta (Lepidoptera: Gelechiidae)
Author information +
History +
PDF

Abstract

Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a significant global pest of tomato. Although sex pheromones serve as effective biological control tools, their utilization remains inefficient due to a limited understanding of the circadian rhythms of courtship and mating. This study details a six-step “morning flight–mating” behavioral sequence in T. absoluta: (1) resting, (2) preparation for morning flight, (3) morning flight, (4) courtship, (5) mating, and (6) post-mating cessation. Laboratory observations revealed that their rhythmic behavior occurred between 05:30 and 08:00, with a pronounced peak from 05:30 to 06:30, and high population densities negatively impacted mating success rates. Field experiments corroborated these laboratory observations. Furthermore, the synchronized synthesis and release of major and minor sex pheromone components aligned with the timing of calling and mating behavior. These findings suggest that the “morning flight–mating” rhythm is mediated by the pheromone release cycle. Our results offer a basis for optimizing the timing of pheromone-based control techniques, such as mating disruption and mass trapping, to enhance the efficiency and reduce the cost of pest control.

Keywords

calling behavior / mating rhythm / morning flight / sex pheromone / Tuta absoluta

Cite this article

Download citation ▾
Minglei Luo, Liang Huang, Furong Gui, Arnó Judit, Peng Han, Fanghao Wan, Guifen Zhang, Cong Huang, Yibo Zhang. Rhythmic biosynthesis of sex pheromone modulates the calling and mating behaviors of Tuta absoluta (Lepidoptera: Gelechiidae). New Plant Protection, 2025, 2(4): e70030 DOI:10.1002/npp2.70030

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Brady, D., Saviane, A., Cappellozza, S., & Sandrelli, F. (2021). The circadian clock in Lepidoptera. Frontiers in Physiology, 12, 776826. https://doi.org/10.3389/fphys.2021.776826

[2]

Kotwica-Rolinska, J., Chodáková, L., Smykal, V., Damulewicz, M., Provazník, J., Wu, B. C. H., Hejníková, M., Chvalová, D., & Dolezel, D. (2022). Loss of timeless underlies an evolutionary transition within the circadian clock. Molecular Biology and Evolution, 39(1), msab346. https://doi.org/10.1093/molbev/msab346

[3]

Somers, J., Georgiades, M., Su, M. P., Bagi, J., Andrés, M., Alampounti, A., Mills, G., Ntabaliba, W., Moore, S. J., Spaccapelo, R., & Albert, J. T. (2022). Hitting the right note at the right time: Circadian control of audibility in mosquito mating swarms is mediated by flight tones. Science Advances, 8(2), eabl4844. https://doi.org/10.1126/sciadv.abl4844

[4]

Dorcikova, M. M., Duret, L. C., Pottie, E., & Nagoshi, E. (2023). Circadian clock disruption promotes the degeneration of dopaminergic neurons in male. Nature Communications, 14(1), 5908. https://doi.org/10.1038/s41467-023-41540-y

[5]

Zhang, Y., Li, Y., Barber, A. F., Noya, S. B., Williams, J. A., Li, F., Daniel, S. G., Bittinger, K., Fang, J., & Sehgal, A. (2023). The microbiome stabilizes circadian rhythms in the gut. Proceedings of the National Academy of Sciences of the United States of America, 120(5), e2217532120. https://doi.org/10.1073/pnas.2217532120

[6]

Duffield, G. E. (2024). Circadian and daily rhythms of disease vector mosquitoes. Current Opinion in Insect Science, 63, 101179. https://doi.org/10.1016/j.cois.2024.101179

[7]

Zhang, J., Li, S., Li, W., Chen, Z., Guo, H., Liu, J., Xu, Y., Xiao, Y., Zhang, L., Arunkumar, K. P., Smagghe, G., Xia, Q., Goldsmith, M. R., Takeda, M., & Mita, K. (2021). Circadian regulation of night feeding and daytime detoxification in a formidable Asian pest. Communications Biology, 4(1), 286. https://doi.org/10.1038/s42003-021-01816-9

[8]

Wang, Y., Dong, H., Qu, Y., Zhou, Y., Qin, J., Li, K., Luo, C., Ren, B., Cao, Y., Zhang, S., Yin, J., & Leal, W. S. (2024). Circabidian rhythm of sex pheromone reception in a scarab beetle. Current Biology, 34(3), 568–578. https://doi.org/10.1016/j.cub.2023.12.057

[9]

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., Silva, T. L. A. E., Pascini, T. V., Wang, S., & Jacobs-Lorena, M. (2021). Clock genes and environmental cues coordinate pheromone synthesis, swarming, and mating. Science, 371(6527), 411–415. https://doi.org/10.1126/science.abd4359

[10]

van Doorn, G. S., Schepers, J., Hut, R. A., & Groot, A. T. (2024). Sex-specific expression of circadian rhythms enables allochronic speciation. Evolution Letters, 9(1), 65–76. https://doi.org/10.1093/evlett/qrae049

[11]

Krittika, S., & Yadav, P. (2020). Circadian clocks: An overview on its adaptive significance. Biological Rhythm Research, 51(7), 1109–1132. https://doi.org/10.1080/09291016.2019.1581480

[12]

Cong, Q., & Grishin, N. V. (2018). Comparative analysis of swallowtail transcriptomes suggests molecular determinants for speciation and adaptation. Genome, 61(12), 843–855. https://doi.org/10.1139/gen-2018-0084

[13]

Hoikkala, A., & Poikela, N. (2022). Adaptation and ecological speciation in seasonally varying environments at high latitudes: Drosophila virilis group. Fly, 16(1), 85–104. https://doi.org/10.1080/19336934.2021.2016327

[14]

Gottlieb, D. (2019). Agro-chronobiology: Integrating circadian clocks/time biology into storage management. Journal of Stored Products Research, 82, 9–16. https://doi.org/10.1016/j.jspr.2019.03.003

[15]

Hotta, C. T. (2021). From crops to shops: How agriculture can use circadian clocks. Journal of Experimental Botany, 72(22), 7668–7679. https://doi.org/10.1093/jxb/erab371

[16]

Kristensen, N. P., Scoble, M. J., & Karsholt, O. (2007). Lepidoptera phylogeny and systematics: The state of inventorying moth and butterfly diversity. Zootaxa, 1668(1), 699–747. https://doi.org/10.11646/zootaxa.1668.1.30

[17]

Braak, N., Neve, R., Jones, A. K., Gibbs, M., & Breuker, C. J. (2018). The effects of insecticides on butterflies – A review. Environmental Pollution, 242, 507–518. https://doi.org/10.1016/j.envpol.2018.06.100

[18]

Rizvi, S. A. H., George, J., Reddy, G. V. P., Zeng, X., & Guerrero, A. (2021). Latest developments in insect sex pheromone research and its application in agricultural pest management. Insects, 12(6), 484. https://doi.org/10.3390/insects12060484

[19]

Wang, H. L., Ding, B. J., Dai, J. Q., Nazarenus, T. J., Borges, R., Mafra-Neto, A., Cahoon, E. B., Hofvander, P., Stymne, S., & Löfstedt, C. (2022). Insect pest management with sex pheromone precursors from engineered oilseed plants. Nature Sustainability, 5(11), 981–990. https://doi.org/10.1038/s41893-022-00949-x

[20]

Ghosh, S., Suray, C., Bozzolan, F., Palazzo, A., Monsempès, C., Lecouvreur, F., & Chatterjee, A. (2024). Pheromone-mediated command from the female to male clock induces and synchronizes circadian rhythms of the moth Spodoptera littoralis. Current Biology, 34(7), 1414–1425. https://doi.org/10.1016/j.cub.2024.02.042

[21]

Xiang, Y. Y., Zhang, X. W., & Xu, G. M. (2018). The timing of calling and mating in Heterolocha jinyinhuaphaga and the influence of environmental determinants. Journal of Insect Behavior, 31(3), 334–346. https://doi.org/10.1007/s10905-018-9682-0

[22]

Kawahara, A. Y., Plotkin, D., Hamilton, C. A., Gough, H., St Laurent, R., Owens, H. L., Homziak, N. T., & Barber, J. R. (2018). Diel behavior in moths and butterflies: A synthesis of data illuminates the evolution of temporal activity. Organisms, Diversity and Evolution, 18(1), 13–27. https://doi.org/10.1007/s13127-017-0350-6

[23]

Cheng, W. J., Zheng, X. L., Wang, P., Zhou, L. L., Lei, C. L., Si, S. Y., & Wang, X. P. (2015). The circadian rhythm of flight activity of Spodoptera exigua males in response to sex pheromone. Entomologia Experimentalis et Applicata, 154(2), 154–160. https://doi.org/10.1111/eea.12266

[24]

Zhou, K. N., Zhang, S. Y., Zeng, J. P., Luo, D., & Liu, X. P. (2016). Reproductive behavior of the masson pine caterpillar, Dendrolimus punctatus (Lepidoptera: Lasiocampidae) under laboratory conditions. Applied Entomology and Zoology, 51(2), 205–212. https://doi.org/10.1007/s13355-015-0389-9

[25]

Broadhead, G. T., Basu, T., von Arx, M., & Raguso, R. A. (2017). Diel rhythms and sex differences in the locomotor activity of hawkmoths. Journal of Experimental Biology, 220(Pt 8), 1472–1480. https://doi.org/10.1242/jeb.143966

[26]

Xu, J. W., Li, L. L., Wang, M., Yang, H. H., Yao, W. C., Dewer, Y., Zhu, X. Y., & Zhang, Y. N. (2022). Identification and dynamic expression profiling of circadian clock genes in Spodoptera litura provide new insights into the regulation of sex pheromone communication. Bulletin of Entomological Research, 112(1), 78–90. https://doi.org/10.1017/S0007485321000559

[27]

Chen, L., Wang, X. Y., Lu, W., & Zheng, X. L. (2021). Sexual communication in diurnal moths: Behaviors and mechanisms. International Journal of Tropical Insect Science, 41(1), 15–24. https://doi.org/10.1007/s42690-020-00174-z

[28]

Sarto I Monteys, V., Quero, C., Santa-Cruz, M. C., Rosell, G., & Guerrero, A. (2016). Sexual communication in day-flying Lepidoptera with special reference to castniids or ‘butterfly-moths. Bulletin of Entomological Research, 106(4), 421–431. https://doi.org/10.1017/S0007485316000158

[29]

Zheng, X. L., Liu, J. Y., Zhang, Z. L., Wang, P., & Lu, W. (2019). Diel rhythms of sexual behavior and pheromone responses in Phauda flammans Walker (Lepidoptera: Zygaenidae). Pest Management Science, 75(11), 3070–3075. https://doi.org/10.1002/ps.5423

[30]

Wu, S., Refinetti, R., Kok, L. T., Youngman, R. R., Reddy, G. V., & Xue, F. S. (2014). Photoperiod and temperature effects on the adult eclosion and mating rhythms in Pseudopidorus fasciata (Lepidoptera: Zygaenidae). Environmental Entomology, 43(6), 1650–1655. https://doi.org/10.1603/EN14164

[31]

Li, X., Jia, X., Xiang, H., Diao, H., Yan, Y., Wang, Y., & Ma, R. (2019). The effect of photoperiods and light intensity on mating behavior and reproduction of Grapholita molesta (Lepidoptera: Tortricidae). Environmental Entomology, 48(5), 1035–1041. https://doi.org/10.1093/ee/nvz066

[32]

Levi-Zada, A., & Byers, J. A. (2021). Circadian rhythms of insect pheromone titer, calling, emission, and response: A review. Science and Nature, 108(5), 35. https://doi.org/10.1007/s00114-021-01746-w

[33]

Ghosh, S., Suray, C., Bozzolan, F., Palazzo, A., Monsempes, C., Lecouvreur, F., & Chatterjee, A. (2024). Pheromone-mediated command from the female to male clock induces and synchronizes circadian rhythms of the moth Spodoptera littoralis. Current Biology, 34(7), 1414–1425. https://doi.org/10.1016/j.cub.2024.02.042

[34]

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(6527), 411–415. https://doi.org/10.1126/science.abd4359

[35]

Desneux, N., Han, P., Mansour, R., Arno, J., Brevault, T., Campos, M. R., Chailleux, A., Guedes, R. N. C., Karimi, J., Konan, K. A. J., Lavoir, A. V., Luna, M. G., Perez-Hedo, M., Urbaneja, A., Verheggen, F. J., Zappala, L., Abbes, K., Ali, A., Bayram, Y., … Biondi, A. (2022). Integrated pest management of Tuta absoluta: Practical implementations across different world regions. Journal of Pest Science, 95(1), 17–39. https://doi.org/10.1007/s10340-021-01442-8

[36]

Biondi, A., Guedes, R. N. C., Wan, F. H., & Desneux, N. (2018). Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: Past, present, and future. Annual Review of Entomology, 63(1), 239–258. https://doi.org/10.1146/annurev-ento-031616-034933

[37]

Tarusikirwa, V. L., Machekano, H., Mutamiswa, R., Chidawanyika, F., & Nyamukondiwa, C. (2020). Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for integrated management initiatives. Insects, 11(11), 764. https://doi.org/10.3390/insects11110764

[38]

Guedes, R. N. C., Roditakis, E., Campos, M. R., Haddi, K., Bielza, P., Siqueira, H. A. A., Tsagkarakou, A., Vontas, J., & Nauen, R. (2019). Insecticide resistance in the tomato pinworm Tuta absoluta: Patterns, spread, mechanisms, management and outlook. Journal of Pest Science, 92(4), 1329–1342. https://doi.org/10.1007/s10340-019-01086-9

[39]

Zhang, G. F., Zhang, Y. B., Zhao, L., Wang, Y. S., Huang, C., Lu, Z. C., Li, P., Liu, W. C., Xian, X. Q., Zhao, J. N., Li, Y. H., Wan, F. H., Liu, W. X., & Wang, F. L. (2023). Determination of hourly distribution of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) using sex pheromone and ultraviolet light traps in protected tomato crops. Horticulturae, 9(3), 402. https://doi.org/10.3390/horticulturae9030402

[40]

Jabamo, T., Ayalew, G., Goftishu, M., & Wakgari, M. (2023). Integrated effect of insecticide and sex pheromone on the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Crop Protection, 171, 106285. https://doi.org/10.1016/j.cropro.2023.106285

[41]

Lobos, E., Occhionero, M., Werenitzky, D., Fernandez, J., Gonzalez, L. M., Rodriguez, C., Calvo, C., Lopez, G., & Oehlschlager, A. C. (2013). Optimization of a trap for Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) and trials to determine the effectiveness of mass trapping. Neotropical Entomology, 42(5), 448–457. https://doi.org/10.1007/s13744-013-0141-5

[42]

Lee, M. S., Albajes, R., & Eizaguirre, M. (2014). Mating behaviour of female Tuta absoluta (Lepidoptera: Gelechiidae): Polyandry increases reproductive output. Journal of Pest Science, 87(3), 429–439. https://doi.org/10.1007/s10340-014-0576-4

[43]

Toshova, T. B., Subchev, M. A., & Tóth, M. (2007). Role of olfactory and visual stimuli in the mating behaviour of male vine bud moths, Theresimima ampellophaga (Lepidoptera: Zygaenidae). European Journal of Entomology, 104(1), 57–65. https://doi.org/10.14411/eje.2007.009

[44]

Balkenius, A., Rosén, W., & Kelber, A. (2006). The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. Journal of Comparative Physiology A-Neuroethology, Sensory, Neural, and Behavioral Physiology, 192(4), 431–437. https://doi.org/10.1007/s00359-005-0081-6

[45]

Quero, C., Sarto I Monteys, V., Rosell, G., Puigmartí, M., & Guerrero, A. (2017). Sexual communication in castniid moths: Males mark their territories and appear to bear all chemical burden. PLoS One, 12(2), e0171166. https://doi.org/10.1371/journal.pone.0171166

[46]

Groot, A. T. (2014). Circadian rhythms of sexual activities in moths: A review. Frontiers in Ecology and Evolution, 2, 43. https://doi.org/10.3389/fevo.2014.00043

[47]

Liu, S., Zhou, J., Kong, L., Cai, Y., Liu, H., Xie, Z., Xiao, X., James, A. A., & Chen, X. (2022). Clock genes regulate mating activity rhythms in the vector mosquitoes, Aedes albopictus and Culex quinquefasciatus. PLoS Neglected Tropical Diseases, 16(12), e0010965. https://doi.org/10.1371/journal.pntd.0010965

[48]

Rath, A., Benita, M., Doron, J., Scharf, I., & Gottlieb, D. (2021). Social communication activates the circadian gene Tctimeless in Tribolium castaneum. Scientific Reports, 11(1), 16152. https://doi.org/10.1038/s41598-021-95588-1

[49]

Winkler, L., Eilhardt, R., & Janicke, T. (2023). Population density affects sexual selection in an insect model. Functional Ecology, 37(10), 2734–2747. https://doi.org/10.1111/1365-2435.14410

[50]

Cattelan, S., Evans, J. P., Garcia-Gonzalez, F., Morbiato, E., & Pilastro, A. (2020). Dietary stress increases the total opportunity for sexual selection and modifies selection on condition-dependent traits. Ecology Letters, 23(3), 447–456. https://doi.org/10.1111/ele.13443

[51]

Winkler, L., & Janicke, T. (2022). Diet quality impairs male and female reproductive performance and affects the opportunity for selection in an insect model. Ecology and Evolution, 12(11), e9533. https://doi.org/10.1002/ece3.9533

[52]

Svatos, A., Attygalle, A. B., Jham, G. N., Frighetto, R. T. S., Vilela, E. F., Saman, D., & Meinwald, J. (1996). Sex pheromone of tomato pest Scrobipalpuloides absoluta (Lepidoptera: Gelechiidae). Journal of Chemical Ecology, 22(4), 787–800. https://doi.org/10.1007/Bf02033586

[53]

Griepink, F. C., van Beek, T. A., Posthumus, M. A., de Groot, A., Hans Visser, J., & Voerman, S. (1996). Identification of the sex pheromone of Scrobipalpula absoluta; determination of double bond positions in triple unsaturated straight chain molecules by means of dimethyl disulphide derivatization. Tetrahedron Letters, 37(3), 411–414. https://doi.org/10.1016/0040-4039(95)02172-8

[54]

Cheng, W. J., Zheng, X. L., Wang, P., Zhou, L. L., Lei, C. L., Si, S. Y., & Wang, X. P. (2015). The circadian rhythm of flight activity of males in response to sex pheromone. Entomologia Experimentalis et Applicata, 154(2), 154–160. https://doi.org/10.1111/eea.12266

[55]

Uchoa-Fernandes, M. A., Della Lucia, T. M. C., & Vilela, E. F. (1995). Mating, oviposition and pupation of Scrobipalpuloides absoluta (Meyr.)(Lepidoptera: Gelechiidae). Anais Da Sociedade Entomológica Do Brasil, 24(1), 159–164. https://doi.org/10.37486/0301-8059.v24i1.1007

[56]

Zhang, D., Huang, X. Y., Gang, S., Song, L., Li, Y. H., Zhang, W. M., Meng, W., & Du, Y. J. (2024). Effects of sex pheromones released by active aerosol dispensers on the calling and mating of Tuta absoluta (Lepidoptera: Gelechiidae) and their control efficacy. Acta Entomologica Sinica, 67, 1661–1670. https://doi.org/10.16380/j.kcxb.2024.12.009

RIGHTS & PERMISSIONS

2025 The Author(s). New Plant Protection published by John Wiley & Sons Australia, Ltd on behalf of Institute of Plant Protection, Chinese Academy of Agricultural Sciences.

PDF

9

Accesses

0

Citation

Detail

Sections
Recommended

/