Mating Behavior and Chemical Communication in the Order Hymenoptera

Home , Dasypoda, Diadegma melanium, Harpagoxenus canadensis, Lek mating, Mating plug, Mating system

P1: FXY November 15, 2000 11:58 Annual Reviews AR119-02

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, mating systems, and sex pheromones. We review what is known of their sex pheromone chemistry and function, paying particular emphasis to the Hymenoptera Aculeata (primarily 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 cuticle. However, very few sex pheromones have been definitively characterized using bioassays, in part because of the behavioral sophistication of many Aculeata. The relative 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 consume 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 important ecosystem functions. They are the primary angiosperm pollinators (bees) and natural predators and parasitoids (ants, aculeate wasps, Parasitica) of other insects 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 modalities 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-, nestmate-, 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 mating 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 system in which they can typically mate repeatedly; the eusocial bees (honey bees and stingless bees) and leafcutter ants (genus Atta) represent some bizarre exceptions, in which a male’s genitalia are torn off during copulation, resulting in his death (143, 156, 226). However, the operational sex ratio of these species is thought to be male biased, leading to intense competition among males for mates. Hymenopteran males rarely invest in paternal care of offspring, either directly or via a nutritious spermatophore (cf 176). Nest guarding occurs in a very few species (7), but it seems to be a by-product of mate guarding. It has been reported that the bees Osmia rufa (233, 258) and Bombus terrestris (98) have a mating plug that can be found in the female genital chamber after mating. B. terrestris males may monopolize females to prevent them from remating. The plug’s function in O. rufa is not yet clear. In general, therefore, selection strongly favors those hymenopteran males that maximize their number of mates or their probability of finding a mate, and the hymenopteran males use various tactics to increase their access to receptive females. Following the system of Alcock et al (7), we classify male mate-seeking tactics according to the three principal locations, so-called rendezvous sites, at which males search for and mate with females (Table 1). The distribution in space and time of receptive females and competing males (7, 259) is thought to dictate the rendezvous site used. For example, many hymenopteran males patrol specific emergence sites where receptive females are aggregated (Table 1). When emerging females are dispersed, rendezvous sites are non-resource-based landmarks (e.g. tops of tall trees, hilltops, or along a hedge) or resources visited by females for self-nourishment or for providing for their offspring (e.g. for many oligolectic bees, the flowers from which females collect provisions for offspring) (Table 1). Typically, males engage in a scramble contest for females, though there are examples of male territoriality at all three rendezvous sites (Table 1). Con- siderable intraspecific variability in male mate-seeking behavior can also exist (7), with individual males sometimes using more than one tactic or different members of the male population using different tactics (6). The social organi-

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org zation of a species does not seem to inﬂuence the mate-seeking tactics used by males. Hymenopteran females generally provide considerable parental care; many Aculeata build complex nests in which they provide for offspring (288). Selec- tion is likely to strongly favor females that discriminate among mates, for example, in terms of species identity, genetic complementarity, or quality. Females may discriminate among potential male mates by the sex pheromones that they

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. emit. Despite the paucity of data on mating frequencies of hymenopteran females, single-partner mating (monandry) at or soon after emergence is considered common (see e.g. 100) and is expected whenever mating is costly in terms of time or risk of predation. However, multiple mating by females (polyandry) is P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 35

TABLE 1 Rendezvous sites and male mating behavior for one species each of candidate taxa of the Hymenoptera Male Behavior Rendezvous Site Nonterritorial Territorial

Female Ant: Harpagoxenus Ant: Cardiocondyla emergence sitea sublaevis (60) spp. (132) Overwintering site, Bee: Colletes Bee: Centris Sleeping site aggregation, cunicularius (71) pallida (10) Oviposition site Sphecid wasp: Bembix Sphecid wasp: Philanthus rostrata (231) bicinctus (123) Vespid wasp: Polistes Vespid wasp: Polistes chinensis antennalis fuscatus (210) (157) Resource-based Bee: Andrena Bee: Anthidium (e.g. flowers) florea (284) manicatum (234) Vespid wasp: Masaridae: Pseudomasaris maculifrons (3, 4) Non-resource-based Ant: Pogonomyrmex spp. Bee: Centris adani (114) (e.g. landmark (137) or flyway) Bee: Andrena (252) Sphecid wasp: Sphecid wasp: Eucerceris spp. (108) Philanthus spp. (108) Vespid wasp: Vespid wasp: Polistes gallicus (260) Polistes dominulus (36)

aFor example, nest, nest entrance, general nesting area.

also widespread in hymenopterans, as is female receptivity extending throughout adulthood (see e.g. 86). Numerous potential beneﬁts of polyandry to females, especially for social species, have been hypothesized (52). Monandrous and polyan- drous taxa are known for species using each of the three rendezvous sites (Table 1), Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org and intraspeciﬁc variation in female mating frequency is known to occur in several taxa (52, 198).

ODOR PRODUCTION AND PERCEPTION Production Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Insect pheromones are generally produced by exocrine glands that are modiﬁ- cations of the epidermal cells of the integument; all exocrine glands are associated with the cuticle. In most insects, simple unicellular glands are the source of pheromones (189). In addition, internal aggregates of glandular cells may be P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

36 AYASSE PAXTON TENGO¨

connected to a common reservoir, a situation particularly prevalent in the social hymenopterans (46, 203). The diversity of exocrine glands is greatest among social insects, for which 63 different glands have been described (46). The primary functions of cuticular lipids are the prevention of desiccation and the regulation of cuticular permeability (125), but in many insects they also have a secondary function, acting as sex pheromones (49, 50). There is increasing evidence that, in hymenopterans, sex pheromones are also located on the surface of the cuticle (22, 25, 229).

Perception and Specificity of Pheromones Hymenopteran insects perceive pheromones via olfactory sensilla located in the antennae (230). Many sex pheromones in hymenopteran insects contain dou- ble bonds and/or are chiral. Although many chiral compounds from members of the order Hymenoptera have been identified (51), enantiomeric discrimination at the receptor site is rare. One exception is the bee Andrena wilkella, whose males mark odor spots along their patrol routes with a cephalic gland secretion (253). They were also found to discriminate both behaviorally and electrophysiolog- ically between enantiomers of (E,E )-2,8-dimethyl-1,7-dioxaspiro[5.5]undecane, the major compound in the male cephalic secretion, suggesting great specificity in their sensillum receptors (253).

SEX PHEROMONES: A Taxonomic Compendium

Sawﬂies Symphyta (sawﬂies) is the more ancient of the two hymenopteran suborders, and its members are almost entirely phytophagous. The other suborder, Apocrita, contains all other known hymenopterans. Knowledge about mating systems and sex pheromones within the suborder Symphyta is very limited, with some genera of the family Diprionidae, harmful defoliators of conifers, being exceptions (15, 16). In these latter genera, “female calling,” in which the female advertises her pres-

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org ence and receptivity to males through the production of volatile attractants, is the predominant pheromonal system used to bring the sexes together (16). The pine sawﬂies of the family Diprionidae are well studied (16). The sex pheromones of the species of Diprion, Neodiprion, and related genera are acetates and proprionates of secondary alcohols of 11- to 16-hydrocarbon chain lengths, particularly 3,7-dimethyl-2-pentadecanol (diprionol). Diprionol has three asym- metric centers and therefore eight stereoisomers. All enantiomers have been

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. synthesized (135) and used in electroantennogram (EAG) recording (158), in single-sensillum recording (17, 126), and in ﬁeld bioassays (15). The alcohols are not behaviorally active. The biosynthetic origin of the alcohols is not known, nor is the mode of their esteriﬁcation. Diprionol occurs, and may be produced, in many body parts of a diprionid female (274). Most investigated diprionid species P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 37

rely on a single substance for sex attraction (16). This odor component is the one present in the largest quantity (275).

Parasitica Mating behavior and sex pheromones of the Parasitica have recently been exhaus- tively reviewed (120, 215). Parasitica courtship behavior has also been extensively investigated. Assem and his coworkers present detailed studies of some chalci- doid wasps (e.g. 19, 20), and we recommend their work for a broader coverage. Here we restrict our account to some general characteristics and some patterns that diverge from the other hymenopteran groups. Of special importance for the mating systems of parasitic wasps is the spatial distribution of the hosts. In many species, larvae develop in gregarious clutches. Furthermore, more than one wasp may develop from the same host individual. Parasitica mating systems have been analyzed for a large number of species. However, sexual signaling via pheromones, if it occurs, deserves further attention. Female calling is the dominant system of long-range attraction in members of the suborder Parasitica, whereas chemical signals in connection to courtship may be produced by both sexes (215). Normally, only virgin females release sex pheromones. Monandry seems to be the general rule (155); however, further matings with different partners may occur during the female’s short period of receptivity soon after the first copulation. Male post-copulatory guarding (99) might function to close this window of receptivity for conspecific rivals (e.g. 12, 121, but see 151). A male’s readiness to mate again after copulation varies. Gordh & Hendrickson (122) reported a 1-h refractory period for an ichneumonid wasp. Mating may last from seconds up to several hours, depending on the species. Quicke (215) lists seven Parasitica species for which female-produced sex pheromones have been identified. Four of these species are ichneumonids, two are braconids, and one is a charipid. One compound, (Z )-4-tridecenal, is part of a three-component sex pheromone of the braconid Macrocentrus grandii. It seems to be produced by atmospheric oxidation of diene precursors (251). The site of sex pheromone production by female Parasitica is known in very few cases. As shown by Assem and coworkers, male-female antennal contact is often im- Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org portant in Parasitica courtship. In several parasitic wasps, the male is equipped with antennal sex glands (147, 148). In the scelionid Trissolcus basalis, a proteina- ceous secretion derived from the antennal sex glands is spread over the females’ antennae during mating (47). A female will reject a male that has had these glands experimentally removed.

Ants Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. All 10,000 species of ants in the suborder Aculeata are eusocial, living in matriﬁlial colonies that often comprise tens to millions of workers (more or less sterile females) and are usually headed by one to several queens (143). In addition to, or maybe because of, their complex sociality, ants are also among the most inventive P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

38 AYASSE PAXTON TENGO¨

of chemists. Ants produce a bewildering variety of compounds (143), from a diversity of exocrine glands that exceeds the number of such glands in all other hymenopteran groups (46), many of which function in communication among nestmates. Despite the attention given to the identification of ant semiochemicals and their role in social interactions (264), the identification of their sex pheromones lags far behind (Table 2). Ant gynes (young, unmated queens) and males, the sexually reproductive individuals, are typically produced during a brief period of the year. Though mating in a few species of ants regularly occurs among nestmates inside the nest, when males may be ergatoid (i.e. wingless; see 55, 133), males and females of most ants are usually winged, and one or both sexes fly from their nest to mate (143). In these cases, Hölldobler & Bartz (139) have defined two principal mating systems for ants, the “male-aggregation syndrome” and the “female-calling syndrome.” They correspond to the use of “non-resource-based” and “emergence site” rendezvous sites, respectively (Table 1). Though providing a workable conceptual framework to define mating behavior of ants, the two syndromes are too limited to capture the range of mating behaviors observed in the ants, let alone those of other Aculeata. For both syndromes, pheromones have often been implicated in coordinating the departure of sexuals from a nest and in attraction of mates.

Male-Aggregation Syndrome The sexuals of many species of the genera Camponotus, Lasius, and Pogonomyrmex collect at species-speciﬁc landmarks and at times of the day and year when mating is thought ordinarily to occur. Both sexes ﬂy upwind to groups of males, attracted to the landmark and often to the odor cues of emitting males. The males’ mandibular glands have been implicated as the source of the sex attractant in numerous genera (e.g. Acanthomyops, Calomyrmex, Lasius, and Myrmecocystus; reviewed in 143) and conclusively demonstrated in several Pogonomyrmex species (137). In the latter genus, the dominant component of the gland is 4-methyl-3-heptanone (180; Table 2). However, glandular contents have not been fully chemically characterized, and the components active in mate attraction remain unknown. For some Pheidole species of the southwest- ern United States, gynes gather and attract males (139); the pheromones, if any,

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org used in mate attraction are not identiﬁed. Typically, Pogonomyrmex males are not agonistic at aggregations. When virgin queens are near an aggregation, female-derived pheromones are then assumed to attract mates or to stimulate males [e.g. Pogonomyrmex (137)]. For Formica lugubris, the source of the attractant has been identiﬁed as the gyne’s Dufour’s gland, which contains undecane (90%), (Z )-4-tridecene (4%), and tridecane (4%) (273; Table 2). Synthetic undecane elicits as strong a male response as natural

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Dufour’s gland extract in this species, namely, pouncing on a mate and attempting copulation. Undecane is the only ant semiochemical that has been conclusively demonstrated via a bioassay to function as a sex pheromone. Undecane is also found in the Dufour’s gland secretion of F. lugubris workers and, indeed, of most formicine ants (186) where in other contexts it functions as an alarm pheromone P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 39

(273). This underscores the importance of context for pheromonal function. Un- decane is a common component of the Dufour’s gland of Formica polyctena gynes, in which it has also been hypothesized to function in sexual attraction (171). In the male aggregation syndrome, mating flights of both females and males of species are usually synchronized both within and between colonies (143), and the pheromones released by males at the nest entrance have been implicated in coordinating the departure of sexuals from the colonies’ own nest entrances. For Camponotus herculaneum, experiments with crushed heads have demonstrated that male mandibular glands are the source of the pheromone that induces flight by gynes from the nest (142). Male mandibular gland pheromones are thought to perform the same function in the genera Atta and Acromyrmex (264). Chemical characterization of the male mandibular glands of many Camponotus species has revealed a range of components (Table 2), although in no case has the active component(s) been identified in bioassays.

Female-Calling Syndrome The female-calling syndrome is a mating system typical of many insects (e.g. Lepidoptera; 259, 167, 223). Ant gynes who “call” typically do so from near or within their natal nests to attract males that fly widely in search of mates. Calling females often take up a characteristic position, with gasters raised and stings extruded, suggesting that the venom glands may be the source of a chemical male attractant. Indeed, for Xenomyrmex floridanus, Hölldobler (136) showed that the queen’s venom glands both attracted males and elicited copulatory behavior. The venom gland is also the location of the sex attractant and copulatory releaser in Formicoxenus nitidulus (62). For Leptothorax kutteri and a number of other dulotic leptothoracine ants (Formicoxenus nitidulus, Harpagoxenus spp.), a crushed gyne’s venom gland also attracts males and releases copulatory behavior, although male copulatory behavior of other species is only exhibited following contact with the body of the queen, a worker, or a pupa (61, 63). In the ponerine Megaponera foetens, which has ergatoid (wingless) queens, males are attracted to the chemical trails laid by workers and follow these to their nests in search of mates (58). In the ponerine Rhytidoponera metallica, the source

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org of the pheromone that attracts males is the pygidial gland of the gyne (141), whose contents, in workers, include isogeraniol and m-hydroxybenzaldehyde (182; Table 2). In the ponerines in which workers can mate ( 100 species), the pygidial gland is also a source of male attractant (202). For other∼ species exhibit- ing the female calling syndrome, the source of the pheromone lies elsewhere: the glands associated with the sting apparatus in myrmicine ants, the venom gland in leptothoracine ants, and the Dufour’s gland in Monomorium pharaonis (reviewed

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. in 143). In four leptothoracine ants in which venom gland extract is thought to or has been shown to attract males, the contents of the venom gland have been partially characterized, with 3-methyl-1-(3-methylbutyl)-pyrrolidine being a major constituent of the extract of all (218). However, neither isolated components nor synthetic P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

40 AYASSE PAXTON TENGO¨ 44, 71 + others + tridecene, pyrrolidine , Z-4- 273 related alakaloids tridecane 3-Methyl-1-(3- isogeraniol, m-hydroxybenzaldehyde mellein, octanoic acid, methyl anthranilate Linalool Undecane behavior, ma(e) Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org Female PGFemale MG MaMale MG Ma(e) Male territory markers? Citral, heptanones 51 182 DG Releases male copulatory Male MG Fa and ma? 4-methyl-3 heptanone 180 VG Ma ethylbutyl) 218 Male MG Triggers ﬂight of Methyl 51, 170 . spp ) sexuals from the nest 6-methylsalicylate, + Female and male sex pheromones identiﬁed in different groups of Hymenoptera Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. sublaevis acevorum goeswaldi spp. (10 Rhytidoponera Colletes cunicularius Oxaea Formica lugubris Harpagoxenus Laptothorax L. muscorum Doronomyrmex Pogonomyrmex Camponotus Colletidae Oxaeidae BEES TABLE 2 TaxonANTS Source Function Chemistry Reference(s) P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 41 ) 253, 255 243, 276 Continued 42 257 229 21 45, 54, 252, 31, 32, 25, 242 ( 50 compounds— alcohols, terpenes nerol, geraniol, 1-heptanol, 2-phenyl-ethanol, nerolicacid, geranolic acid alkanes, alkenes acetates, butanoates, spiroketals farnesol, geranial, alcohols, alkanols, aldehydes, acetates lactones, hydrocarbons Alkanes, aldehydes, Neral, geranial, Hexadecyl octadecenoate Lactones Isopentenyl esters, behavior, copulatory behavior, ma(e) antiaphrodisiac (e) markers, ma and fa(e) antiaphrodisiac(e) Ma(e) copulatory Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org thoraces and abdomina, female and male HE Extract of female Ma(e) Female MG Ma(e) Female CC, MGMale MG Releases male Male territory markers Citral, ketones, alcohols, 96, 112, 113 Male cuticle, headFemale head Male-produced Male LG and MG Ma(e) Male territory More than Unknown 278 Female cuticle, DG? Ma(e) Female cuticle, DG Releases male Male-produced Unknown 159 . ssp Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. P. calacaratus Dasypoda altercolor Panurgus banksianus, A. nigroaenea Panurginus L. malachurum Andrena Nomia triangulifera L. zephyrum L. zephyrum L. malachurum Melittidae Andrenidae Halictidae P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

42 AYASSE PAXTON TENGO¨ 185, 265, 267 265, 267, 286 22 22 esters, hexanoic acid lactone all transfarnesal, 3,7,11-methyl 1-2, 7,10 dodcatrienal fatty acids ketones, ethyl myristate, 2-heptanone, hydrocarbons Vanillin, guaiacol Cis-2-methyl-5-hydroxy Hydrocarbons, ethyl ester Hydrocarbons, ethyl copulatory behavior, ma(e) aggressiveness in other males, fa(e) aggressiveness in other males, fa(e) antiaphrodisiac(e) markers, fa(e) laurate, geranyl acetate, 114, 270 copulatory ma(e) behavior, Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org Male MG and THGFemale MG Fa Releases male Ethyl oleate Unknown 178 265a, 265b Male MG, THGFemale MGMale THG Signal-induced Ma(e) Fa(e) Unknown All trans-geranylgeraniol, 18, 185 118, 268 Male MGMale MG Antiaphrodisiac Signal-induced Unknown 114 Male SGFemale IG and CCMale MG and LEG Male-produced Ma(e) Male territory Nerol, neral, geraniol, ethyl Unknown 9, 79, 236 Female MG and CC Releases male ) Continued ( Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. hirsutissima X. micans Bombus terrestris X. varipuncta X. sulcatipes X. sulcatipes Centris Xylocopa O. rufa Eucera palestinae Centris adani Osmia rufa TABLE 2 Taxon Source Function Chemistry Reference(s) Apidae Anthophoridae Megachilidae P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 43 ) Continued

(

222, 239

106, 107

191

219 227

179

102, 103,

116

64, 117, 221,

287

74, 164

39, 40, 43, 96

)-11-Eicosen-1-ol,

esters, ketones and acids

pentadecanal, hexadecanal,

phenylethanol

HOB, 4-hydroxy-3-methoxy

alcohols, acids

tetradecanol, other

acid derivatives

Unknown

Alcohols

9-ODA

9-ODA, 9(R)-and 9-(S)-HDA,

Unknown

Citronellol, geranylcitronellol,

Isoprenoids, fatty

markers, ma, fa

markers, ma, fa(e) farnesol, aldehydes,

markers, fa(e)

Ma(e) Male pheromone

Male territory marker, fa (

Ma(e)

Ma(e) Male territory

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org

cephalic gland

prot G, mesot G, DG

Female cuticle; male Ma(e)

Female cuticule, VG, Ma(e)

Female head

Female MG

Female MG and TG Ma(e)

Male MG

Male LG and HE Male territory

Male LG and MG Male territory

spp. Male MG

(5) Female extract

ssp

spp spp

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only.

Apis sylvestris

Vespa

Vespa crabro

Dolichovespula

Vespula squamosa

6 Philanthus

Scaptotrigona postica

Apis mellifera

Euglossa

Psithyrus

Bombus

Vespinae

SPHECID WASPS VESPID WASPS P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

44 AYASSE PAXTON TENGO¨ 212, 219 262, 279 Unknown Male marking pheromone Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org prot G, mesot G, DG hind leg, Female VGMale SGFemale VG, cuticule,? Ma (e) Ma (e) Male marking pheromone VG Male Unknown marking pheromone Unknown Ma (e) 219 166, 210Ð unknown 263 153 Male SG?Male SG? Male marking pheromone Ma(e) Unknown Unknown 169 168 Abdomen extract, 220, 261, ) -hydroxy benzoate. Bold type indicates components with demonstrated function in biotests. p Continued spp. Male MG, SG, Male marking pheromone Unknown 34, 35, 208, ( Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Polistes Liostenogaster, Eustenogaster labiatus 4 P. fuscatus P. exclamans Parischnogaster Metischnogaster, Belonogaster Mischocyttarus M. ﬂavitarsis Polistinae TABLE 2 Taxon Source Function Chemistry Reference(s) Abbreviations: CC, cuticle; CG,pygidial cephalic gland; gland; SG, DG, sternal Dufour’s gland; gland; TG,decenoic tergal HE, gland; head acid; THG, extract; HOB, thoracic methyl- IG, gland; VG, intersegmental venom gland; gland; LEG, e, leg experimental work; glands; fa, LG, female labial attractant; ma, gland; male MG, attractant; mandibular HDA, gland; 9-hydroxy-2-(E)- PG, P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 45

mixes of venom gland components have been used in bioassays to demonstrate conclusively their function in sex attraction.

Bees Bees are primarily vegetarians, consuming pollen and nectar as larvae. Most species of this aculeate group are solitary, although some have evolved complex eusociality (183). There are several reviews that deal with the glandular systems of bees (13, 81, 134) and the chemistry of exocrine secretions produced by bees (96, 128, 285). Therefore, we do not list all the compounds identiﬁed in various glands, but rather we focus on those systems for which the sex pheromonal function of compounds has been demonstrated by behavioral experiments with odor extracts or with synthetic mixtures of compounds. Sex pheromones of bees may be produced by either males or females, depending on the species’ mating system, and may attract the opposite sex over long and/or short distances. In bees, the mating systems are more complex and diverse than those of the ants (Table 1). Therefore, although we divide bee sex pheromones into those produced by females and males, this does not correspond with their principal mating systems.

Sex Pheromones of Females One of the first identified sex pheromones of insects was the so-called “queen substance” of the honey bee, which is produced in the queens’ mandibular glands (64, 117). Although the whole mandibular gland extract of a queen is highly attractive to drones, 9-keto-(E )-2-decenoic acid (9-ODA) has a key function and is almost as active as the whole blend. The predominant role of this compound was confirmed by EAG analysis (59, 150). Mandibular gland extracts of honey bee queens attract drones from a distance of 60 m when at a congregation site where mating occurs, but drones are also attracted by the queen’s abdominal or tergal gland extracts. Compounds from these glands probably stimulate copulatory behavior in drones after they contact a queen. Further investigations have shown that four other Apis species use 9-ODA as a key substance in the sex pheromone (116). Further examples of sex pheromones that are produced in the female

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org mandibular glands have been found in eusocial stingless bees (105, 107), bumblebees (265a), carpenter bees (118), Andrena spp. (252), and Colletes spp. (71, 128). The role of the female mandibular gland secretion as a sex pheromone has generally been supported by behavioral experiments with natural glandular extracts in all of these cases. However, the importance of particular chemical compounds has rarely been shown. In the stingless bee Scaptotrigona postica, 2-alcohols attracted males from a long distance, but copulatory attempts at a close range were released

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. by males only when 2-ketones, compounds also identiﬁed in queens’ mandibular glands, were added to the artiﬁcial blend of synthetic compounds used in bioassays (106). In the ground-nesting solitary bee Colletes cunicularius, linalool, a major compound in the mandibular glands of females but also present in males, directed P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

46 AYASSE PAXTON TENGO¨

males to emerging, receptive females even before they reached the soil surface (71). Female-derived sex pheromones have also been described in other bees nesting in aggregations (9). A typical chemotactic searching behavior can be observed in males of the social bee Lasioglossum malachurum. Males assemble close to nest entrances where virgin females are expected to appear. Some even inspect entrances of nests containing receptive females. Other males start to clean their antennae with the front legs, a behavior indicating sexual stimulation by the female odor (25). The best studied gland in non-Apis bees is the Dufour’s gland, whose primary function is to line brood cells with a hydrophobic and germicide lining (69, 128, 130). In Lasioglossum zephyrum, Smith et al (243) found that macrocyclic lactones produced in the Dufour’s gland are used as a sex pheromone. However, use of synthetic lactones in bioassays on males only induced pouncing, and no attempts to copulate were recorded. Therefore, other compounds are probably important in stimulating the whole sequence of mating behaviors in males (31, 276). Recently, behavioral experiments with L. malachurum virgin queen extracts have shown that their sex pheromone is localized on the cuticle surface (25). Hydrocarbons were found to have a function as a male attractant; however, copulatory attempts were elicited by isopentenyl esters of unsaturated fatty acids and, to a lesser extent, by unsaturated macrocyclic lactones, both of which were also found in cuticular extracts of gynes. Other findings support the idea that female sex pheromones in many bees are localized on the cuticular surface (22, 276). In the megachilid bee Osmia rufa,extracts of the cuticle surface elicited copulatory behavior in males (22). Saturated and unsaturated fatty acids, ethyl esters, hydrocarbons, and aldehydes, identified by gas chromatography with electroantennographic detection (GC-EAD) and gas chromatography-mass spectrometry (GC-MS), were mixed according to the proportions found on the cuticle surface of unmated females. These mixtures were significantly more attractive to males than dummies impregnated with solvent alone (22). In the solitary bee Andrena nigroaenea, saturated and unsaturated hydrocarbons triggered EAG responses in male antennae. Synthetic copies of these hydrocarbons, blended in the relative proportion found in cuticle extracts, proved

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org to elicit attempts at copulation by males in the ﬁeld (229).

Male-Produced Pheromones In many bees, secretions produced by male mandibular glands or labial glands are used to mark spots along male ﬂight paths. These spots are attractive to females but also to conspeciﬁc males. This was shown for Centris adani, whose males mark grass in their territories to attract females (270). A similar scent-marking behavior was observed in males of the genus Xylo-

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. copa (118, 178). The male mating system of Xylocopa micans varies under different situations. Ethyl oleate is produced in large amounts in the mesosomal glands and mandibular glands of only those males that defend non-resource-based or landmark territories. Therefore, it may act as an attractant and potentially demonstrate male ﬁtness to the females. Males that defend territories at ﬂowers that females P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 47

visit do not need a female attractant. In Xylocopa sulcatipes and Xylocopa hirsutissima, the mandibular gland secretions contained compounds common to both species. However, there was species specificity in their other components. In Xy- locopa sulcatipes, the scent had a dual function: the detection (or recognition) of intruding males and the attraction of conspecific females. The results of bioassays showed that guaiacol was an aggression elicitor, whereas vanillin was attractive to females that visited a male’s territory (118). A function in attraction of mates has also been shown for the mandibular glands of male Andrena bees (252). Males of many Andrena species nonaggressively patrol areas, marking vegetation with mandibular gland secretions that attract other males and also females (252, 254, 255). The mandibular glands of all investigated species showed a species-specific composition of compounds. Behavioral tests with synthetic mandibular gland compounds demonstrated that males are attracted to the scent mark in the patrolled areas. Tengö (252) demonstrated that the whole blend of components in the mandibular gland secretions had the highest behavior- releasing capacity. Interestingly, in almost all of the Andrena species analyzed to date, both sexes produce the same major constituents. When several species simultaneously patrol overlapping flight paths, a species-specific odor mark may help males as well as females to recognize marks of conspecific males. In bumblebees, males patrol flight paths that differ in location within a habitat from species to species (124). During the morning, males mark objects with their labial gland secretions. Other conspecific males are attracted to these scent marks, and flight paths of several males may overlap along some of their courses (116). In the temperate-climate Bombus species, the flight routes generally contain <30 males, but in tropical species like Bombus pullatus, Stiles (246) estimated 460– 720 males per path. Virgin queens are thought to be attracted to the pheromones and land on the marked spots, where copulation is initiated or takes place. It is interesting that most Bombus terrestris queens prefer spots that have been marked by several males (175), suggesting that cooperation between males may enhance the probability of attracting females. For >30 species of bumblebees, labial gland secretions appeared to be species- specific in composition and to be restricted to males (41). Probably interspecific

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org mating is avoided partly because of the species specificity of the signals and partly because the different species of bumblebees occurring in the same habitat tend to establish their flight routes at different heights above the ground (124). A recent study (40) supported the view that labial gland secretions were the source of the scent marking compounds in male bumblebees, a notion already suggested by Kullenberg et al (163). In Bergman and Bergström’s (40) comparative study, mandibular glands of Bombus lapidarius—a species whose males are known to use

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. treetops for patrolling—contain a larger total amount of odor than those of Bom- bus pratorum, a species that exhibits patrolling and marking behavior at ground level. For B. lapidarius, stronger wind and solar radiation at the tops of trees may necessitate larger amounts of scent compounds in order to maintain a signaling effect throughout the day. Furthermore, B. lapidarius males marked leaves with P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

48 AYASSE PAXTON TENGO¨

(Z )-9-hexadecenol and hexadecanol, whereas B. pratorum added compounds of higher volatility, like farnesol, geranylgeraniol, geranyl acetate, and farnesyl acetate, to their marks. A further interpretation of this result by the authors was that B. lapidarius compensates for the lower volatility of the main marking compounds, compared to the more volatile ones of B. pratorum, by using a larger total amount of scent. In megachilid and xylocopine bees and in a sphecid wasp, epidermal odor glands were found in the foreleg basitarsi of males (289). During copulation, the openings of these glands come into close contact with the antennae of the female. Whether pheromones of these males increase the likelihood that the females will mate was not experimentally proven.

Sphecid Wasps The sphecid wasps (Sphecidae) of the suborder Aculeata have been a favored and amenable insect group for ethological research, in part because of the sophisticated nesting behavior of the females (108). Though the mating behavior of sphecids has also been the subject of much study (7, 259), less attention has been paid either to the role of chemical communication in mediating attraction of mates, courtship, and copulation or to the analysis of the exocrine glands and other potential sources of semiochemicals. Sphecid males display a range of mate-seeking tactics (Table 1) and often search for females at their emergence sites. In these cases, females are suspected of releasing attractants to which males are drawn (e.g. Bembix rostrata; 231), although the source and chemical nature of these putative odors are unknown. Mandibular glands are a common source of sex pheromones in the phylogenetically related bees (see above). Head or mandibular gland extracts of relatively few sphecid wasps have been analyzed: Extracts of Sceliphron caementarium were found to be dominated by geranyl acetate and 2-decen-1-o1 (129); those of two Argogorytes species contained 2,5-dimethyl-3-isopentylpyrazine; and those of four Ammophila species had mixes of alkylpyrazines (95), which differed between the sexes in one species. However, the function of cephalic compounds in sphecids is not known.

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org Males of several philanthine wasps (beewolves, Cerceris, Clypeadon, Eucer- ceris, and Philanthus) regularly set up territories at discrete landmarks, such as bushes, and scent-mark their territory with mandibular gland secretions (reviewed in 108). They generally have brushes of hairs on the sides of the clypeus and the underside of the abdomen, which presumably aid in the transfer of glandular exudates to scent marks on plant stems. Major chemical constituents of the mandibular glands of several territorial Philanthus species have been characterized, some of

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. which are sex specific (summarized in 179; Table 2). Though male mandibular gland exudates are prime candidates as sex pheromones that attract females, there has been no definitive demonstration that females are attracted either to glandular extracts or to natural scent marks. GC-EAD analysis may allow identification of semiochemicals, the roles of which could then P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 49

be tested in ﬁeld experiments. However, the behavioral sophistication of sphecids makes it difﬁcult to design a bioassay for sex pheromone function. An alternative function for territorial marks of philanthine males is that they help defend the territory against other males, although males without territories are thought to be attracted to territories of other males and are often thought to set up their own adjacent territories (108).

Vespid Wasps Solitary wasps of the family Vespidae (Aculeata) have received scant attention from chemical ecologists, in contrast to the social vespid wasps, which are known to possess two major categories of pheromones: (a) queen-produced pheromones that attract males and stimulate copulatory behavior and (b ) male-produced perch- and possibly territory-marking pheromones (reviewed in 149, 165). However, not one sex pheromone in the family Vespidae has been chemically characterized. There is also a lack of information about communication by means of sex pheromones in the other lineages of the aculeates not discussed above, such as the chrisidid wasps and their allies.

Female Sex Pheromones In the vespine and polistine wasps, female-produced sex pheromones attract males from a distance and stimulate courtship behaviors such as mounting and attempts to copulate (92, 149, 165). In the southern yellowjacket, Vespula squamosa, attraction of the males by female-produced sex pheromones was demonstrated in a ﬂight tunnel. Males ﬂew upwind in response to caged females and to various body parts of unmated queens. The greatest response was to the thorax (219). Possible sources of the attractant pheromone may be the prothoracic gland and mesothoracic gland, possibly ac- companied by components from the venom gland and Dufour’s gland in the abdomen. Secretions from the venom gland have been shown to attract males and stimulate copulatory behavior in several species of polistine wasps (153, 210, 211, 219). Male members of the genus Polistes respond to a contact pheromone on the female’s

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org cuticle that apparently communicates species identity (211). A similar close-range or contact pheromone that may be involved in the recognition of conspecifics was found in Mischocyttarus flavitarsis (168), Vespa crabro (33), and Vespula maculifrons females (209). Post & Jeanne (211) suggested that the venom gland secretion of Polistes females may be spread over the surface of the body during grooming and act as a sex pheromone. Queens but not workers induced copulatory responses in six Vespa species (191). However, the responses were not species specific. Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only.

Male-Produced Pheromones In many polistine species, males patrol and defend territories and perches in areas visited by females (reviewed in 34). In many species, males mark their perches or other objects with scent by dragging their abdomens P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

50 AYASSE PAXTON TENGO¨

over the substrate, suggesting that sternal glands play a role in pheromone production (210, 220). Dragging of abdominal sterna on territorial perches has been observed in species of Polistes (210, 262, 279), Mischocyttarus (168, 169), and Polybia (280). In polistine species of various genera, glands were found in one or more abdominal sterna of males (reviewed by 92). In other polistine species, exocrine glands were found in the femur, tibia, and tarsi of all three pairs of legs, which suggests that they could be used in marking perches (34). Males of several Polistes species also rub perch sites with their mandibles (220). Facial rubbing may involve the emission of pheromones from enlarged mandibular glands. The only well-characterized male calling behavior in wasps has been observed in Polistes jadwigae (152). Territorial males bend their abdomens while resting in their territories and exposing their distal sternal glands. Two ﬁngerlike projections associated with these glands may aid in dispersing the glandular secretion. Male marking behavior in polistine wasps suggests that male pheromones may serve as a territorial display to ward off other males or as a sex attractant for arriving females; however, there have been no demonstrations of the pheromonal role of male marking by behavioral experiments in the ﬁeld. Evidence of territory marking or of the use of pheromones to attract females is lacking in the Vespinae species studied to date (92).

A FUNCTIONAL CLASSIFICATION OF SEX PHEROMONES

Our compilation of sex pheromones in hymenopterans, in particular the aculeate groups, has demonstrated a potentially great diversity not only in their chemistry, which might be expected given the diversity of their biologies and mate-locating tactics, but also in their function. As a conceptual framework in which to place this diversity of use, we used and further developed Alcock et al’s (7) behavioral classiﬁcation of aculeate male mate-seeking tactics (Table 3). Implicit in this framework is the idea that rendezvous site, male sexual behavior, and sex

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org pheromone use (by both sexes) are all shaped by the density and distribution of receptive females and competing males. Because females are generally the limiting sex, we also envisage that they are likely to assume the less costly role in sexual signaling (11, 205, 206) in terms of time and energy expenditure or ease of detection by predators and parasites. In providing this framework, we aim to bring a functional view of aculeate sex pheromones to the forefront in a ﬁeld of study that has been primarily dominated

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. by the compilation of lists of compounds found in different species. Ideally, the framework will be extended to generate clear and testable predictions of where and when sex pheromones are expected to be found and thereby stimulate further research into their structure, function, and evolution. We highlight some relevant points. P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 51

TABLE 3 Predicted emitter and role of sexual pheromones in relation to rendezvous site and male mating behavior in the aculeate Hymenoptera Male Behavior Rendezvous Site Nonterritorial Territorial

Female emergence sitea Female: in mate Female: in mate attraction Overwintering site, attraction (short (short distance/low Sleeping aggregation, distance/low volatility) Oviposition site volatility) Female: to signal lack of receptivity/ individual recognition Male: as an antiaphrodisiac Resource-based None None (e.g. ﬂowers) Non-resource-based Male: in mate attraction/ Male: in mate attraction/lek (e.g. landmark mating swarm formation formation/individual or ﬂyway) (long distance/high recognition (long volatility) distance/high and Female: in mate attraction low volatility) (long distance/high volatility)

aFor example, nest, nest entrance, general nesting area.

To what extent do the known aculeate examples support our functional classiﬁ- cation of sex pheromones? As we have indicated in our taxonomic compendium, there is a paucity of deﬁnitive data identifying the compound or compounds (if any) used in sex attraction in most hymenopterans. Moreover, taxonomic relationships among many taxa are too poorly resolved to allow a strict, phylogenetically controlled comparative analysis (127) to be made. With these caveats in mind, we draw some generalizations from known examples and highlight interesting avenues for future investigation.

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org Male Attractant When males locate receptive females at emergence or oviposition sites, female- produced odors, when present, are generally used by males as a cue to ﬁnd- ing a mate, a typical mate-attraction system in many insects (e.g. Lepidoptera; 167, 206, 207, 223, 259). This pattern, the “female calling syndrome” of ants (139), is to be expected for both male nonterritorial aculeates and those species in which

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. males establish territories at sites of receptive females (Table 3). Many aculeates appear to ﬁt this pattern (Table 1). Generally, calling female insects produce minute quantities of sex attractant substances (e.g. 206), a pattern consistent with observations of the aculeates. For example, leptothoracine ant queens contain minute (nanogram to picogram) P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

52 AYASSE PAXTON TENGO¨

quantities of attractant when they are the signaling sex (e.g. 218). The faint odor signal requires sensitive, specific odor reception by males. However, in contrast to the well-characterized lepidopterans whose calling females employ high-volatility sex attractants that may function over several kilometers (e.g. 167), aculeate females calling from emergence or oviposition sites often employ relatively low- volatility sex attractants (e.g. hydrocarbons and isopentenyl esters in L. malachurum; 25), which are presumably only detectable over short distances. Why is this? Aculeate males may use other cues, for example habitat features, to locate females over a long distance. In addition, the costs of producing long-distance sex pheromones in terms of the attraction of predators and brood parasites may be great for a female calling close to her nesting or oviposition site. For example, cleptoparasitic Nomada females use host Andrena odor cues to detect host nests (70). Information on whether predators and parasites can detect and use host sex pheromones and over what distances the sex pheromones are actually perceived in the field by both predators/parasites and conspecific males, is sorely needed. The honey bee (Apis mellifera) gyne appears to provide an exception to this pattern because her mandibular glands contain large amounts of sex pheromone (9-ODA) when she is visiting mating sites (>100 µg); 9-ODA can be detected by conspecific males at distances <60 m (116). However, mating sites (drone congregation sites) may be situated several kilometers from a gyne’s colony, and therefore a queen has no risk of attracting brood nest parasites and predators via her sex pheromone (non-resource-based rendezvous site; Table 3). In addition, the high-level 9-ODA production may have more to do with a readiness for later performance, in the nest, because of the important role that it plays in mediating and regulating worker-queen interactions (116).

Female Attractant For species employing non-resource-based rendezvous sites (Table 1), male- produced odors can be expected to act as long-range sex pheromones (Table 3) and have been implicated in sexual attraction in some species. For example, Bom- bus males mark ﬂight routes with scent to attract females, and males may contain

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org substantial quantities of secretion (e.g. microgram quantities of labial gland secretions; 40), suggesting heavy investment in pheromone production. Although it is potentially costly for a hymenopteran female to move toward a signaling male, the potential advantages for her are that she avoids wasting time with non-conspeciﬁc encounters and that she is able to choose her mate (7, 259). When males attract females to a non-resource-based rendezvous site using odors, males may set up territories (Table 1), and the mating system becomes a

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. lek, a defended territory to which females are attracted merely for mating (235). Shelly & Whittier (235) have recently reviewed leking behavior in insects, including all known cases in the order Hymenoptera (essentially some philanthine wasps and xylocopine bees). In these species, male-released odors are assumed to function in territory formation or defense (e.g. Philanthus; 108) or in mate attraction P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 53

(e.g. Xylocopa ﬁmbriata; 269); bioassays are needed to support these suppositions (cf 185). Most hymenopteran males do not form leks at non-resource-based rendezvous sites (Table 1). Rather, they form large aggregations, or they may patrol in large numbers with individual, but overlapping, routes marked by several individuals [e.g. Andrena (252), Bombus (116), the “male aggregation syndrome” of ants (139)]. Agonistic male-male interactions are rare, and males seemingly engage in a scramble competition for females. These latter cases may be more akin to the aerial aggregations or mating swarms of some members of the orders Diptera and Lepidoptera and a few insects in other orders (235, 238). How can we reconcile these observations of apparent cooperative mate signaling by males with an individual selectionist argument? Thornhill & Alcock (259) suggest that a male may parasitize the chemical marks of others. Alternatively, a composite signal of several males may be especially attractive to females and so enhance the absolute number of mates to which each male has access [e.g. Bombus (175) and Andrena (253), but see 235]. When males emit odors that attract receptive females, sexual selection predicts that, over evolutionary time, the male signal will track the response of females (205, 206). The potential also exists for a Fisherian runaway process to act on the male sex pheromone through female choice of male quality (11). In such cases [e.g. numerous bumblebees (Bombus spp.), carpenter bees (Xylocopa spp.), and euglossine bees (Euglossini)], females have been seen to, or are thought to, visit several males before selecting a mate (8, 184, 224). Moreover, the potential for mate choice by females is associated with a rich diversity of male sex pheromonal components, as in the genera Bombus and Andrena (Table 2). Chemical diversity of the pheromonal signal is more consistent with the view that the evolution of male sex pheromones is the result of sexual selection rather than selection for species isolation, although Linn & Roelofs (167) note that complex pheromonal blends may show greater efﬁciency in a chemically “noisy” environment. However, it is not clear what components, if any, of a male-produced sex pheromone are used by aculeate females to detect mates or over what distance they can be detected (but see 185). Electrophysiological and bioassay studies of male-

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org derived sex pheromones are needed to understand the mechanistic basis of female attraction. For example, an interesting avenue of enquiry in bumblebees would be the analysis of interindividual variation in the male labial secretion and its functional significance in mate choice by females. Only then will it be possible to understand the selective pressures shaping a male pheromone signature. Where a resource-based rendezvous site is employed, sex pheromones are unlikely to play a major role in bringing the sexes together (Table 3). Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Species Specificity of Signal It is difficult to define the species specificity of an insect sex pheromone via chemical analysis because many are blends; the relative and absolute concentrations of P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

54 AYASSE PAXTON TENGO¨

individual components of the blend may all play a part in determining the role of an exocrine gland product in mate attraction. Notwithstanding this difficulty, species specificity of sex pheromones was originally considered a natural outcome of character displacement via interspecific interactions; chemical identification of a single component employed by a species in mate attraction probably fostered this view of sex pheromones as species-isolating mechanisms (72, 140), with mu- tually stabilizing selection on signaler and receiver. However, the importance of sexual selection in shaping sex pheromones has since been emphasized, leading to increased understanding of intraspecific diversity in sex pheromone signaling (11, 48, 66, 140, 167, 172, 205, 206, 259, 281, 282). Though not addressing the processes that drive sex pheromone evolution, ex- amination of the patterns of hymenopteran sex pheromone variation, in particular their compositional richness and the extent to which they are species-specific is nonetheless instructive. When thoroughly characterized, hymenopteran female sex pheromones are often found to comprise only one or a few principal components, as in the use of 9-ODA by the honeybee A. mellifera (116) and undecane by the ant F. lugubris (273). However, the simplicity of these two cases may have allowed their ready identification and analysis. Female-derived sex pheromones of Polistes wasps only attract conspecific males (165). However, in other well-characterized hymenopteran cases, there is no apparent species specificity of the female sex pheromone signal. For example, queens of all three sympatric species of honeybee (A. cerana, A. dorsata, and A. florea) in Asia use 9-ODA as the principal male attractant (116). The venom gland contents of European leptothoracine ants attract both conspecific- and heterospecific-males (60). Several species of Vespa queens use the same putative sex pheromone (191). In such cases, a suite of traits such as timing and location of mating flights and visual cues of sexual partners in addition to sex pheromone chemistry might limit heterospecific sexual encounters (e.g. for Apis, see 116). Additional female pheromonal signals that operate at close range [e.g. tergite glands of Apis (222), the cuticle of leptothoracine ants (61)] may also play a role in limiting heterospecific mating (for Pogonomyrmex ants see 137, 139). For putative male sex pheromones of the genus Bombus, a group of bees whose

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org male labial gland chemistry is diverse and varies greatly among species, the composition of the pheromones produced in the labial glands of taxonomically related males is more similar (38), probably owing to the use of common biosynthetic pathways. For Pogonomyrmex ants, whose males attract queens with mandibular gland secretions, males attract heterospeciﬁc queens (137), although little of the chemistry of their sex pheromones is known (180; see Table 2). Heterospeciﬁc mating of Pogonomyrmex ants apparently is avoided because of species differ-

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. ences in the dial periodicity and location of mating ﬂights and in species-speciﬁc cuticular pheromones of the female (137, 139). This circumstantial evidence suggests that in many species hymenopteran female and male sex pheromones do not play a major role in species isolation; other P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 55

cues (e.g. seasonal and diurnal timing and location of mating flights) might play more of a role in this respect. Species specificity in sex pheromones, if it occurs, might be more of an incidental byproduct of (intraspecific) sexual selection on pheromones of individuals (11). Suitable tests of the function of sex pheromones in species isolation will only come from carefully executed and phylogenetically controlled comparative analyses of the active components of sex pheromones of sympatric species with temporally and spatially overlapping rendezvous sites. The diversity of aculeates (e.g. Andrena in northern temperate habitats) would allow such an approach. Identification and synthesis of functional pheromonal components would also allow manipulative experiments in the field to identify the selective pressures and the processes shaping sex pheromone evolution.

Euglossine Bees as Insect “Peacocks” The mating behavior of euglossine bees has been of special interest to chemical ecologists since it was discovered that males collect fragrances from orchids, possibly to use in attraction of mates (287). However, available data from behavioral experiments do not really support this idea. Euglossine males possess speciﬁc perfume-collecting organs on the tibia of the hind legs and are attracted by the scent of orchids that produce the monoterpenes and aromatic compounds (90, 91), from which they acquire these odors. Dodson et al (89) hypothesized that the collected odor itself serves as a sex pheromone in lek formation or to maintain male territories (94); males that had previously collected orchid scent were found to attract other males of the same species (88). Williams & Whitten (287) further suggested that the collected orchid fragrances might be sequestered and internally modiﬁed to produce female sex attractants in the male mandibular glands. It has even been proposed that odors are passed from male to female at mating and that these are subsequently used by the female to repel parasites and predators from her nest (224), in the same way that males of the moth Utheteisa ornatrix transfer defensive pyrrolizidine alkaloids to their mates in ejaculates(101). None of these hypotheses have been supported thus far by bioassays or chemical analyses. Theoretically, euglossine females could be attracted to males based on the com-

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org plexity of their odor bouquets (287), possibly as a measure of the ﬁtnessof a male’s sensory, locomotory, or foraging abilities (174, 259). This “good genes” model of mate selection, or other forms of female choice and intersexual competition among males, would then strongly favor males to collect odors. Certainly, euglossine males seem to be the “chemical peacocks” of the insect world with respect to the rich diversity of components in their odor bouquet, an analogy to the ﬂamboy- ant tail displayed by the male peacock, which is under intense intersexual selection

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. (204). Chemical analyses and behavioral assays that test ideas about female choice based on male odor diversity in euglossine bees are lacking, and the paucity of observations of euglossine copulation suggests that bioassays may be difﬁcult to perform. P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

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Individual Speciﬁcity of Sexual Signaling At close range, it is common for mate detection, selection, and stimulation to involve semiochemicals emitted by one or both sexes (e.g. 48). It has long been considered plausible that sex pheromones of insects, particularly those operating at close range, might carry information on an individual’s identity (170, 253, 259). The interrelationship between individual identity in the context of mating and kin or nestmate identity in social hymenopterans has also been frequently discussed (32, 140, 278). It has been suggested that either male aculeates (e.g. Xylocopa varipuncta; 8) or female aculeates (e.g. L. zephyrum and L. malachurum; 242) or both sexes (e.g. Polistes exclamans; 219) carry individual pheromonal signatures that function in sex attraction. Male signatures of individual identity may allow females to discriminate among potential mates for those species that assemble at non-resource-based rendezvous sites and in which males form leks or engage in courtship (e.g. X. varipuncta; 8), where female choice of mates may be most pronounced (Table 3). Female signatures of identity allow males to discriminate among females they have already encountered and thereby avoid wasting their time in futile mating attempts with unreceptive mates (e.g. 277). However, the chemical basis of individual identity recognition has yet to be worked out for any species.

Inbreeding Avoidance It has also been suggested that individual, kin, or nestmate odor identiﬁcation, used in the context of mate selection, may function to prevent inbreeding (e.g. the Parasitica Bracon hebetor; 190). Males of several hal- ictid bees that mate within or in the vicinity of nesting aggregations avoid nestmate females and preferentially mate with non-nestmates (241, 242, 276, 277). For hymenopterans that mate in the nest, female choice to avoid inbreeding would be expected (55). Several hymenopteran insects that practice intranidal mating appear to show nestmate discrimination in mate selection [e.g. Bombus (111), the ant Iridomyrmex humilis (154), but see 133, 197]. As a corollary, when mating takes place at non-resource-based rendezvous sites and when offspring of many parents gather to mate, risks of inbreeding are likely to be minimal (but see 76), and nest-

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org mate discrimination in mating has not been reported. For species with nestmate or kin discrimination, information on the pheromonal components underlying mate selection is entirely lacking. For the vespid wasps of the genus Polistes, information about the relationship between mate selection and nestmate recognition is conﬂicting (166, 225). Even preferential mating with nestmates (V. maculifrons) has been reported (140). Dif- ferences among studies may arise as laboratory artifacts of experimental design;

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. they serve as a reminder that bioassays in the ﬁeld are necessary to conﬁrm the role of chemical communication in mating. Indeed, as far as mate selection in relation to inbreeding avoidance per se is concerned, there are few good data for any insect (214). P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 57

Single-locus complementary sex determination is widespread in hymenopterans (77); diploid individuals homozygous at the sex locus have very low to zero ﬁtness. There is a theoretical advantage to sex allele signaling and discrimination in mate choice (80, 217), although evidence for it in hymenopterans is equivocal (198).

Signals of Receptivity In many insects, pheromones are important for the regulation of female sexual attractiveness. The decreased attractiveness of females after mating is often due to the presence of a courtship-inhibiting pheromone. It can be male-derived, being transferred from male to female during mating (i.e. antiaphrodisiac; 119), or it may arise owing to cessation of production or alteration of the female sex pheromone after mating. Although the term antiaphrodisiac is sometimes used in the case in which a female alters her sex pheromones after mating to signal that she has mated (232), we use the term for male-contributed repellents only. We note that the two are functionally equivalent. Signaling that she has already mated could directly beneﬁt a female by reducing disturbance from unwanted suitors (259); this may be particularly important when the sexes rendezvous at a nesting/oviposition or resource-based site (Table 3).

Alteration of Female Sex Pheromones After Mating Mating-induced termination of female sex pheromone production has been demonstrated in many insects (181, 216, 228). In bees, receptive females emit a sex pheromone that contains information on age and receptivity (24, 25, 104, 106, 192) and possibly also kin identity (241, 242, 276). Differences in the composition of volatile constituents of virgin and mated females have been shown in several species of bees by chemical analysis (23, 26, 103, 104, 192) as well as by behavioral experiments (25, 104, 277). In the primitively eusocial bee L. malachurum, virgin and nesting (nonreceptive) queens differed clearly in their relative and absolute amounts of cuticular volatiles (25). Virgin gynes produced signiﬁcantly larger total amounts of volatiles than nesting queens. Hydrocarbons were the dominant group of cuticular compounds

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org in both. The relative amounts of isopentenyl esters, key compounds in the sex pheromone, were higher in attractive virgin gynes than in young workers and old breeding queens. The relative proportions of macrocyclic lactones increased after mating. In halictine bees, macrocyclic lactones function to line the wall of brood cells and the nest entrance (128) and to signal size among nest-founding queens (244). In addition, they may be used as a signal to indicate whether a female has mated. Similar results were found in the solitary bees A. nigroaenea and O.

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. rufa. In A. nigroaenea, Farnesyl hexanoate is a major constituent of the Dufour’s gland secretion in mated, breeding females and is used for protective brood cell lining (69). In addition, farnesyl hexanoate inhibits mating behavior of the males (228a). It occurs on the cuticular surface of breeding females and is absent in P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

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virgin females. O. rufa, unmated and mated females showed significantly different odor bouquets, and males were able to discriminate among females on the basis of their matedness within one day after mating (97). In the honeybee (A. mellifera), unmated queens produce significantly less queen mandibular gland pheromone [composed primarily of 9-ODA and four other components, 9(R )- and 9(S )-hydroxy-2-(E )-decenoic acid, methyl-p-hydroxy- benzoate, and 4-hydroxy-3-methoxy phenylethanol; 30, 67, 68, 239, 240] than mated queens. Furthermore, after mating, there is an ontogenetic shift from a high proportion of 9-ODA in unmated queens to almost equal proportions of 9-ODA and 9-hydroxy-2-(E)-decenoic acid in mated queens (192). However, although the total amount of 9-ODA is low in freshly emerged queens, it increases significantly up to the age of 10 days (65), at which time they engage in mating flights. Correspondingly, virgin queens do not attract drones until they are 5 days old, and they elicit a maximum response when they are between 8 and 10 days old (64).

Antiaphrodisiacs Sperm competition is an important selective force that shapes male traits designed to ensure paternity, and a variety of postcopulatory behaviors of male insects have been interpreted in this light (5). Termination of female receptivity after mating is one obvious way in which a male could theoretically enhance or guarantee paternity of his mate’s offspring (259). Antiaphrodisiacs are a means of securing paternity but have rarely been reported in hymenopteran insects. In addition, a male that mates with a female and deposits an antiaphrodisiac on her would beneﬁt by reducing her disturbance by other males, thus increasing his number of offspring. Again, this effect is likely to be most pronounced where the rendezvous is a nesting/oviposition or resource-based site (Table 3). Earlier work suggested that males of the bees C. adani (114) and L. zephyrum (159) deposit a pheromone on females during mating that other males perceive, causing males to avoid mating with the marked females. However, subsequent work failed to demonstrate male-produced antiaphrodisiacs in L. zephyrum (276, 277), suggesting instead that males rapidly habituate to odors of individual females that they have previously encountered and so avoid wasting time in

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org courtship attempts with unreceptive mates (many female bees are thought to mate just once; 100). Chemical characterization of the putative individual odor identi- ﬁers has not been performed. Cuticular compounds play an important role as both courtship stimulants and antiaphrodisiacs in the genus Drosophila (75, 109), other dipterans (73), and hymenopterans. In the bee L. malachurum, odor released by males during mating has an inhibitory effect on the copulatory behavior of conspeciﬁc males (21).

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Signiﬁcant amounts of hexadecyl octadecenoate, the major cuticular compound (wax-type ester), were released during copulation, which possibly provides con- speciﬁc males with information about a female’s mating status (and thereby her lack of receptivity) and ensures his paternity of her offspring. P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 59

In the bee O. rufa, males show a characteristic postcopulatory behavior in which they rub the female wing surfaces with their sternites (233). In doing so, males appear to mark females with an antiaphrodisiac produced in their sternal glands (22). Solvent extracts of wings obtained from freshly mated females showed an increase in the total amount of odor compared to that of unmated females, and many of the dominant chemical compounds identified in the male sternal glands contributed to this increase. In a dual-choice experiment, unmated females impregnated with sternal gland extracts proved significantly less attractive than females impregnated with solvent alone (22). In GC-EAD analyses with sternal gland extracts and further bioassays, (Z )-7-ethyl hexadecenoate has been demonstrated to be the antiaphrodisiac; it is the first male antiaphrodisiac from bees that has been chemically defined (M Ayasse, G Dutzler, F Schiestl, F Ibarra & W Francke, unpublished data). Receptivity signals, whether male derived or female produced, are probably more widespread in hymenopteran insects than has hitherto been documented and deserve further attention. They may complement other forms of signaling by females regarding their lack of receptivity (e.g. acoustic cues by Pogonomyrmex gynes; 177).

Sexual Mimicry and Deceit In some hymenopteran species, alternative mating strategies involving deception are employed by males to secure mating or fertilization success. In the polygynous parasitic wasp Cotesia rubercula, competition for mates is intense; most females mate once, yet there is a short time after copulation in which a second male may induce a female to copulate again (110). To distract rival males and ensure greater paternity success, a male that has just mated will mimic a female and attract conspeciﬁc males long enough for the mated female to become unreceptive. Field & Keller (110) suggest that contamination of the mimicking male with sex pheromones of his mate may act in concert with visual cues to distract rival males. Mimicry of the female by the male is, in this case, a postcopulatory mate-guarding mechanism (5). In army ants (Eciton spp.), males have to enter a colony to access the gyne,

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org and therefore workers can potentially choose the male that will inseminate the gyne. Males are queenlike in shape and morphology and have exocrine glands of a form and location similar to those of queens. These glands do not occur in workers (115). Besides these examples of intraspeciﬁc sexual mimicry and deceit, interspeciﬁc chemical mimicry may be important in enabling females of several cleptoparasitic bees of the genus Nomada to gain access to nests of females of their host genus

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. Andrena (256). Unmated Nomada females do not produce host compounds; rather, Nomada males produce host-speciﬁc chemicals in their mandibular glands that they may spray onto females during mating, allowing females ready access to host nests. P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

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Sexual Deception in Orchids Interspecific sex pheromone mimicry has been developed to an extreme degree by many so-called sexual deceit orchids to ensure their pollination by naive male hymenopterans (82, 84, 85, 87, 188, 250, 271). Their flowers mimic females of their pollinators in shape, color, and odor, and thereby attract males for pollination. Such reproductive mimicry has been termed Pouyannian mimicry (193), because Pouyanne was the first to describe the behavior of Campsoscolia cili- ata (Scoliidae) and Andrena males on Ophrys flowers as a “pseudocopulation” (78, 213). Pseudocopulation was subsequently studied intensively by Kullenberg (160), who postulated that Ophrys flowers mimic the odor of hymenopteran (and other insect) females to dupe males into visiting their flowers, thereby pollinating them (“chemical mimicry”). Pollination by sexual deception is exclusive to the Orchidaceae (1, 83, 188) and can be found in Australia (199), South America (265), South Africa (245), and the Mediterranean basin (160, 162, 195). Because the orchid genera involved are unrelated, it can be assumed that there is a polyphyletic origin to this pollination syndrome (14, 29, 93). Pollination by deceptive sexual attraction involves mostly male aculeate hymenopterans but also males of some sawflies, dipterans, and scarabaeid beetles (85, 195, 250). None of the pseudocopulatory species are known to offer a nutritious reward for the male insect that visits their flowers. Olfactory stimuli appear to be crucial for the attraction of pollinators in the European genus Ophrys (160) as well as in southern Australian species (85, 200), and they elicit innate sexual behavior in male pollinators. Pollinator relationships in sexually deceptive orchids were found to be highly species-specific. Numerous behavioral tests have shown that many European Ophrys species are visited and pollinated by males of only one or a few pollinator species (160, 194–196). Similar species specificity is seen in the Australian orchid genera Caladenia (249) and Chiloglottis (57) and their pollinators. Be- cause many orchids are interfertile, the species-specific attraction of pollinators is important in maintaining reproductive isolation.

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org As a possible consequence of the extreme species specificity of the plant- pollinator interaction, the rate of pollination in sexually deceptive orchids is usually low (27, 187). A further reason for low rates of pollination may be learning and habituation of male pollinators to unrewarding flowers, discouraging their further visits. However, sexually deceptive orchids appear to have evolved strategies that function to optimize the number of pollination events and therefore the number of seeds produced. Ophrys sphegodes plants were found to exploit the learning capabilities of their male pollinators to increase their reproductive success: By Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. behavioral experiments and chemical analyses, it was shown that variation in the odor bouquets of individual flowers within an inflorescence raises the chance of more than one flower being visited by the same male, thereby increasing the plant’s rate of pollination (28). P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 61

Sexual Mimicry in Australian Orchids In Australia, more than 150 species of orchids representing 10 genera attract male pollinators by sexual deception (199). Seventy species of orchids in the genera Arthrochilus, Caladenia, Chiloglottis, Drakaea, Spiculaea, and Paracaleana are pollinated by male thynnine wasps (Tiphiidae: Subfamily Thynninae) (249). Various wasps (Ichneumonidae and Scoliidae) pollinate Cryptostylis and Calochilus species, sawflies pollinate Caleana species (249), and male ants pollinate Leporella species (199, 201). In Australian as well as other orchids, the flower labellum of many sexually deceptive species mimics the color of the female body of their pollinating insect (160, 247, 248, 272). This mimicry varies between species, ranging from being barely recognizable in the genus Caladenia to being remarkably insect-like in some species of the genus Chiloglottis (56). The speculum may show ultraviolet reflection, but ultraviolet reflection is absent in southern Australian species of pseudocopulatory orchids pollinated by tiphiid wasps (85). However, in Australian orchids as well as in European Ophrys species, odor is the most important factor in attracting pollinators and stimulating copulatory behavior. In the genus Caladenia, these odors are emitted by glands on the orchid labellum or the tips of the petals and/or sepals (249), and the pollinating wasps are attracted to these areas. The chemical structure of the pollinator-attracting scent has not been identified so far in any species.

Sexual Mimicry in Ophrys Orchids Orchids of the genus Ophrys grow principally around the Mediterranean, and their pollinators are mostly bees (Andrenidae, Anthophoridae, Colletidae, Megachilidae, and Apidae). Sphecid and scoliid wasps and beetles (Elateridae and Scarabaeidae) are also sometimes pollinators of these orchids (53, 160, 195). Male insects are lured to the orchid flower by visual cues and volatile semiochemicals. At close range, chemical signals from flowers elicit copulatory behavior in males, who try to copulate with the flower labellum. In so doing, the male touches the gymnostemium and the pollinia may become attached to his head or, in some species, to the tip of his abdomen. Through his pseudocopulation with another flower, pollinia may be transferred to that flower’s stigmatic surface, and pollination ensues.

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org In addition to the selective attraction of pollinators via odors, the location of where the pollinia are attached to the male provides a mechanical component to the isolating mechanism between orchid species. Flowers of O. sphegodes and Ophrys fusca are both pollinated by A. nigroaenea males. However, although the pollinia are deposited on the head of the male O. sphegodes bee, O. fusca males reverse into a ﬂower and receive pollinia on the tip of the abdomen. Thereby an effective mechanical isolating mechanism between species is achieved and loss of

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. pollinia to heterospecific orchids is minimized. Intensive study of many Ophrys species has been conducted by Kullenberg and his coworkers (2, 53, 54, 160–162, 252). Through chemical analysis, it was found that Ophrys flowers produce complex species-specific mixtures of more than 100 compounds (53), mainly saturated and unsaturated hydrocarbons, aldehydes, P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

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alcohols, esters, ketones, and terpenoids; aromatic compounds are present in mi- nor amounts. Ophrys species mimic sex pheromones of their pollinators. Floral fragrances produced by flowers contained chemical compounds identical to those of the pheromonal secretions of the respective female insects. Behavioral experiments with synthetic compounds demonstrated that compounds identified only in insect glandular secretions had a greater ability to attract males than volatiles identified in flowers. Borg-Karlson (53) therefore concluded that Ophrys flowers produce a set of “second class attractivity compounds” that successfully attract only a certain fraction of the male population that, at that particular moment, has a low threshold for sexual attraction. The finding that O. sphegodes flowers produce the same compounds as the sex pheromone of females of their pollinators, A. nigroaenea (229), in similar relative proportions, argues against this idea. Saturated and unsaturated hydrocarbons (C21–C29) triggered EAG responses in male antennae, and synthetic copies of these hydrocarbons, blended in the relative proportions found in the odor samples of females and the orchid flower, elicited attempts at copulation in males (229).

CONCLUSIONS AND FUTURE DIRECTIONS

Insects of the order Hymenoptera show great diversity in their mating strategies, with corresponding variation in sex pheromone production [e.g. who emits, from which glandular source(s)], and sometimes there is great complexity in the chemical compounds that appear to be involved in mate attraction. Sex pheromones are one among many cues used by hymenopteran insects to locate suitable, receptive mates. For a variety of reasons, however, few aculeate sex pheromones have been identified. 1. Because glandular exudates often comprise complex mixes (96, 285), identification of the active components in the exudates has proven difficult. Recent studies have demonstrated the power of the GC-EAD technique, which allows extremely sensitive and selective detection of potentially active pheromone components, even within a complex multicomponent sample. We strongly urge further use of GC-EAD. Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org 2. Many of the compounds present in glandular extracts are not commercially available, so they have to be synthesized for use in behavioral tests. Most such syntheses yield racemic mixtures that, because hymenopteran insects often discriminate between the components of these mixtures (e.g. 253), require further, difficult separation into their respective enantiomers. As a consequence, the functionally active components of sex pheromonal blends are rarely known in this group of insects. Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. 3. Even when a role for an exocrine product in sex attraction has been demonstrated and chemical analysis of the product has been achieved, researchers have not always gone on to test the synthetic components of the product in bioassays. In part, this may be because of difficulties in P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

SEX PHEROMONES IN THE HYMENOPTERA 63

designing adequate bioassays in the ﬁeld for the behaviorally sophisticated hymenopterans. Yet bioassays are the only clear means of conclusively demonstrating the function of a sex pheromone. Much headway will be made in the study of hymenopteran sex pheromones through the development of appropriate bioassays. A recent good example that utilizes the approach we advocate is the work by Schiestl et al (229), in which the importance of cuticular hydrocarbons in and renid bee mate attraction has been highlighted.

Hölldobler & Bartz’s (139) classification of ant mating systems into female calling (female-produced sex pheromones) and male aggregation (male-derived sex pheromones) syndromes can be used to describe many hymenopterans. Other aculeates, however, show greater diversity in their mating systems and their apparent use of sex pheromones therein. With the caveat that the sex pheromones of few species have been thoroughly identified, it appears that females emit short-range sex attractants when the rendezvous site is close to the site of nesting and males emit long-range sex attractants when the rendezvous site is distant from the nest and non-resource-based. For species that use a more distant site and where males are nonterritorial, females may also emit a long-distance sex attractant. Future research should aim to identify the sex pheromones of sympatric hymenopteran species with different mating strategies, preferably within a genus or tribe. Such studies will reveal whether there is a correlation between the mating strategy of a species, the physical chemistry (e.g. volatility) of its sex pheromones, and the importance of phylogeny and ecology in shaping the sex pheromone signature. They will also help reveal whether sexual selection provides a more sat- isfactory explanation for hymenopteran sex pheromone evolution than a species isolationist explanation. Sociality appears to have little or no bearing on the role of pheromones in mating, although sex pheromones may be used by a queen in different contexts, for example, in queen-worker communication inside the colony. For known sex pheromones, generally only the attractant function has been identified. Research should therefore also concentrate on finding those compounds that trigger other aspects of mating behavior, such as copulation. Even in the

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org well-studied honeybee (A. mellifera), few of the compounds that elicit copulatory behavior in males have been identiﬁed (cf 222). Our knowledge of the genetics and physiology of sex pheromone production and perception in other insect orders has advanced greatly, particularly in the Lepidoptera (e.g. 172, 173), in part because of the ease with which these insects can be reared in the laboratory. This is generally not feasible for the majority of aculeate hymenopterans. However, their behavioral sophistication and diversity

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. of mating systems offer other opportunities. Aculeate hymenopterans provide candidate model systems for the analysis of sexual selection, in particular via female choice, mate discrimination on the basis of individual or kin identity, and suppressers of sexual signaling (e.g. antiaphrodisiacs). In all of these areas, sig- niﬁcant advances will be brought about through an understanding of the chemical P1: FXY November 6, 2000 12:13 Annual Reviews AR119-02

64 AYASSE PAXTON TENGO¨

basis of sexual signaling. For example, males of euglossine and some xylocopine bees form leks and attract females, apparently using pheromones (185). Moreover, females of these bees and bumblebees are attracted to males and have been hypothesized to select them by the complexity of their odor bouquets (e.g. 259), yet there are no data available on male pheromones used to choose mates. Chemical and electrophysiological analyses are sorely needed here and elsewhere; identiﬁ- cation of the functional components of pheromonal blends should form the basis of bioassays and reveal the importance of intraspeciﬁc variation in pheromone signaling for a suite of evolutionary hypotheses.

ACKNOWLEDGMENTS We thank O Anderbrant, M Blum, J Cane, W Engels, W Francke, J Heinze, F Ibarra, H Paulus, and F Schiestl for providing critical comments on the manuscript. We further gratefully acknowledge the help of C Wirkner and E Zellinger in its preparation.

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CONTENTS

BIOGEOGRAPHY AND COMMUNITY STRUCTURE OF NORTH AMERICAN SEED-HARVESTER ANTS, Robert A. Johnson 1 MATING BEHAVIOR AND CHEMICAL COMMUNICATION IN THE ORDER HYMENOPTERA, M. Ayasse, R. J. Paxton, J. Tengö 31

INSECT BIODEMOGRAPHY, James R. Carey 79

PREDICTING ST. LOUIS ENCEPHALITIS VIRUS EPIDEMICS: Lessons from Recent, and Not So Recent, Outbreaks, Jonathan F. Day 111 EVOLUTION OF EXCLUSIVE PATERNAL CARE IN ARTHOPODS, Douglas W. Tallamy 139 MATING STRATEGIES AND SPERMIOGENESIS IN IXODID TICKS, Anthony E. Kiszewski, Franz-Rainer Matuschka, Andrew Spielman 167

GENETIC AND PHYSICAL MAPPING IN MOSQUITOES: Molecular Approaches, David W. Severson, Susan E. Brown, Dennis L. Knudson 183 INSECT ACID-BASE PHYSIOLOGY, Jon F. Harrison 221 EVOLUTION AND BEHAVIORAL ECOLOGY OF HETERONOMOUS APHELINID PARASITOIDS, Martha S. Hunter, James B. Woolley 251

SPECIES TRAITS AND ENVIRONMENTAL CONSTRAINTS: Entomological Research and the History of Ecological Theory, Bernhard Statzner, Alan G. Hildrew, Vincent H. Resh 291

Genetic Transformation Systems in Insects, Peter W. Atkinson, Alexandra C. Pinkerton, David A. O'Brochta 317

TESTS OF REPRODUCTIVE-SKEW MODELS IN SOCIAL INSECTS,

Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org H. Kern Reeve, Laurent Keller 347 BIOLOGY AND MANAGEMENT OF GRAPE PHYLLOXERA, Jeffrey Granett, M. Andrew Walker, Laszlo Kocsis, Amir D. Omer 387

MODELS OF DIVISION OF LABOR IN SOCIAL INSECTS, Samuel N. Beshers, Jennifer H. Fewell 413

Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only. POPULATION GENOMICS: Genome-Wide Sampling of Insect Populations, William C. Black IV, Charles F. Baer, Michael F. Antolin, Nancy M. DuTeau 441

THE EVOLUTION OF COLOR VISION IN INSECTS, Adriana D. Briscoe, Lars Chittka 471

METHODS FOR MARKING INSECTS: Current Techniques and Future Prospects, James R. Hagler, Charles G. Jackson 511

RESISTANCE OF DROSOPHILA TO TOXINS, Thomas G. Wilson 545 CHEMICAL ECOLOGY AND SOCIAL PARASITISM IN ANTS, A. Lenoir, P. D'Ettorre, C. Errard, A. Hefetz 573 COLONY DISPERSAL AND THE EVOLUTION OF QUEEN MORPHOLOGY IN SOCIAL HYMENOPTERA, Christian Peeters, Fuminori Ito 601

JOINING AND AVOIDANCE BEHAVIOR IN NONSOCIAL INSECTS, Ronald J. Prokopy, Bernard D. Roitberg 631

BIOLOGICAL CONTROL OF LOCUSTS AND GRASSHOPPERS, C. J. Lomer, R. P. Bateman, D. L. Johnson, J. Langewald, M. Thomas 667

NEURAL LIMITATIONS IN PHYTOPHAGOUS INSECTS: Implications for Diet Breadth and Evolution of Host Affiliation, E. A. Bernays 703

FOOD WEBS IN PHYTOTELMATA: ""Bottom-Up"" and ""Top- Down"" Explanations for Community Structure, R. L. Kitching 729 Annu. Rev. Entomol. 2001.46:31-78. Downloaded from www.annualreviews.org Access provided by Chinese Academy of Agricultural Sciences (Agricultural Information Institute) on 04/27/17. For personal use only.