Abstract
Recent GS-MS and GC-EAD studies of pheromone production and perception in caddisflies and lower moths have shown that these insects use a rather limited selection of volatiles as attractants. Most of them are alcohols and ketones, although the diversity of chemicals produced by sternal glands of abdominal segment V is much wider, especially in the lower Trichoptera. Sternal pheromone glands produce only short-chain polymers in all Amphiesmenoptera. These glands are part of the ground-plan for the related orders, Trichoptera and Lepidoptera, occurring in both sexes and producing similar but not identical sets of components in males and females. The presence of pheromone volatiles is shown to be restricted to the gland segments (Fig. 1), although some other shortchain polymers do occur in the head of females of Molanna angustata (Molannidae). The pheromone blends of lower Trichoptera (Glossosomatidae, Rhyacophilidae, and Philopotamidae) are multi-component and resemble plant volatiles in composition. A hypothesis of the origin of pheromone communication is proposed postulating basic resemblance of early pheromones and plant volatiles in variety and chemical composition. These pheromones were detected by non-specialized receptors of the amphiesmenopteran ancestor and served as guides for insect aggregation on plants as well as on shores of reservoirs, marking the places suitable for a wide variety of species. The primary aggregation function of pheromones was changed in more advanced communication systems to the species-specific signaling with sex-related asymmetry of signals, although the aggregation significance persisted in some species. Pheromone communication has disappeared in some most advanced lineages (e.g., Leptoceridae) with parallel reduction of glands, secretion, and antennal receptors. The pheromone composition does not show gradual divergent evolution in related species; instead, abrupt transformation of pheromone blends with persistence of major components in remote families seems to be the typical case.
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References
Ansteeg, O. and Dettner, K., “Chemistry and Possible Biological Significance of Secretions from a Gland Discharging at the 5th Abdominal Sternite of Adult Caddisflies (Trichoptera),” Entomol. Gen. 15, 303–312 (1991).
Ayasse, M., Paxton, R.J., and Tengo, J., “Mating Behavior and Chemical Communication in the Order Hymenoptera,” Annu. Rev. Entomol. 46, 31–78 (2001).
Bergmann, J., Identifizierung und Synthese fluchtiger Inhaltsstoffe aus Insekten. Diss. zur Erlangung des Doktorgrades des Fachbereiches Chemie der Universität Hamburg (Hamburg, 2002).
Bergmann, J., Löfstedt, C., Ivanov, V.D., and Francke, W., “Identification and Assignment of the Absolute Configuration of Biologically Active Methyl-Branched Ketones from Limnephilid Caddisflies,” Eur. J. Org. Chem., No. 16, 3175–3179 (2001).
Bergmann, J., Löfstedt, C., Ivanov, V.D., and Francke, W., “Electrophysiologically Active Compounds Identified from Six Species of Caddisflies (Trichoptera),” in Proceedings of 10th International Symposium on Trichoptera, Germany, Potsdam, 31 July–6 August 2000 (Keltern, 2002), pp. 37–46 [Nova Suppl. Entomol. 15, 37–46 (2002)].
Bergmann, J., Löfstedt, C., Ivanov, V.D., and Francke, W., “Identification and Synthesis of New Bicyclic Acetals from Caddisflies (Trichoptera),” Tetrahedron Letters 45, 3669–3672 (2004).
Billen, J. and Morgan, E.D., “Pheromone Communication in Social Insects: Sources and Secretions,” in Pheromone Communication in Social Insects: Ants, Wasps, Bees, and Termites, Ed. by R.K. Vander Meer, M.D. Breed, K.E. Espelie, and M.L. Winston (Westview Press, Colorado, USA, 1998), pp. 3–33.
Bjostad, L.B., Jewett, D.K., and Brigham, D.L., “Sex Pheromone of Caddisfly Hesperophylax occidentalis (Banks) (Trichoptera: Limnephilidae),” J. Chem. Ecol. 22(1), 103–121 (1996).
Byer, J.A., “Pheromone Component Patterns of Moth Evolution Revealed by Computer Analysis of the Pherolist,” J. Animal Ecol. 75, 399–407 (2006).
Djernaes, M. and Sperling, F.A.H., “Evolutionary Riddles and Phylogenetic Twiddles: the Ground Plan and Early Diversification of the Sternum V Gland in Amphiesmenoptera (Trichoptera + Lepidoptera),” in Proceedings of the 13th International Symposium on Trichoptera. Białowieża, Poland, June 22–27, 2009 (Zoosymposia No. 5) (Magnolia Press, 2011), pp. 83–100.
Djernaes, M. and Sperling, F.A.H., “Exploring a Key Synapomorphy: Correlations between Structure and Function in the Sternum V Glands of Trichoptera and Lepidoptera (Insecta),” Biol. J. Linn. Soc. 106, 561–579 (2012).
Duffield, R.M., Blum, M.S., Wallace, J.B., et al., “Chemistry of the Defense Secretion of the Caddisfly Pycnopsyche scabripennis (Trichoptera: Limnephilidae),” J. Chem. Ecol. 3, 649–656 (1977).
El-Sayed, A.M., The Pherobase: Database of Pheromones and Semiochemicals (2013), http://www.pherobase.com.
Elizarov, Yu.A., Chemoreception in Insects (Moscow State Univ., Moscow, 1978) [in Russian].
Hashimoto, Y. and Kobayashi, Y., “Morphology of Sternum V Glands in Three Caddisfly Species, Stenopsyche marmorata, Eubasilissa regina and Nemotaulius admorsus (Insecta: Trichoptera),” Entomol. Sci. 12(3), 298–307 (2009).
Ivanov, V.D., “The Behavior of Caddisflies in Flight,” Latv. Entomol. 28, 85–94 (1985).
Ivanov, V.D., “Principles of the Sexual Communication in Caddisflies (Insecta, Trichoptera),” in Sensory Systems of Arthropods, Ed. by K. Wiese et al. (Birkhuser Verlag, Basel, 1993), pp. 609–626.
Ivanov, V.D., Laanmaa, M.K., and Tsibulsky, A.I., “Attraction of Caddisflies to Pheromone Traps in the Ust-Lena Reserve,” in Hydrobiological Studies in Nature Reserves (Nauka, Moscow, 1996), pp. 121–128 [in Russian].
Ivanov, V.D. and Melnitsky, S.I., “Structure of Sternal Pheromone Glands in Caddisflies (Trichoptera),” Entomol. Obozr. 78(3), 505–526 (1999) [Entomol. Rev. 79 (8), 926–942 (1999)].
Ivanov, V.D. and Melnitsky, S.I., “Structure of Pheromone Glands in Trichoptera,” in Proceedings of the 10th International Symposium on Trichoptera, Germany, Potsdam, 31 July–6 August 2000 (Keltern, 2002), pp. 17–28 [Nova Suppl. Entomol. 15, 17–28 (2002)].
Ivanov, V.D. and Melnitsky, S.I., “New Caddisfly Species of the Genus Wormaldia (Trichoptera: Philopotamidae) from Baltic Amber,” Paleontol. J. 39(3), 284–288 (2005).
Ivanov, V.D. and Melnitsky, S.I., “The Morphology of Dajella tenera (Trichoptera, Glossosomatidae): Taxonomic Status and Evidence for Pheromone Communication in the Mesozoic,” Entomol. Obozr. 85(2), 365–374 (2006) [Entomol. Rev. 86 (5), 568–575 (2006)].
Ivanov, V.D. and Melnitsky, S.I., “Structure and Morphological Types of the Antennal Olfactory Sensilla in Phryganeidae and Limnephilidae (Insecta: Trichoptera),” in Proceedings of the 13th International Symposium on Trichoptera. Białowieża, Poland, June 22–27, 2009 (Zoosymposia No. 5) (Magnolia Press, 2011), pp. 210–234.
Ivanov, V.D. and Melnitsky, S.I., “Ten New Species of Caddisflies (Insecta: Trichoptera) from the Baltic Amber,” Paleontol. J. 47(2), 166–176 (2013a).
Ivanov, V.D. and Melnitsky, S.I., “The Structure of Pheromones and Antennal Receptors in Caddisflies (Insecta: Trichoptera),” in Hydroentomology in Russia and Adjacent Countries: Proceedings of V All-Russia Symposium on Amphibiotic and Aquatic Insects (Borok, 2013b), pp. 62–68.
Ivanov, V.D., Melnitsky, S.I., and Syrnikov, Yu.S., “Attraction of Males of Anabolia laevis Zett. (Trichoptera: Limnephilidae) to Pheromone Traps,” Vestnik Sankt-Peterburg. Gos. Univ. Ser. 3, No. 19, 113–116 (2000).
Ivanov, V.D., Melnitsky, S.I., and Zhukovskaya, M.I., “Chemical Communication of Anabolia laevis Zett. (Trichoptera: Limnephilidae): the Behavioral and Physiological Aspects,” Sensor. Sistemy 22(4), 333–341 (2008).
Ivanov, V.D. and Sukacheva, I.D., “Trichoptera (Phryganeida),” in History of Insects, Ed. by A.P. Rasnitsyn and L.J. Quicke (Kluwer Acad. Publ., Dordrecht etc., 2002), pp. 199–220.
Ivanov, V.P., “Ultrastructural Organization of Insect Chemoreceptors,” Trudy Vses. Entomol. O-va 53, 301–333 (1969).
Ivanov, V.P., Sensory Organs of Insects and Other Arthropods (Nauka, Moscow, 2000) [in Russian].
Jacobson, M., Insect Sex Pheromones (Academic Press Inc., New York, 1972; Mir, Moscow, 1976) [in Russian].
Kite, G.C., “The Floral Odor of Arum maculatum,” Biochem. Syst. Ecol. 23, 343–354 (1995).
Kjer, K.M., Blahnik, R.J., and Holzenthal, R.W., “Phylogeny of Caddisflies (Insecta, Trichoptera),” Zool. Scr. 31(1), 83–91 (2002).
Kozlov, M.V., Ivanov, V.D., and Rasnitsyn, A.P., “Lepidoptera (Papilionida),” in History of Insects, Ed. by A.P. Rasnitsyn and L.J. Quicke (Kluwer Acad. Publ., Dordrecht etc., 2002), pp. 220–227.
Kozlov, M.V., Zhu, J., Philipp, P., et al., “Pheromone Specificity in Eriocrania semipurpurella (Stephens) and E. sangii (Wood) (Lepidoptera: Eriocraniidae) Based on Chirality of Semiochemicals,” J. Chem. Ecol. 22, 431–454 (1996).
Kozlov, M.V. and Zvereva, E.L., “A Failed Attempt to Demonstrate Pheromone Communication in Archaic Moth of the Genus Sabatinca Walker (Lepidoptera, Micropterigidae),” Ecol. Letters 2, 215–218 (1999).
Kristensen, N.P., “Studies on the Morphology and Systematics of Primitive Lepidoptera,” Steenstrupia 10, 141–191 (1984).
Kristensen, N.P., “Early Evolution of the Lepidoptera + Trichoptera Lineage: Phylogeny and the Ecological Scenarios,” Mem. Mus. Natn. Hist. Nat. N. S. Zool. 173, 253–271 (1997).
Kristensen, N.P. and Skalski, A.W., “Phylogeny and Paleontology,” in Lepidoptera: Moths and Butterflies. 1 (Handbook of Zoology, Vol. IV, Part 35), Ed. by N.P. Kristensen (De Gruyter, New York, 1999), pp. 7–25.
Liénard, M.A. and Löfstedt, C., “Functional Flexibility as a Prelude to Signal Diversity? Role of a Fatty Acyl Reductase in Moth Pheromone Evolution,” Comm. Integr. Biol. 3(6), 586–588 (2010).
Löfstedt, C., “Evolution of Moth Pheromones,” in Insect Chemical Ecology. Proceedings of a Conference Held in Tebor, 1990, Ed. by I. Herdy (Acad. Prague and SPB Acad. Publ., The Hague, 1991), pp. 57–73.
Löfstedt, C., Hansson, B.S., Petersson, E., et al., “Pheromonal Secretions from Glands on the 5th Abdominal Sternite of Hydropsychid and Rhyacophilid Caddisflies (Trichoptera),” J. Chem. Ecol. 20, 153–170 (1994).
Löfstedt, C., Bergmann, J., Francke, W., et al., “Identification of a Sex Pheromone Produced by Sternal Glands in Females of the Caddisfly Molanna angustata Curtis (Trichoptera, Molannidae),” J. Chem. Ecol. 34(2), 220–228 (2008).
Löfstedt, C. and Kozlov, M., “A Phylogenetic Analysis of Pheromone Communication in Primitive Moths,” in Insect Pheromone Research, Ed. by R.T. Cardé and A.K. Minks (Springer, 1997), pp. 473–489.
Melnitsky, S.I., “Preliminary Data on the Histological Structure of the Sternal Pheromone Glands in Caddisflies,” in Fauna, Ecology, Ethology, and Physiology of Amphibiotic and Aquatic Insects in Russia: Proceedings of VI All-Russia Trichopterological Symposium and I All-Russia Symposium on Amphibiotic and Aquatic Insects, Voronezh, 20–22 May 2000 (Voronezh, 2001), pp. 37–39.
Melnitsky, S.I., “Comparative Morphological Analysis of Abdominal Sternites IV and V in Amphiesmenoptera,” in Fauna, Ecology, Ethology, and Physiology of Amphibiotic and Aquatic Insects in Russia: Proceedings of II All-Russia Symposium on Amphibiotic and Aquatic Insects, Voronezh, 15–17 September 2003 (Voronezh, 2004), pp. 111–118.
Melnitsky, S.I. and Deev, R.V., “The Fine Structure of Sternal Pheromone Glands in Two Caddisfly Species from the Rhyacophilidae and Limnephilidae Families (Insecta: Trichoptera),” Russ. Entomol. J. 18(2), 107–116 (2009).
Melnitsky, S.I. and Ivanov, V.D., “Evolution of the Palpal Receptor Complexes in Amphiesmenoptera,” in Problems of Aquatic Entomology in Russia and Adjacent Countries: Proceedings of IV All-Russia Symposium on Amphibiotic and Aquatic Insects (Vladikavkaz, 2010), pp. 27–33.
Melnitsky, S.I., Ivanov, V.D., and Zueva, L.V., “Pheromone Gland Musculature in Phryganeidae: Structural Features, Postcopulatory Modification and Taxonomic Significance,” in Proceedings of the 13th International Symposium on Trichoptera. BiaŁowieża, Poland, June 22–27, 2009 (Zoosymposia No. 5) (Magnolia Press, 2011), pp. 319–330.
Nasonov, N., A Course of Entomology. Part 1: The Integument (Warsaw, 1901) [in Russian].
Noirot, C., “The Sternal Glands of Termites: Segmental Pattern, Phylogenetic Implications,” Ins. Soc. 42, 321–323 (1995).
Noirot, C. and Quenneedey, A., “Fine Structure of Insect Epidermal Glands,” Annu. Rev. Entomol. 19, 61–80 (1974).
Prather, A., “Revision of the Neotropical Caddisfly Genus Phyloicus (Trichoptera: Calamoceratidae),” Zootaxa 275, 1–214 (2003).
Quennedey, A., “Morphology and Ultrastructure of Termite Defense Glands,” in Defensive Mechanisms in Social Insects, Ed. by H.R. Hermann (Praeger Press, New York, 1984), pp. 151–200.
Quennedey, A., “The Molting Process of Perennial Class 3 Gland Cells during the Postembryonic Development of Two Heterometabolous Insects: Blaberus (Dictyoptera) and Dysdercus (Heteroptera),” Ann. Soc. Entomol. Fr. 27(2), pp. 143–161 (1991).
Quennedey, A., “Insect Epidermal Gland Cells: Ultrastructure and Morphogenesis,” in Microscopic Anatomy of Invertebrates, Vol. 11, Ed. by F.W. Harrison and M. Locke (Wiley-Liss Inc., New York, 1998), pp. 177–207.
Quennedey, A., “Perspectives on Four Decades of Transmission-Electron Microscopy on Insect Exocrine Glands,” Atti Acad. Naz. Ital. Entomol. 48, 85–116 (2000).
Resh, V.H., Jackson, J.K., and Wood, J.R., “Techniques for Demonstrating Sex Pheromones in Trichoptera,” in Proceedings of the 5th International Symposium on Trichoptera, Ed. by M. Bournaud and H. Tachet (Dr. W. Junk, Boston, 1987), pp. 161–164.
Roelofs, W. and Bjostad, L., “Biosynthesis of Lepidopteran Pheromones,” Bioorg. Chem. 12(4), 279–298 (1984).
Skirkevicius, A.V., Pheromone Communication in Insects (Mokslas, Vilnius, 1986) [in Russian].
Skirkevicius, A.V., Pheromones: A Reference Book (Vilnius, 1988) [in Russian].
Solem, J.O., “Swarming and Habitat Segregation in the Family Leptoceridae (Trichoptera),” Norv. J. Entomol. 25, 145–148 (1978).
Solem, J.O. and Petersson, E., “Demonstration of Female Sex Pheromones and Adult Behavior in Molanna angustata (Trichoptera: Molannidae),” Entomol. Gen. 12, 115–118 (1987).
Symonds, M.R.E. and Elgar, M.A., “The Evolution of Pheromone Diversity,” Trends Ecol. Evol. 23(4), 220–228 (2008).
Toth, M., Szocs, G., van Nieukerken, E.J., et al., “Novel Type of Sex Pheromone Structure Identified from Stigmella malella (Stainton) (Lepidoptera: Nepticulidae),” J. Chem. Ecol. 21, 13–27 (1995).
Ulmer, G., “Die Trichopteren des Baltischen Bernsteins,” Beitr. Naturk. Preuss 10, 1–380 (1912).
Wilson, E.O. and Bossert, W.H., “Chemical Communication among Animals,” Rec. Progr. Hormone Res. 19, 673–716 (1963).
Zhu, J., Kozlov, M.V., Philipp, P., et al., “Identification of a Novel Moth Sex Pheromone in Eriocrania cicatricella (Zett.) (Lepidoptera: Eriocraniidae) and Its Phylogenetic Implications,” J. Chem. Ecol. 21, 29–43 (1995).
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Original Russian Text © V.D. Ivanov, S.I. Melnitsky, 2014, published in Entomologicheskoe Obozrenie, 2014, Vol. 93, No. 2, pp. 311–327.
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Ivanov, V.D., Melnitsky, S.I. Questions of molecular evolution of pheromone communication in caddisflies and lower moths (Insecta: Trichoptera, Lepidoptera). Entmol. Rev. 94, 930–942 (2014). https://doi.org/10.1134/S0013873814070021
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DOI: https://doi.org/10.1134/S0013873814070021