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Mating Behavior and Chemical Communication in the Order Hymenoptera

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Mating Behavior and Chemical Communication in the Order Hymenoptera P1: FXY November 15, 2000 11:58 Annual Reviews AR119-02 Annu. Rev. Entomol. 2001. 46:31–78 Copyright c 2001 by Annual Reviews. All rights reserved MATING BEHAVIOR AND CHEMICAL COMMUNICATION IN THE ORDER HYMENOPTERA M. Ayasse,1 R. J. Paxton,2 and J. Tengo¨3 1Institute of Zoology, Department of Evolutionary Biology, University of Vienna, A-1090 Vienna, Austria; e-mail: [email protected] 2Institute of Zoology, University of Tubingen,¨ D-72076 Tubingen,¨ Germany 3Ecological Research Station, Uppsala University, S-38693 Farjestaden,¨ Sweden Key Words sex pheromones, mating strategies, chemistry, behavior, chemical mimicry ■ Abstract Insects of the order Hymenoptera are biologically and economically important members of natural and agro ecosystems and exhibit diverse biologies, mat- ing systems, and sex pheromones. We review what is known of their sex pheromone chemistry and function, paying particular emphasis to the Hymenoptera Aculeata (pri- marily ants, bees, and sphecid and vespid wasps), and provide a framework for the functional classification of their sex pheromones. Sex pheromones often comprise multicomponent blends derived from numerous exocrine tissues, including the cuti- cle. However, very few sex pheromones have been definitively characterized using bioassays, in part because of the behavioral sophistication of many Aculeata. The rel- ative importance of species isolation versus sexual selection in shaping sex pheromone evolution is still unclear. Many species appear to discriminate among mates at the level of individual or kin/colony, and they use antiaphrodisiacs. Some orchids use hymenopteran sex pheromones to dupe males into performing pseudocopulation, with extreme species specificity. CONTENTS Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org PERSPECTIVES AND OVERVIEW .................................. 32 HYMENOPTERAN MATING SYSTEMS .............................. 33 ODOR PRODUCTION AND PERCEPTION ............................. 35 Production .................................................... 35 Perception and Specificity of Pheromones ............................. 36 SEX PHEROMONES: A Taxonomic Compendium ........................ 36 Sawflies ...................................................... 36 Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Parasitica ..................................................... 37 Ants ........................................................ 37 Bees ........................................................ 45 Sphecid Wasps ................................................. 48 Vespid Wasps .................................................. 49 0066-4170/01/0101-0031$14.00 31 P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02 32 AYASSE PAXTON TENGO¨ A FUNCTIONAL CLASSIFICATION OF SEX PHEROMONES .............. 50 Male Attractant ................................................ 51 Female Attractant ............................................... 52 Species Specificity of Signal ....................................... 53 Euglossine Bees as Insect “Peacocks” ................................ 55 Individual Specificity of Sexual Signaling ............................. 56 Signals of Receptivity ............................................ 57 Sexual Mimicry and Deceit ........................................ 59 Sexual Deception in Orchids ....................................... 60 CONCLUSIONS AND FUTURE DIRECTIONS .......................... 62 PERSPECTIVES AND OVERVIEW Sex pheromones are defined as odors, produced by either males or females, that stimulate one or more behavioral reactions in the opposite sex, bringing the sexes together for the purpose of mating (237). Compounds may attract mates from a longer distance and aggregate them near the pheromone-emitting individual(s) (sex attractant pheromones). After the two sexes come together, compounds acting at a close range stimulate so-called courtship behavior (courtship pheromones, aphrodisiacs, and antiaphrodisiacs) and copulation. Within the order Hymenoptera [115,000 described species (283)], there is a tremendously wide spectrum of life strategies, covering almost all types of niches exploited by insects and at all trophic levels. Probably no other insect order shows as much biological diversity as Hymenoptera. Hymenopterans are herbaceous or predacious or live as parasitoids within or on other insects. The plant eaters con- sume one or more types of plant material, from pollen to hardwood. The predators may consume invertebrates or vertebrates. Among the parasitic species, there are brood parasites (cleptoparasites, social parasites) and hyper- and superpara- sitoids (215). Social parasites and cleptoparasites commonly eat host eggs or larvae (183, 288). Most hymenopteran species are solitary, but others live in colonies with advanced social structures (288); the range of social forms is greater within the Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org order Hymenoptera than within any other animal group. Among insects, they are at the zenith of ethological sophistication. Moreover, hymenopterans fulfill im- portant ecosystem functions. They are the primary angiosperm pollinators (bees) and natural predators and parasitoids (ants, aculeate wasps, Parasitica) of other in- sects in many terrestrial biomes, and they have commensurate economic value in playing the same beneficial roles in crop pollination and in the control of harmful insects in agroecosystems. A few hymenopterans (Symphyta) are also agricultural Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. or forestry pests in their own right. Commensurate with their diversity of life histories, numerous sensory modal- ities may be used by hymenopterans as communication channels in bringing the sexes together for mating. Although often seen in conjunction with other sensory modalities, chemical signaling seems to be the most common method employed P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02 SEX PHEROMONES IN THE HYMENOPTERA 33 in sex attraction and recognition in Hymenoptera as well as in other insect orders (138). The study of chemical ecology and chemical communication of insects has developed rapidly in the past 30 years (37, 146). Hymenopteran insects exhibit behavioral complexity and great diversity in their mating behavior and in the chemistry of their exocrine secretions (7, 96, 285). New and more sensitive methods and analytical techniques on one side and intensive collaboration between entomologists and chemists on the other have led to the identification of numerous compounds produced in their exocrine glands. However, in only very few cases has a function in sex attraction been shown for these compounds. Here we review odor communication in conjunction with mating behavior in hymenopteran insects. Because the mating behavior of the taxonomic groups Symphyta (sawflies) and Parasitica has been reviewed very recently (16, 215), we focus on the aculeates, principally the ants, bees, and sphecid and vespid wasps. We have limited our discussion of the evolution of sex pheromones because the functionally active compounds have been identified in only a few species. Nonethe- less, behavioral evidence is accumulating for the role of individual-, kin-, nest- mate-, and caste-specific odors in mediating hymenopteran mate discrimination. Even with these restrictions, this review is far from complete because we have chosen to refer predominantly to recent reports or to review papers. However, we have included a section on mimicry and deceit connected to sex pheromone communication, an area that has received little attention in the past. HYMENOPTERAN MATING SYSTEMS Because hymenopterans are holometabolous, the adult niche may be ecologically separated from environmental and other constraints of larval life. However, the latter will determine the spatial and temporal point of pupation and, accordingly, the distribution of the emergence sites of adults. These circumstances will have a strong influence on the mating system within a species. The diversity of their Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org ecologies means there is also much interspecific variation in the mating systems of the order Hymenoptera. Notwithstanding the obvious interrelationship between male and female mat- ing behaviors, attempts to classify hymenopteran mating systems have usually focused on each sex separately (7, 259). This is understandable because females generally invest more in offspring than do males, and therefore females are the limiting sex, whereas males must compete for mating partners. Many aculeate Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. hymenopteran females construct nests for their offspring (288), and therefore their parental investment relative to that of males is even greater than in other groups of insects. This asymmetry in sexual selection in males versus females (11) is likely to have an important impact on the role of chemical communication in the mating behavior of each sex (205–207). P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02 34 AYASSE PAXTON TENGO¨ Sexual dimorphism is common in hymenopterans, and males are often smaller than females. Although spermatogenesis rarely continues into adult life (131), males have a mating
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