Diet acts on sexual behavior development in a male moth

Evan Force , Caroline Suray , Christelle Monsempes , Chloé Danis , Gabrielle Bonfils , Stéphane Debernard , Matthieu Dacher

Insect Science ›› 2025, Vol. 32 ›› Issue (4) : 1439 -1452.

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Insect Science ›› 2025, Vol. 32 ›› Issue (4) : 1439 -1452. DOI: 10.1111/1744-7917.13457
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Diet acts on sexual behavior development in a male moth

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Abstract

In many animals, drastic changes are observed during sexual maturation characterized by the reproductive system development concomitantly to the sexual behavior ontogenesis. These modifications are under the control of internal and external factors such as food. Sexual maturation requires considerable energetic investment, and diet has been shown to affect reproductive activities in many taxonomic groups, especially in insects and vertebrates. By contrast, diet effects on sexual behavior development remain largely unexplored. To elucidate this aspect, we used the male moth Agrotis ipsilon which undergoes sexual maturation occurring between the third and the fifth day postemergence. During this period, males are sensitive to female sex pheromones and a stereotypical sexual behavior characterized by female-oriented flight takes place. In our study, we compared (1) sex pheromone detection by electroantennography recordings and (2) behavioral response in wind tunnel assays between males fed with different diets found in nature. Compared to standard sucrose diet, males fed with sucrose, fructose, and glucose supplemented with sodium (a mineral element necessary for the locomotor activity in several moths) did not respond better to female sex pheromones but clearly exhibited an earlier behavioral response. Thus, such a diet accelerates the development of sex pheromone-mediated oriented flight, probably by facilitating the central processing of sex pheromone information in male A. ipsilon moths. Our results provide new information on the influence of nutritional intake on the ontogenesis of male sexual behavior in animals.

Keywords

Agrotis ipsilon / feeding / insect / oriented flight / sexual maturation / sex pheromone detection

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Evan Force, Caroline Suray, Christelle Monsempes, Chloé Danis, Gabrielle Bonfils, Stéphane Debernard, Matthieu Dacher. Diet acts on sexual behavior development in a male moth. Insect Science, 2025, 32(4): 1439-1452 DOI:10.1111/1744-7917.13457

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References

[1]

Aguilar, P. Bourgeois, T. Maria, A. Couzi, P. Demondion, E. Bozzolan, F. et al. (2023) Methoprene-tolerant and Krüppel homolog 1 are actors of juvenile hormone-signaling controlling the development of male sexual behavior in the moth Agrotis ipsilon. Hormones and Behavior, 150, 105330.

[2]

Angell, C.S. Oudin, M.J. Rode, N.O. Mautz, B.S. Bonduriansky, R. and Rundle, H.D. (2020) Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild. Proceedings of the Royal Society B, 287, 20201876.

[3]

Ankola, K. Aishwarya, D. Anusha, R. Vaishnavi, N. Supriya, V.K. and Puttaraju, H.P. (2021) Ecological significance of puddling as a behavioural phenomenon in the life history of butterfly Papilio polytes Linn. (Lepidoptera: Papilionidae). Journal of Asia-Pacific Entomology, 24, 1-6.

[4]

Axon pCLAMP 11. [WWW Document] (2023) (accessed 3.5.23) URL https://fr.moleculardevices.com/products/axon-patch-clamp-system/acquisition-and-analysis-software/pclamp-software-suite

[5]

Badisco, L. Van Wielendaele, P. and Vanden Broeck, J. (2013) Eat to reproduce: a key role for the insulin signaling pathway in adult insects. Frontiers in Physiology, 4, 202

[6]

Bai, Y. Pei, X.J. Ban, N. Chen, N. Liu, S.N. Li, S. et al. (2022) Nutrition-dependent juvenile hormone sensitivity promotes flight-muscle degeneration during the aphid dispersal-reproduction transition. Development (Cambridge, England), 149, dev200891.

[7]

Barrozo, R.B. Gadenne, C. and Anton, S. (2010) Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. Journal of Experimental Biology, 213, 2933-2939.

[8]

Bifano, T.D. Alegria, T.G.P. and Terra, W.R. (2010) Transporters involved in glucose and water absorption in the Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) anterior midgut. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 157, 1-9.

[9]

Boggs, C.L. and Dau, B. (2004) Resource specialization in puddling lepidoptera. Environmental Entomology, 33, 1020-1024.

[10]

Bozzolan, F. Duportets, L. Limousin, D. Wycke, M.A. Demondion, E. François, A. et al. (2015) Synaptotagmin I, a molecular target for steroid hormone signaling controlling the maturation of sexual behavior in an insect. The FEBS Journal, 282, 1432.

[11]

Caccia, S. Casartelli, M. Grimaldi, A. Losa, E. de Eguileor, M. Pennacchio, F. et al. (2007) Unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect (Aphidius ervi, Hymenoptera) and mammals. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 292, R2284-R2291.

[12]

Castellano, J.M. and Tena-Sempere, M. (2016) Animal modeling of early programming and disruption of pubertal maturation. Puberty from Bench to Clinic, 29, 87-121.

[13]

Causse, R. Buès, R. Barthes, J. and Toubon, J. (1988) Mise en évidence expérimentale de nouveaux constituants des phéromones sexuelles de Scotia ipsilon et Mamestra suasa. Médiateurs chimiques: Comportement et systématique des lépidoptères. Coll. INRA, 46, 75-82.

[14]

Causse, R. Buts, R. Barthes, J. Toubon, J.F. and Poitout, H.S. (1989) Utilisation du piégeage sexuel pour l’étude des migrations de A. ipsilon Hufnagel (Lepidoptera: Noctuidae). Comparaison avec le piégeage lumineux. Bulletin SROP, 12, 49-50.

[15]

Clark, R.M. Zera, A.J. and Behmer, S.T. (2015) Nutritional physiology of life-history trade-offs: how food protein-carbohydrate content influences life-history traits in the wing-polymorphic cricket Gryllus firmus. Journal of Experimental Biology, 218, 298-308

[16]

Colvin, C.W. and Abdullatif, H. (2013) Anatomy of female puberty: the clinical relevance of developmental changes in the reproductive system. Clinical Anatomy, 26, 115-129.

[17]

Cremers, J. and Klugkist, I. (2018) One Direction? A tutorial for circular data analysis using R with examples in cognitive psychology. Frontiers in Psychology, 9, 2040.

[18]

Deisig, N. Dupuy, F. Anton, S. and Renou, M. (2014) Responses to pheromones in a complex odor world: sensory processing and behavior. Insects, 5, 399-422.

[19]

Dogra, G.S. and Gillott, C. (1971) Neurosecretory activity and protease synthesis in relation to feeding in Melanoplus sanguinipes (Fab.). Journal of Experimental Zoology, 177, 41-49.

[20]

Dow, J.A. (1992) pH gradients in lepidopteran midgut. Journal of Experimental Biology, 172, 355-375.

[21]

Du, Y. Feng, B. Li, H. Liu, C. Zeng, J. Pan, L. et al. (2015) Field evaluation of Agrotis ipsilon (Lepidoptera: Noctuidae) pheromone blends and their application to monitoring moth populations in China. Environmental Entomology, 44, 724-733.

[22]

Duportets, L. Dufour, M.C. Bécard, J.M. Gadenne, C. and Couillaud, F. (1996) Inhibition of male corpora allata activity and sexual pheromone responsiveness in the black cutworm, Agrotis ipsilon, by the hypocholesterolemic agent, fluvastatin. Archives of Insect Biochemistry and Physiology, 32, 601-611.

[23]

Duportets, L. Dufour, M.C. Couillaud, F. and Gadenne, C. (1998) Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). Journal of Experimental Biology, 201, 2425-2432.

[24]

Duportets, L. Maria, A. Vitecek, S. Gadenne, C. and Debernard, S. (2013) Steroid hormone signaling is involved in the age-dependent behavioral response to sex pheromone in the adult male moth Agrotis ipsilon. General and Comparative Endocrinology, 186, 58-66.

[25]

Dweck, H.K.M. Ebrahim, S.A.M. Thoma, M. Mohamed, A.A.M. Keesey, I.W. Trona, F. et al. (2015) Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences USA, 112, E2829-E2835.

[26]

Eberhard, S.H. Hrassnigg, N. Crailsheim, K. and Krenn, H.W. (2007) Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera). Journal of Insect Physiology, 53, 126-131.

[27]

Force, E. Couzi, P. Dacher, M. and Debernard, S. (2023) Diet impacts the reproductive system's maturation in the male moth Agrotis ipsilon (Noctuidae, Lepidoptera). Journal of Insect Physiology, 148, 104532.

[28]

Force, E. Sokolowski, M.B.C. Suray, C. Debernard, S. Chatterjee, A. and Dacher, M. (2024a) Regulation of feeding dynamics by the circadian clock, light and sex in an adult nocturnal insect. Frontiers in Physiology, 14, 1304626.

[29]

Force, E. Suray, C. Dacher, M. and Debernard, S. (2024b) Effect of adult male diet on fertilization and hatching in an insect. MicroPublication Biology. https://doi.org/10.17912/micropub.biology.001074

[30]

Gadenne, C. and Anton, S. (2000) Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth. Journal of Insect Physiology, 46, 1195-1206.

[31]

Gadenne, C. Renou, M. and Sreng, L. (1993) Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experientia, 49, 721-724.

[32]

Gassias, E. Durand, N. Demondion, E. Bourgeois, T. Aguilar, P. Bozzolan, F. et al. (2019) A critical role for Dop1-mediated dopaminergic signaling in the plasticity of behavioral and neuronal responses to sex pheromone in a moth. Journal of Experimental Biology, 222, jeb211979.

[33]

Gemeno, C. and Haynes, K.F. (2000) Periodical and age-related variation in chemical communication system of black cutworm moth, Agrotis ipsilon. Journal of Chemical Ecology, 26, 329-342.

[34]

Gemeno, C. and Haynes, K.F. (1998) Chemical and behavioral evidence for a third pheromone component in a North American population of the black cutworm moth, Agrotis ipsilon. Journal of Chemical Ecology, 24, 999-1011.

[35]

Gemeno, C. Lutfallah, A.F. and Haynes, K.F. (2000) Pheromone blend variation and cross-attraction among populations of the black cutworm moth (Lepidoptera: Noctuidae). Annals of the Entomological Society of America, 93, 1322-1328.

[36]

Greiner, B. Gadenne, C. and Anton, S. (2002) Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing. Chemical Senses, 27, 45-48.

[37]

Gu, S.H. Sun, L. Yang, R.N. Wu, K.M. Guo, Y.Y. Li, X.C. et al. (2014) Molecular characterization and differential expression of olfactory genes in the antennae of the black cutworm moth Agrotis ipsilon. PLoS ONE, 9, e103420.

[38]

He, L. Jiang, S. Chen, Y. Wyckhuys, K.A.G. Ge, S. He, W. et al. (2021) Adult nutrition affects reproduction and flight performance of the invasive fall armyworm, Spodoptera frugiperda in China. Journal of Integrative Agriculture, 20, 715-726.

[39]

Hoffmann, A. Bourgeois, T. Munoz, A. Anton, S. Gevar, J. Dacher, M. et al. (2020) A plant volatile alters the perception of sex pheromone blend ratios in a moth. Journal of Comparative Physiology A, 206, 553-570.

[40]

Jarriault, D. Barrozo, R.B. de Carvalho Pinto, C.J. Greiner, B. Dufour, M.C. Masante-Roca, I. et al. (2009) Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: combined effects of octopamine and juvenile hormone. Hormones and Behavior, 56, 185-191.

[41]

Kaushik, S. Kumar, R. and Kain, P. (2018) Salt an essential nutrient: advances in understanding salt taste detection using Drosophila as a model system. Journal of Experimental Neuroscience, 12.

[42]

Kenny, D.A. and Byrne, C.J. (2018) Review: the effect of nutrition on timing of pubertal onset and subsequent fertility in the bull. Animal, 12, s36-s44.

[43]

Kupferberg, S.J. (1997) The role of larval diet in anuran metamorphosis. American Zoologist, 37, 146-159.

[44]

Lebreton, S. Trona, F. Borrero-Echeverry, F. Bilz, F. Grabe, V. Becher, P.G. et al. (2015) Feeding regulates sex pheromone attraction and courtship in Drosophila females. Scientific Reports, 5, 13132.

[45]

Li, Y. Wang, W. and Lim, H.Y. (2021) Drosophila solute carrier 5A5 regulates systemic glucose homeostasis by mediating glucose absorption in the midgut. International Journal of Molecular Sciences, 22, 12424.

[46]

Lin, H.H. Cao, D.S. Sethi, S. Zeng, Z. Chin, J.S.R. Chakraborty, T.S. et al. (2016) Hormonal modulation of pheromone detection enhances male courtship success. Neuron, 90, 1272-1285.

[47]

Masumura, M. Satake, S. Saegusa, H. and Mizoguchi, A. (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. General and Comparative Endocrinology, 118, 393-399.

[48]

Matsunami, H. and Amrein, H. (2003) Taste and pheromone perception in mammals and flies. Genome Biology, 4, 220.

[49]

McLean, H. and Caveney, S. (1993) Na+-dependent medium-affinity uptake of l-glutamate in the insect epidermis. Journal of Comparative Physiology B, 163, 297-306.

[50]

Mitra, C. Reynoso, E. Davidowitz, G. and Papaj, D. (2016) Effects of sodium puddling on male mating success, courtship and flight in a swallowtail butterfly. Animal Behaviour, 114, 203-210.

[51]

Molleman, F. (2010) Puddling: from natural history to understanding how it affects fitness. Entomologia Experimentalis Et Applicata, 134, 107-113.

[52]

Nicolson, S.W. (1976) Diuresis in the cabbage white butterfly, Pieris brassicae: water and ion regulation and the role of the hindgut. Journal of Insect Physiology, 22, 1623-1630.

[53]

Niewalda, T. Singhal, N. Fiala, A. Saumweber, T. Wegener, S. and Gerber, B. (2008) Salt processing in larval Drosophila: choice, feeding, and learning shift from appetitive to aversive in a concentration-dependent way. Chemical Senses, 33, 685-692.

[54]

Perez-Hedo, M. Rivera-Perez, C. and Noriega, F.G. (2014) Starvation increases insulin sensitivity and reduces juvenile hormone synthesis in mosquitoes. PLoS ONE, 9, e86183.

[55]

Peyronnet, O. Vachon, V. Schwartz, J.L. and Laprade, R. (2000) Ion channel activity from the midgut brush-border membrane of gypsy moth (Lymantria dispar) larvae. Journal of Experimental Biology, 203, 1835-1844.

[56]

Picimbon, J.F. Gadenne, C. Bécard, J.M. Clément, J.L. and Sreng, L. (1997) Sex pheromone of the french black cutworm moth, Agrotis ipsilon (Lepidoptera: Noctuidae): Identification and regulation of a multicomponent blend. Journal of Chemical Ecology, 23, 211-230.

[57]

Plesnar-Bielak, A. Woch, K.R. Małszycki, M.A. Alkhawlany, A.T.H. Hołysz, A. Assis Correia, J.F. et al. (2017) Larval and adult nutrition effects on reproductive traits in the red flour beetle. Journal of Zoology, 302, 79-87.

[58]

Pontes, G. Pereira, M.H. and Barrozo, R.B. (2017) Salt controls feeding decisions in a blood-sucking insect. Journal of Insect Physiology, 98, 93-100.

[59]

R Core Team. (2021) R: The R Project for statistical computing. (accessed 2.16.22) https://www.r-project.org/

[60]

Ravenscraft, A. and Boggs, C.L. (2016) Nutrient acquisition across a dietary shift: fruit feeding butterflies crave amino acids, nectivores seek salt. Oecologia, 181, 1-12.

[61]

Renou, M. Gadenne, C. and Tauban, D. (1996) Electrophysiological investigations of pheromone-sensitive sensilla in the hybrids between two moth species. Journal of Insect Physiology, 42, 267-277.

[62]

Rewitz, K.F. Yamanaka, N. and O'Connor, M.B. (2013) Developmental checkpoints and feedback circuits time insect maturation. Current Topics in Developmental Biology, 103, 1-33.

[63]

Roy, R. Schmitt, A.J. Thomas, J.B. and Carter, C.J. (2017) Review: nectar biology: from molecules to ecosystems. Plant Science, 262, 148-164.

[64]

Seong, K.H. Uemura, T. and Kang, S. (2023) Road to sexual maturity: behavioral event schedule from eclosion to first mating in each sex of Drosophila melanogaster. Iscience, 26, 107502.

[65]

Shirai, Y. (2006) Flight activity, reproduction, and adult nutrition of the beet webworm, Spoladea recurvalis (Lepidoptera: Pyralidae). Applied Entomology and Zoology, 41, 405-414.

[66]

Smedley, S.R. and Eisner, T. (1996) Sodium: a male moth's gift to its offspring. Proceedings of the National Academy of Sciences USA, 93, 809-813.

[67]

Snell-Rood, E.C. Espeset, A. Boser, C.J. White, W.A. and Smykalski, R. (2014) Anthropogenic changes in sodium affect neural and muscle development in butterflies. Proceedings of the National Academy of Sciences USA, 111, 10221-10226.

[68]

Tolle, A.E. and Wagner, W.E. (2011) Costly signals in a field cricket can indicate high- or low-quality direct benefits depending upon the environment. Evolution; International Journal of Organic Evolution, 65, 283-294.

[69]

Tu, M.P. Yin, C.M. and Tatar, M. (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. General and Comparative Endocrinology, 142, 347-356.

[70]

Vandroux, P. Li, Z. Capoduro, R. François, M.C. Renou, M. Montagné, N. et al. (2022) Activation of pheromone-sensitive olfactory neurons by plant volatiles in the moth Agrotis ipsilon does not occur at the level of the pheromone receptor protein. Frontiers in Ecology and Evolution, 10, 1035252.

[71]

Watanabe, T. and Sasaki, K. (2021) Regulation of dopamine production in the brains during sexual maturation in male honey bees. Journal of Insect Physiology, 132, 104270.

[72]

Wagner, W.E. and Hoback, W.W. (1999) Nutritional effects on male calling behaviour in the variable field cricket. Animal Behaviour, 57, 89-95.

[73]

Wyatt, G.R. and Kalf, G.F. (1957) The chemistry of insect hemolymph. The Journal of General Physiology, 40, 833-847.

[74]

Xiao, K. Shen, K. Zhong, J.F. and Li, G.Q. (2010) Effects of dietary sodium on performance, flight and compensation strategies in the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Frontiers in Zoology, 7, 11.

[75]

Zeiske, W. (1992) Insect ion homeostasis. Journal of Experimental Biology, 172, 323-334.

[76]

Zhang, B. Zhang, Y. Guan, R. Du, M. Yin, X. Zhao, W. et al. (2022) Trehalase is required for sex pheromone biosynthesis in Helicoverpa armigera. Insect Molecular Biology, 31, 334-345.

[77]

Zibaee, A. Bandani, A.R. and Ramzi, S. (2008) Lipase and invertase activities in midgut and salivary glands of Chilo suppressalis (Walker) (Lepidoptera, Pyralidae), rice striped stem borer [For this article an Erratum has been published]. Invertebrate Survival Journal, 5, 180-189.

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