27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ 10.1146/annurev.ento.51.110104.151058

Annu. Rev. Entomol. 2006. 51:413–40 doi: 10.1146/annurev.ento.51.110104.151058 Copyright c 2006 by Annual Reviews. All rights reserved First published online as a Review in Advance on September 21, 2005

MATING SYSTEMS OF BLOOD-FEEDING

Boaz Yuval Department of Entomology, Hebrew University of Jerusalem, Rehovot 76100, Israel; email: [email protected]

KeyWords Diptera, sexual behavior, swarm, female choice ■ Abstract The of each species is a unique, dynamic suite of inter- actions between the sexes. In this review I describe these interactions in the families of flies that contain blood-feeding species. A transition from the aerial swarm, with rapid copulae and no direct female choice, to substrate-based systems with lengthy copulae and opportunities for female choice is evident at both a phylogenetic scale and within nematoceran families under specific ecological conditions. Female monogamy is associated with the former, polyandry with the latter. I suggest that the intensity of sexual selection operating on males in systems where the probability of mating is low has favored male ability to control female receptivity. Reproductive success of males is universally correlated to successful foraging for sugar or blood and (in some species and ecological conditions) to body size. Understanding the ecological basis of the mating systems of these flies will help formulate integrative, sustainable, and biologically lucid approaches for their control.

INTRODUCTION

Every species of sexually reproducing organism manifests a unique mating sys- tem. Each such system is a species-specific work in progress molded by sexual selection acting on the differential mating success of individuals in the population and characterized by patterns of female receptivity, gametic and parental invest- ment, and the distribution, in time and space, of both sexes (45, 136, 150). The evolutionary history of each species constrains, to a great extent, the repertoire of Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org morphological, behavioral, and physiological adaptations that can be employed

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. in the interactions between the sexes. Furthermore, the ecological conditions that prevail in the ’s habitat, particularly the distribution patterns of reproductive resources, contribute enormously to the final shape or type of the mating system. While each species mating system is unique, these systems may be conveniently grouped into categories primarily on the basis of their ecological or behavioral attributes (45, 150). The Diptera, or true flies, are an ecologically diverse order comprising more than 150,000 species (163, 167). The modification of the mouthparts to enable sugar ingestion may have been a key adaptation that preceded the explosive radi- ation of this order, most of whose members still maintain the sugar-feeding habit 0066-4170/06/0107-0413$20.00 413 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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(42). Within the Diptera, blood feeding has evolved at least five times. This event occurred at least twice in the lower flies (the Nematocera) (121), namely in the Culicimorpha (four families with blood-feeding species) and Psychodomorpha (one blood-feeding family); once in the brachyceran Tabanomorpha (two families with blood-feeding species); and twice in the higher Calypteratae—one blood- feeding family in the Muscoidea and four such families in the Hippoboscoidea (85, 156). Twoevolutionary pathways have been suggested for the evolution of blood feeding, each based on a powerful preadaptation. In the first, mouthparts became specialized for piercing plants or prey and then could quite easily be brought to bear on a vertebrate host. Alternatively, a life-history adaptation that entailed seeking the proximity of the host’s nest, burrow, fur, or hair led to an intimate ecological association that culminated in blood feeding (156). In this review I take a close look at the mating systems of the various groups of blood-feeding flies. I attempt to identify the key life-history characteristics and ecological conditions that are the primary factors shaping and maintaining the mating systems of these . While less concerned with precisely naming each particular mating system, I seek common threads and unique features by focusing on the sequence of behavioral events leading to the fertilization of the female’s eggs. Thus, mainly at the family level, I address the attributes of encounter site, courtship, female choice, copula duration, sperm storage, and female remating. In addition, where such information is available, I identify correlates to male reproductive success. I show how all dipteran mating systems stem from mass mating swarms at emergence sites and document a transition from the aerial swarm, with rapid copulae and no direct female choice, to substrate-based systems with lengthy copulae and opportunities for female choice. I suggest that mating systems based on the vertebrate host have evolved in species or groups of species in which contact with the host is prolonged beyond the time necessary for imbibing blood, and attempt to identify the factors that promote host-based encounters in species with brief host contacts.

CULICIMORPHA Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. There are four families in this group of primitive flies that contain blood-feeding species: the Ceratopogonidae, Simuliidae, Culicidae, and Corethrellidae. Only females are blood-feeders, whereas both males and females ingest sugar. The basic mating system in this group, and probably the basal mating system of all Diptera (41), is the polygynous mating swarm. Swarm mating systems have been described for many species and a number of excellent reviews exist (39, 138, 146). The polygynous mating swarm, which consists of males swarming over markers near emergence sites, is the typical mating system of aquatic insects with synchronized emergence (136). In addition to the Nematocera, this includes the relatively primitive Ephemeroptera (4, 60) and the Trichoptera, another modern 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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panorpid order (123). Indeed, to understand their behavior, it may be convenient to look at the Culicimorpha as long-lived mayflies with short larval stages. There are some recurrent and salient fixtures of all nematoceran swarms that suggest a common ancestry: 1. Swarm sites: Swarm sites are species specific, in time and space. 2. Male behavior: Males form and remain in the swarm in response to a visually detected swarm marker. Most commonly, swarming males maintain position in the swarm in response to swarm markers, not to other swarming males. The strength of the swarm-inducing stimulus determines swarm size. 3. Female behavior: Sexually receptive females respond to the same visual markers that release male-swarming behavior and copulate within seconds of entering a swarm. Female mate choice is usually indirect due to the short time they spend in the swarm before and to the heavily male- skewed operational sex ratio. As described below, several other mating systems have evolved from the swarm. On the timescale from emergence to female blood feeding, these systems involve either advancing or postponing the time of mating. In the former, males find recep- tive females either by guarding pupae or patrolling emergence sites. In the latter, swarms have moved from an inanimate marker to one containing a resource, such as carbohydrates or blood meal hosts. From swarming above or near the host, it is but a short step to initiate copulation on the host. Mating at resting sites is also found in some species and may have evolved when reproductive resources are randomly distributed, with predation exerting a significant pressure on swarming insects.

Simuliidae Simuliid black flies (of which there are approximately 1200 species) mate primarily in full daylight in marker swarms (39, 162), although in some species males may await females on vegetation or flowers (162). Massive swarms that may number thousands of individuals form downwind of prominent visual markers (64). As in other swarming flies, the presence of numerous visual markers, such as branches Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org and bushes abutting a river or stream, has the effect of breaking up the swarming

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. population into many smaller swarms consisting of fewer than 10 individuals (162). In several species, males swarm near the vertebrate host and mating occurs as females approach to feed (39, 97, 162). This behavior can be host specific, as in the case of Simulium euryadmiculum,inwhich males are attracted to the uropygial gland excretions of the common loon, the host preferred by females (97). In species such as Simulium ornatum and S. erythrocephalum,inwhich the females partition the host and feed on the navel or ears, respectively, of cattle, males follow suit and copulation occurs near these feeding sites (162). Unlike the other families in the Culicimorpha, the antennal auditory organs are not developed in the Simuliidae and recognition of females is not based on auditory 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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stimuli (39). However, males have high visual acuity due to enlarged holoptic eyes and respond in flight to fast-moving objects (be they females or predators) ap- proaching the swarm. When a female enters a swarm she is chased, and copulation is attempted on the wing. Although courtship is absent, females apparently dis- criminate between con- and heterospecific males and may even exercise some degree of choice whether to copulate with a conspecific male (162). Whether these abilities reflect the presence of a contact pheromone or a rapidly acting system of genital recognition is unknown. Copulations last for less than a minute, during which a spermatophore contain- ing about 4000 sperm is transferred to the female (94). The spermatophore releases its contents to the single spermatheca within an hour after copulation and disap- pears within 24 h (162). Multiple mating is apparently rare. Females containing more than one spermatophore are seldom encountered in the field, and chromo- somal analysis of offspring of individual Similium damnosum females captured in the field indicated that approximately only 5% of females had mated multiply (17).

Ceratopogonidae The females of most species in this family are predaceous; others are phytophagous, parasitic, or cannibalistic upon males. The minority of species (∼1100), grouped in four genera and known as the biting midges, are blood-feeders. In most of the predatory species, females prey on the mating swarms of other nematoceran or mayfly species and visit conspecific swarms for copulations. In a number of species females occasionally cut travel costs and practice sexual cannibalism, consuming conspecific males while in copula (40). The primary mating encounter sites of the blood-feeding species are species-specific, rather inconspicuous crepuscular swarms formed by males over a contrasting feature of the habitat such as a bush, intersecting paths, or even a modest cow pat (16, 25, 38, 179). In some of these species, swarms may occasionally form near or above the vertebrate host (54, 76). Females approaching swarms or hosts are recognized by their wing beat frequency, registered on the erectile hairs and Johnston’s organ at the base of the plumose antennae of males, which function in concert as highly sensitive auditory organs Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org (15). They are rapidly intercepted, and the copulating pairs tumble out of the swarm

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. to the ground, where copulation terminates after 1 to 3 min (16, 38, 168, 179). In afew species the proximity of swarms to hosts has evolved into a substrate-based mating system, whereby males land on the host and copulate with females before or while they feed [e.g., Culicoides nebeculusos (38), C. variipennis sonorensis and C. utahensis (49), and C. sinanoensis (54)]. Some nonblood-feeding midges [e.g., Atrichopogon sp. (38)] aggregate on plants for sugar and pollen feeding, and encounters between males and females lead to lengthy copulations. In nature, the blood-feeding Culicoides melleus mate on algae-covered rocks and possibly other stationary assemblage sites (90). When confined within vials in the laboratory, C. nebeculusos and C. melleus copulate 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 417

readily, without swarming or erection of antennal setae (38, 90, 99). Indeed, any contact with another individual releases indiscriminate copulatory behavior in the male. When such contact is with a conspecific female, contact and volatile pheromones facilitate recognition (92, 100), and copulation, lasting from 8 to 14 min, rapidly ensues (90). During copulation, which in the nonswarming species is accompanied by vigor- ous contractions of the male abdominal sclerites, which may have a mechanical or a copulatory courtship (43) function, a spermatophore containing (in C. melleus) approximately 1200 sperm is transferred to the female (93) and rapidly emptied into the paired spermathecae (179). A vestigial third spermatheca is present in this species but is seldom functional (89). Following the successful transfer of a spermatophore, female C. melleus and C. nebeculusos become unreceptive to further copulations and actively discourage (although not always successfully) male copulation attempts (91, 100). In the field, fewer than 1% of Culicoides variipennis females copulating in swarms were identified as parous, suggesting that only young nulliparous females of this species copulate (179). The evolution of substrate-based mating systems in this group is accompanied by loss of auditory recognition by males, increased female choice based on male courtship, and increased copula duration. Why have these mating systems evolved in this family? Not enough is known of the ecology of the substrate mating species to answer this question. I speculate that the clumped distribution of hosts in extreme environments may be a predictor of host-based mating systems in ceratopogonids. This speculation is based solely on the convergence of males of desert-inhabiting midges to the female vertebrate host (49, 166) and on the few reports of hemi-arctic species converging on hosts (38, 54), and of course needs validation.

Culicidae In this family of ∼3000 species, we find three subgroups: the nonblood- feeding Toxorhynchitinae, the Anophelinae, and the (containing the Aedini, Culicini, Sabethini, and Uranotaeniini). Mass swarms at (or near) aquatic emergence sites are the most common mating system (34, 39, 114), although Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org several other behaviors have evolved in this family.

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. Most anophelines mate in crepuscular swarms. These include Old World vectors of malaria such as members of the Anopheles gambiae complex (29, 31, 101), An. funestus (32), An. culicifacies (128), An. maculipennis (11), An. stephensi, and An. subpictus (120), and some New World anophelines such as An. franciscanus (14), An. pseudopunctipennis (11), and An. freeborni (178). However, species of the neotropical subgenus Anopheles (Nysssorhynchus)have not been observed in the field to mate in swarms (96) and apparently copulate at emergence sites, resting sites, or possibly near the blood meal host (96, 165). Members of other mosquito genera also swarm above markers, including many culicine and aedine species (39, 50, 114). These species are typically explosive 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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breeders with synchronized hatching and high local densities, such as members of the () subgenus (141, 172), many species of Culex (127), and (122). While apparently most male anophelines and culicines are incapable of re- sponding to host cues (107), in a number of other species, males swarm in the immediate vicinity of the host. Notable among these are members of the Aedes (Stegomyia) subgenus (Ae. aegypti, Ae. albopictus, Ae. vitatus, Ae. scutellaris, and Ae. polynesiensis) that are continuous breeders in small permanent or semiper- manent containers of low volume, resulting in highly dispersed populations at low densities (172). Interestingly, three species of the Ochlerotatus subgenus also swarm near the host: Ae. diantaeus, Ae. sierrensis, and Ae. spencerii. These species share the life-history attributes of the Stegomyia species in that their emergence sites are widely dispersed and their emergence is gradual and not explosive (69, 114, 172). I suspect that species from other genera that form swarms around the host, such as Mansonia (Mansonioides) uniformis and Ma. africana (107), share these ecological characteristics. In all swarming culicids (whether at inanimate markers or near the host), females that enter the swarms are recognized by their wing beat frequency. There is no discernible courtship, and mating on the wing lasts between 10 and 30 s. Swarming males exhibit erect antennal fibrillae, which, in addition to the highly sensitive Johnston’s organ, allow them to recognize the frequency of the female’s wing beats and pounce on her as she approaches or enters the swarm. The specificity of these frequencies is enough to distinguish between conspecific males and females and (in some Aedes species) between females of closely related species (20). However, there is extensive overlap between harmonic amplitudes of the wing beat of members of the An. gambiae group (151, 161). Thus other mechanisms— such as volatile (147) or contact pheromones (115, 125)—must be invoked as final recognition cues before copulation. The ability to respond to female wing beats has been reduced and lost in the culicine species that do not mate in flight. One such mating system is based on pupal guarding and has evolved in two genera, and Deinocerites. Male Opifex fuscus,acoastal rock pool mosquito of New Zealand, cannot distinguish between male and female pupae and guard both with equal determination; only

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org when attempting genital contact is the truth revealed. If the pupa is female, she is copulated even before emerging; if male, the pupal case is abandoned and by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. the guarding male rapidly seeks another potential mate (139). Male Deinocerites cancer, the crabhole mosquito, are one step ahead. Although males attempt to copulate with emerging males as well as females, pupal guarding is more intense on female pupae or (albeit briefly) empty female pupal cases (35, 126). Copulation (in the laboratory) is a lengthy affair (40 to 50 min), resulting in the filling of all three spermathecae (126). An intermediate form between mating in swarms and pupal attendance may be exemplified by Culiseta inornata, another small pool breeder. Females are receptive minutes after eclosion. Males, whose antennal fibrillae are scarce, skim 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 419

the surface of emergence sites and copulate with females resting after their eclosion. A contact pheromone and possibly a volatile pheromone aid recognition (39). Interestingly, a similar reduction of the swarming habit is seen in the closely related (but not blood feeding) ground-dwelling crane flies (Tipulidae), in which females broadcast a volatile pheromone that alerts the patrolling males to their location (1). A completely different mating system is exhibited by members of the sabethine tribe (Sabethes, Malaya, and Wyeomyia spp.). In this group, diurnal substrate- based sexual encounters are the rule. Males patrol resting sites, locate females on vegetation, and perform elaborate courtship displays before copulation (59). Copulation is significantly longer than in the swarming species, lasting 2 to 3 min (59, 124). A basic attribute of the polygynous mating swarm is a low variance in female mating success and a high variance in male mating success (136). Few studies have attempted to find correlates to male mating success in swarms. In An. freeborni, copulating males were significantly larger on average than the general population of swarming males (178). However, this was not the case for An. gambiae and An. funestus,inwhich male size was not related to copulatory success (30, 32). The effect of size may vary between species or be related to the variation in size of the population as a whole and to the level of competition in larval habitats. Further- more, the intensity of competition for mates may vary between species or spatially and temporally within species. Thus, male size was significantly correlated to male copulatory success in the pupal-guarding O. fuscus only in pools where the level of competition rose above a certain threshold (140). In any event, success hinges on attending the encounter site, and for swarming mosquitoes this ultimately depends on sugar feeding. A comparison of the energetic reserves of resting and swarm- ing male An. freeborni revealed that males feed on nectar during the night once swarming has concluded and that a swarming bout of 30 min consumes more than 50% of their caloric reserves (175). Thus, foraging successfully is a prerequisite for participation in swarms. In general, the genitalia of male culicids are remarkably adapted for rapid coitus and efficient insemination (145) rather than for species recognition or cop- ulatory courtship. Many studies have attempted to determine how many females

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org an individual male mosquito can inseminate (34). However, given the enormously male-skewed operational sex ratio in swarms (39, 178), and the mortal risks asso- by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. ciated with this habit (32, 146, 173), few males are likely to mate more than once. In light of this low probability, the reproductive interests of a male that manages to copulate are well served by assuring his mate will not copulate again. Following copulation, an ejaculate of approximately 1000 sperm, suspended in male acces- sory gland secretions (MAGS), is retained by the female. These two agents, sperm and MAGS, mediate the control of female receptivity (79). In anophelines, a gelatinous mating plug is produced by the accessory glands and deposited into the vagina after sperm have been transferred (52). This plug, often protruding from the female genital opening, provides a short-term barrier 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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(lasting 24 to 48 h) against further copulations. The storage in the spermathecae of a substantial ejaculate accounts for the long-term inhibition of female receptivity (80). In aedines and culicines, spermathecal filling may provide short-term inhibi- tion, until peptides produced in the accessory glands find their target in the female nervous system and effectively curtail female sexual receptivity (36, 79, 169). In Deinocerites spp., an effective copulation fills all three spermathecae and females do not copulate again (126). Furthermore, in this genus the temporal window of receptivity to copulation is narrow. Virgin females denied copulation for a week are no longer receptive when allowed access to males (126). Studies of remating by female mosquitoes may produce misleading results in the laboratory when unnatural densities and frequencies of male-female contact are contrived (see Reference 98 for an experimental demonstration of this concept). In the field, female mating patterns have been investigated only in populations of six anopheline species. No evidence of polyandry was found in An. dirus, An. maculatus (10), or An. messae (Novikov 1981, quoted in Reference 34); low rates (1% to 4% of female remating) were found in An. gambiae (152) and An. freeborni (174). A higher rate of polyandry was exhibited by female An. nuneztovari, 15% of which had mated with at least two males (131). Multiple spermathecae are believed to be instruments of cryptic female choice by allowing females to segregate and discriminate between ejaculates of suc- cessive mates (44, 137). Intriguingly, numbers of spermathecae vary among fe- male mosquitoes, one in Anopheles,two or three in most aedines, and three in Culex, Deinocerites, and Toxorhynchites (34). Thus, although all these females are monogamous, some exhibit the morphological features associated with polyandry and others do not. Perhaps the current number of spermathecae and the effects of MAGS on females are evidence of past conflicts between, or the conver- gence of, male and female reproductive interests. Accordingly, Sherlock Holmes’ approach—“In solving a problem of this sort, the grand thing is to be able to rea- son backward”—needs to be employed to explain this situation. Let us assume that monogamy and autogeny were the primitive state of the short-lived ancestral culicids. This assumption is supported by the biology of the Chaoboridae, the sister group of Culicidae (13). Chaoborid larvae are relatively long-lived, adults are short-lived and form massive mating swarms at emergence sites (67), and fe-

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org males have only one spermatheca (108). The original function of the MAGS may have been to provide a nutritional nuptial gift, designed to push females over the by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. autogeny threshold. This function may still survive in some species (116, 117) and provide a trigger for egg development (81, 95). As sugar feeding evolved, and longevity increased, promiscuous female behavior and multiple spermathecae would have appeared. When females evolved the novel blood-feeding habit, pater- nal investment became less important and the accessory glands developed a more selfish and less cooperative function—that of curbing female receptivity (36, 79). Apparently, all this never evolved in anophelines, the basal group in this family (113). Uniquely, male Anopheles ejaculate directly into the single spermatheca [in the other mosquito genera the ejaculate is deposited into the bursa copulatrix, from 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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which sperm are transported to the spermathecae (145)], and the female genital tract is physically plugged by MAGS. Thus, anopheline males may have evolved the ability to impose monogamy earlier than males of other genera and before females were able to manifest an evolutionary response. In conclusion, swarming is the basic and most common mating system in the Culicidae, branching off into mating at emergence sites and pupal guarding, host- based swarms, or diurnal encounters at resting sites that include courtship. Depar- tures from encounters in swarms have evolved in response to discrete ecological conditions or life-history characteristics. Host-based swarms have evolved in cases in which life history has departed from synchronized emergence and the host pro- vides a convenient encounter site. Pupal guarding seems to have evolved in species with ephemeral breeding sites, protandry, and possibly intensive predation pressure on swarms (a convenient guess). Resting site encounters, with elaborate courtship displays and relatively long copulations, have evolved in the sabethines, species with relatively low local abundance that exhibit catholic host preferences but highly specific oviposition and resting site preferences.

Corethrellidae This is a small family recently separated from the Chaoboridae. Females are at- tracted to the mating calls of male anurans and feed upon them (109). Males are not attracted to these hosts (110). In laboratory colonies, females mate following emergence, suggesting that in the field mating takes place at emergence or resting sites (109). Sperm are stored in a single spermatheca, similar in structure to that of anophelines (108).

PSYCHODOMORPHA Psychodidae Of the six families in this group, blood feeding has evolved in only three genera (constituting the Phlebotominae) within the family Psychodidae. These genera are Phlebotomus, Lutzomyia, and Sergentomyia. The life history of these sandflies is

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org typified by an intimate association with vertebrates, as females seek moist, dark, and humic habitats to oviposit and frequently do so in the burrows and nests of by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. wild or in the cracks and crevices, rich with decomposing organic matter, found in the enclosures of domestic animals (77). This prolonged association with the host seems to dictate the mating system. Although males do not take a blood meal, copulation occurs on or in the vicinity of the host, and its probability is enhanced by host-produced cues (74, 75, 170). In the few species for which sexual behavior has been studied with some degree of ecological realism, common characteristics of the mating system emerge. The sandfly mating system can be considered to be a classic lek (136), as males occupy and defend discrete territories on or near the host and produce a complex courtship 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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display comprising pheromone emissions, wing fanning, and elaborate, stereotyp- ical movements of the abdomen. Pheromone-disseminating structures have been found on the abdominal tergites of males in species from all blood-feeding genera (160). Females approach signaling males and experience a bout of close range, aggressive courtship that culminates in copulation or rejection of the male by the female. Similar mating systems are seen both in Old World phlebotomines, such as Phlebotomus martini (12), P. papatasi (170), P. argentipes (84), and P. duboscqi (154), and in the New World species Lutzomyia vexator (28) and L. longipalpis (70, 74). The duration of the various elements of courtship, pheromone emission, and copulation (and species-specific behaviors such as “piggy-backing” in P. dubosqui) are influenced by host presence and density, the operational sex ratio, and the age and reproductive history of the individuals involved (70, 74, 154). This may explain why reports of copula duration vary greatly. Copulation lasts approximately 1 min in L. longipalpis (71, 74), 3 to 5 min in L. vexator (28), 19 min on average in P. papatasi (range 2 to 80 min) (170), 1 to 3 min in P. argentipes (119), and in P. dubosqui copula duration ranges from 4 to 20 min (154). Correlates to male mating success have been studied in L. longipalpis by Jones and colleagues. Female L. longipalpis prefer 4- to 6-day-old males over younger or older individuals, a preference that is significantly correlated with their subse- quent reproductive success (72). Leks differ in their attractiveness to mate-seeking females. Larger males congregate in larger leks, which on average attract more females (74). Furthermore, females attending large leks have, on average, a shorter latency to copulate than do females at smaller leks (74). Although the ability to win fights was not correlated with male mating success, there was a correlation between the amount of time spent wing fanning and amount of pheromone present in the abdominal glands (73). This suggests a link between nutritional status, either carried over from the larval stage or improved by foraging for plant sugars, and reproductive success. Such a link is also apparent in the nocturnal behavior and distribution patterns of male P. papatasi (171, 177). Thus, there is evidence for nutritional status, size, and age as determinants of male reproductive success in phlebotomines. The genitalia of male sandflies are complex and elaborate, suggesting a poten-

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org tial for their use in copulatory courtship (43) and the action of sexual selection in determining their shape and size (8). Ejaculation and insemination in these flies by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. occur within the paired spermathecae by means of the thin and elongated male aedeagal filaments that reach well into the lumen of each spermatheca (66, 102). Within the spermathecae of P. papatasi, the ejaculate undergoes a series of func- tional transformations. Initially, sperm are inactive and the ejaculate functions as an effective mating plug. Sperm are activated after females ingest blood and eggs mature, and all are mobilized for fertilization (103). Female phlebotomines usually mate only once during a gonotrophic cycle (71). However, female receptivity is routinely renewed following oviposition and depletion of sperm supplies in the spermathecae (56, 176). 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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The few species in which sexual behavior has been critically investigated show common ethological trends. However, diversity in structure of pheromone glands and their emissions (58), as well as in the discrete repertoires of courtship and mate guarding unique to some species (144, 154), suggests that there is much undiscovered variation within this group. Nevertheless, the critical life-history pa- rameter that distinguishes these flies from other nematocerans is the disassociation from aquatic larval habitats and the adoption of decomposing organic matter as the larval habitat. This habit promoted intense contact with vertebrates, favored the evolution of blood feeding, and led to host-based leks with female choice.

TABANOMORPHA

There are two families containing blood-feeding genera in this large brachyceran group, the Tabanidae and Rhagionidae. In both families, the larvae are relatively long-lived predators that inhabit semi-aquatic habitats. In the adult stage, only females take blood yet both sexes feed on plant-derived sugars (133).

Rhagionidae Little is known about the mating systems of snipe flies, which are among the most primitive of the Brachycera and may represent a link between the Nematocera and the more recently evolved dipteran suborders. Hoy & Anderson (63) studied the behavior of several species of snipe flies of the genus Symphoromyia that feed primarily on deer. These flies mate in swarms, often containing hundreds of individuals, that form along the banks of streams and forest pathways, among trees, on slopes or crests of hills, and even on mountaintops (63, 153). Males hovering in the swarm maintain fixed distances from each other and pursue flying objects that penetrate the airspace of the swarm. Swarming takes place during the day from midmorning to early afternoon, seems to be regulated by temperature, with an initiation threshold of 21◦C, and is absent on cool and cloudy days (63, 153). Copulations are initiated on the wing and terminate several seconds later on the ground. Although males are not found on or near hosts, all nulliparous females collected while biting deer or in CO2-baited traps were inseminated (63). Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org Conversely, noninseminated females were caught only in mating swarms, and most

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. of these were nullipars (63). These observations suggest that females mate early in life and seldom, if ever, remate.

Tabanidae Although there are more than 3500 species in this family of clegs, deer flies, and horse flies, the sexual behavior of fewer than 60 species has been described, and many of these descriptions are highly anecdotal. For example, while most students of swarms use sweep nets to collect specimens, Bailey (9) reports that in 1919, Mosier and Barber used a .22 caliber pistol loaded with dust shot to 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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sample swarming tabanids and that “the ten specimens so obtained were all males.” Most of the studies on sexual behavior of tabanids have been conducted in tem- perate habitats of the New World. The most frequently reported behavior preceding mating is the swarming or hovering of males near emergence sites or in hilltop clear- ings. A great interspecific variation is observed, from dense swarms to isolated, spaced individuals (39). In Tabanus americanus, males form massive aggregations resembling nematoceran swarms (Snyder 1917, quoted in Reference 9). However, males of most species hover in evenly spaced aggregations numbering tens rather than thousands of individuals (9, 164). Several alternatives to hovering over veg- etation near emergence sites or in hilltop clearings have been reported. In the two Old World species Haematopota sewelli and Tabanus aurupunctatus, males were observed hovering over hosts and, in the latter species, copulating with females coming in to feed (9). A more common and more rigorously studied alternative to hovering is termed perch and dart, whereby males await females on blades of grass or other salient features of the habitat and dart at them as they approach or pass above (88, 148). It has been postulated that in some species of perching Chrysops, males emit a sex pheromone to attract potential mates to their waiting station (164). Male sexual activity is expressed in clear weather during discrete temporal windows of relatively short duration (88, 164). These periods are species specific, regulated by light intensity and temperature, and constrained by carbohydrate re- serves (88, 133, 148, 164). Sympatric species with overlapping activity periods are usually spatially separated (48, 142). The holoptic eyes of males, which al- low high visual acuity for detecting and intercepting females, are also adapted to the specific light intensity prevailing during hovering bouts (164). In temperate and hemi-arctic habitats male activity is strictly regulated by temperature. Thus, Ch. fuliginosus males assume head-up interception positions in their salt marsh habitat at air temperatures of 18◦Cbut intercept and copulate with females only when temperatures exceed 20◦C (27). Similarly, in populations of T. nigrovittatus two groups of hovering males are observed, each having significantly different temperature requirements. One group hovers when ambient temperatures range from 15 to 20◦C, the other at temperatures between 22 and 27◦C (48, 132). These preferences, which have a genetic basis, result in temporal separation of the two

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org groups and may evince the action of an isolating mechanism leading to eventual speciation (134). The location of hovering males corresponds to female emergence by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. sites, suggesting that they are well placed to intercept young females (111). In- deed, the few studies of the hierarchical relationship between mating and feeding behavior of female tabanids indicate that copulation precedes feeding, as more than 90% of host-seeking females are inseminated (6, 86, 87). Hilltops are frequently used as aggregation sites by both hovering and perching species (88). For example, in North America, Hybomitra arpadi males hover in hilltop clearings and vigorously intercept females that approach the area (142). Similarly, male H. illota aggregate in clearings in the woods, where they perch and accost females and other insects flying overhead (148). 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 425

Copulation, initiated on the wing, proceeds on the ground or vegetation and (depending on ambient temperature) lasts from 3 to 60 min, with averages (in Ch. fulginosus) ∼30 min (9, 27, 164). Most copulation attempts are rejected by females, and it may be that the pursuit flight of the male provides information for female choice and that contact pheromones provide information on species and status of both pursuer and pursued (142, 148). Little is known of the determinants of male reproductive success, but it is clear that sugar reserves constrain the ability of both hovering and perching males to pursue females (88, 142, 148). Furthermore, in H. arpadi (the only species in which this was studied), males that captured females had shorter legs, were heavier, and had larger wing areas than did the remainder of the population (142). The presence of three spermathecae are a basal feature of the Brachycera (167), including female tabanids. However, in tabanids this complement is apparently not associated with multiple mating. Smith et al. (142) observed a few failed copulation attempts of H. arpadi with parous females yet concluded that females of this species mate only once; there are no other reports of multiple mating by females. The transition from hovering to perching may have been mediated by energetic constraints or by predators. Tabanid males are frequently captured by sphecid wasps (9, 46, 83), and past selection pressures may have driven the perching species away from hovering. Perching and darting itself has its dangers, particularly when the darting is indiscriminate, and sphecids such as Oxybelus may mimic female behavior and capture tabanids that attempt to copulate with them (21). The blood feeding habit evolved again in the higher flies, in the calypteratae section of the cyclorrhaphous Schizophora, in which the most recently and highly evolved superfamilies of flies, the Muscoidea, Hippoboscoidea and Oestrodea are found (167). It is curious that blood feeding did not evolve in the groups bridging the gap between the Brachycera and higher Cyclorrapha, groups in which the greatest diversity (both ecological and taxonomic) is found. This question, however, is not the subject of my review. The big difference between the calypterate blood- feeding flies and all others dealt with before is the introduction in the former of the evolutionary novelty that both sexes feed on blood. This habit favors a strong association between both sexes and the vertebrate host and greatly influences the

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org mating systems. by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. MUSCOIDEA

Muscidae Two genera from this infamous family are blood-feeders: the stable flies (Stomoxys spp.) and the horn and buffalo flies (Haematobia spp). Male Stomoxys calcitrans await females in assembly stations that typically form on prominent, sunlit objects close to or within the animal enclosures that are the habitat of these flies (23). These stations serve a dual function as both encounter and basking sites that aid 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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in thermoregulation (5). Responding visually, males assault approaching objects energetically and proceed to copulate following recognition by contact pheromones (18, 62). If the assault flight is unsuccessful, they return to the original waiting station, which they defend with vigor. Copulations, on the ground or perch, last between 3 and 14 min, the latter time apparently characteristic of a sperm-depleted male (23). Experiments in laboratory cages resulted in copula durations of 5 min on average (7). During copulation the male uses his hind legs to stroke and lift the terminal part of the female abdomen (7), behaviors that may represent copulatory courtship. The closely related Haematobia, which spend most of their adult lives on hosts in pastures, mate on the host (82) where final recognition is also facilitated by a contact pheromone (18). Copulations take place throughout the day and are of relatively short duration (29 s on average) (82). In Stomoxys spp., male mating success depends significantly on prior ingestion of several blood meals. Males that do not ingest blood fail to pursue and court females (7). Furthermore, although spermatogenesis is independent of blood feed- ing, accessory glands fail to develop in males that do not feed on blood and such males are incapable of producing seminal fluid (7). Females have two spermathecae and reportedly seldom remate on the days following a successful copulation (61, 143). However, Stomoxys females confined with males for life had higher lifetime fecundity than did females who copulated only once early in life (78). This suggests that female stable flies may adaptively remate, probably when sperm supplies decline or the effects of male-imposed inhibitions wane.

HIPPOBOSCOIDEA

In this suborder, viviparity (112) has evolved in addition to blood feeding, whereas sugar feeding has been lost. Three families in this group, constituting the louse flies and bat flies, spend most of their adult life on the vertebrate host. A fourth family, the tsetse flies, visit the host periodically to imbibe blood and, at least in some species, to encounter mates. Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. Hippoboscidae, Streblidae, and Nycteribiidae Although few studies have directly addressed the sexual behavior of these recondite flies, the following general picture emerges: In most species, both sexes congregate in a nonrandom fashion on individuals of the host population (47, 57, 149). In both families of bat flies, blood feeding is an essential prerequisite before copulation, as nonfed individuals are mechanically incapable of coupling (105, 130). Copulation [which lasts ∼25 min in Hippobosca equina (57) and ∼5 min in the streblid Megistopoda aranea (118)] usually takes place on the host. However, although both males and females of the nycteribiid Basilia hispida are found on the bat host, 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 427

copulations take place off the host immediately after extrusion of the prepupa (105). Males in this species guard females for up to 4 h before copulation, which itself may last from 30 min to2h(104). Furthermore, males of other nycteribiid species have never been found on hosts (or anywhere else, for that matter), suggesting that copulation occurs off the host, in the cracks and crevices of the roost site (6). Female Hippobosca remate after larviposition (57), female streblids remate before each puposition event (47, 118), and female nycteribiids remate after ex- truding each prepupa (105). These generalizations suggest little variation in sexual behavior within this group. However, I suspect the opposite is the case. Seasonal and spatial variations in sex ratios on hosts (106, 149, 155), in combination with variations in patterns of host spatial distribution and daily activity, may contribute to a diversity (albeit all host based) of mating tactics that remain to be explored.

Glossinidae There are about 30 species of tsetse flies, which are ecologically segregated among savanna, forest, and riverine habitats. The unique life-history characteristics com- mon to all species are the need of both males and females to imbibe blood at least every 3 days and the slow development of a single larva at a time within the female uterus. Local density of tsetse flies is low in all the habitats in which they occur, yet virgin females are rarely encountered in the field (159). In savanna species, males form “following swarms” in the vicinity of hosts, from within which they react rapidly to flying females. Mating on or around the host has been observed for Glossina morsitans morsitans and G. swynnertoni. G. morsitans morsitans have been observed in the field copulating in flight. Conversely, G. pallidipes, although sympatric, do not mate near hosts with the same alacrity and have rarely been seen mating in the field (68). Tsetse vision is highly suited to intercepting or chasing flying females, as the extended region of binocular overlap in males enables them to detect the approach of females (51). In the field males respond to flying objects by chasing them, apparently using speed-matching as a preliminary species recognition cue (19). Following male interception of the female, a nonvolatile species-specific contact pheromone is recognized (26, 65) and copulation ensues. In the field it is unclear Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org whether copulation begins in the air as a culmination of a successful chase or on

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. the ground after females land. Mating occurs opportunistically throughout the day, with no clear rhythm, much as blood feeding does. In all species studied, male activity during copulation is consistent with copu- latory courtship—leg rubbing and drumming, shaking, and audible wing buzzing produced by both sexes (68, 159). Sperm are transferred within a spermatophore during the final stages of copulation and stored in two spermathecae. Copula du- ration varies between and within species, ranging from 30 min to2h(37, 68, 159). Females remain attractive to males after copulating, and multiply mated females are more fecund than those that are singly mated (68). Immature males fail to 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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inhibit female receptivity, a failure also apparently incurred by sterile males (37). However, a successful copulation with a mature male (involving transfer of a substantial spermatophore containing copious amounts of sperm and accessory gland secretions) usually results in temporary inhibition of female receptivity and triggering of ovulation (53). Male mating success, in all species studied, improves with age and the attendant development of accessory glands following blood feeding. Indeed, young male G. swynnertoni do not participate in the following swarms, nor are young males of G. pallidipes and G. morsitans morsitans trapped on mobile baits containing female decoys (159). Furthermore, although the host-based mating system allows males to switch opportunistically between blood-feeding and host-seeking females, the nutritional status of males affects sexual activity. Thus, Bursell (22) suggested that in G. swynnertoni mating activity increases after blood feeding and decreases as energy stores decline in the fat body. This pattern was experimentally confirmed in laboratory studies for both G. pallidipes and G. morsitans morsitans (157, 158). Furthermore, in G. palpalis males of high nutritional status spend relatively more time flying than do females, an activity pattern consistent with maximizing mating opportunities (2). Although low local density predicts mating on or near hosts, and observations on a few savanna species support this prediction, our knowledge of most tsetse species is limited by the difficulty of studying these insects in the field. Higher order interactions, beyond the male-female conflict and feeding versus mating tradeoffs, may shape some aspects of the mating systems of these flies. A first step in illuminating this complexity has been taken by Gouteux & Jarry (55), who have shown how interspecific sexual interactions can affect the spatial, temporal, and populational dynamics of the tsetse guild sharing the same locality.

SYNTHESIS AND CONCLUDING REMARKS

The families of blood-feeding Diptera exhibit a transition from the aerial swarm, primarily with auditory recognition, rapid copulae, and no direct female choice, to substrate-based systems. This transition is accompanied by increased reliance on

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org visual and chemical recognition, greater opportunities for female choice, longer copulations including rituals of copulatory courtship, and frequent remating by by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. females (Table 1). While this progression from air to substrate has an obvious phylogenetic trend, it also occurs occasionally within the various nematoceran groups. Furthermore, the progression from aerial to substrate-based mating sys- tems is not unique to the blood-feeding flies: While most nematoceran families mate in swarms, many of the Brachycera, as well as acalypterate and calypter- ate flies, exhibit a gradual shift to hilltopping and thence substrate mating, with increasingly complex male courtship behavior and pre- or postcopulatory female choice (3, 135). This move from aerial swarming to substrate-based systems in the Diptera occurred when the substrate offered a resource such as a blood meal 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 429

or oviposition site or served as a convenient marshalling point, as in hilltoping or leks. In addition, predation on swarms may in the past have pushed swarming males out of the air and into more protected sites. In the blood-feeding flies, mating on the host has evolved under several discrete conditions. The first (and easiest to demonstrate) is when life history dictates a prolonged association with the host. This happens in the stable flies, louse flies, and bat flies, in which both sexes frequently feed on the host and spend virtually all their adult life on or around it. Such an association is also true of the phlebotomine sandflies, whose oviposition habits engender an intimacy with vertebrates, and although males do not take blood meals, the vicinity of the host is sought for establishing leks and attracting females. Host-based mating systems are also seen in some species belonging to families in which most species form aerial swarms over inanimate markers. With the exception of the aedines that exhibit this behavior, not enough is known about the specific ecological conditions that promote such situations. Nevertheless, on the basis of what we know from Aedes biology, and a few snippets of information about certain simuliids and ceratopogonids, I would hazard a generalization that these associations evolve either when highly species- specific blood-feeding preferences develop (97), when the emergence pattern of the flies is temporally staggered (69, 172), or when the spatial distribution of the hosts in harsh environments is highly clumped (49, 54, 166). Determinants of male reproductive success have not been studied in many species of blood-feeding flies. Nevertheless, when we look at the few species for which this question has been addressed, a pattern emerges. Whereas individual size is not a universal correlate to copulatory success, nutritional status is. Thus, whether the males are sugar-feeders or blood-feeders, success in foraging for nutrients significantly affects subsequent copulatory success. Sugars are essential to fuel swarming (175), lekking (73), or hovering (142) in mosquitoes, sandflies, and tabanids, respectively. Ingesting blood is a prerequisite for successful copulation in both families of bat flies (105, 130). Finally, in both muscid and tsetse flies, blood feeding is essential for accessory gland development and, in the latter, also serves to fuel flight (2, 7). A trend in patterns of female remating is evident in the various families of blood- feeding flies and is closely linked to the operational sex ratio, opportunities for

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org female choice, and copula duration. In the nematoceran and brachyceran families that mate in the air, operational sex ratios are highly male skewed, female choice is by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. indirect, copulae are relatively short, and remating by females is rare. Conversely, in the Psychodidae, in which females actively choose males in leks, copulae are relatively long and females remate before each gonotrophic cycle. Similarly, in the higher Diptera, copulations are lengthy and females routinely mate more than once. I suggest that the intensity of sexual selection operating on males in systems in which the probability of mating is low has favored male ability to control female receptivity. The study of mating systems has progressed immensely in the last 20 years, providing the empirical basis for formulating and testing hypotheses 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

430 YUVAL ycle 5% emale gonotrophic c emating < F r 0%–4% 1 1 5 20 Each Copula duration (min) 8–14 < < ∼ ∼ visual contact contact + + + pheromone pheromone pheromone?) Olfactory & contact Contact pheromone 40–50 Never Auditory or hosts guarding swarms On hostsOn vegetation Contact pheromone(?) Other encounter sites Mate recognition Resting sites VisualPupal ( Host-based Unknown Olfactory host Main mating encounter site Male nutrition Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. Host contact Summary of some life-history and mating system attributes of the families of blood-feeding Diptera Simuliidae Brief Sugar Swarm Visual 3–7 Ceratopogonidae BriefCulicidae Sugar Brief Swarm Sugar Swarm Auditory Auditory 1–3 Rare Corethrellidae BriefPsychodidae Prolonged Sugar Sugar Unknown Lek on/near Unknown Unknown Unknown Unknown ABLE 1 axonomic group T T Nematocera Culicimorpha Psychodomorpha 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

MATING OF BLOOD-FEEDING FLIES 431 Rare Frequent(?) 1 < 10 Rare 5 30–120 Frequent contact contact contact contact + + + + isual pheromone pheromone pheromone pheromone V Perch and dart Visual On host Resting sites? host Perch and dart Visual + blood Sugar Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. prolonged abanidae Brief Sugar Swarm Visual Rhagionidae Brief Sugar Swarm Unknown Visual T Muscidae Brief or HippoboscidaeStreblidae ProlongedNycteribiidaeGlossinidae Blood On host Brief Blood Swarm near Near On host host Unknown 25 Frequent 30–120 5 Frequent Frequent Brachycera Tabanomorpha Schizophora Calypteratae Muscoidea Hippoboscoidea 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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about many aspects of and its evolution (33, 137, 150). This knowledge is also frequently used judiciously to control populations of pest insects (24, 129). Conversely, with few notable exceptions, progress in our knowledge and understanding of the sexual behavior in the field of blood-feeding in general and flies in particular has been slow. Nevertheless, blood-feeding flies and the diseases they transmit are still very much with us and will remain so until inte- grative, sustainable, and biologically lucid approaches for their control are devised. Understanding and ultimately manipulating the sexual behavior of blood-feeding flies will be part of these efforts.

ACKNOWLEDGMENTS I thank Marc Klowden for suggesting that I attempt this review. Batya Kamensky translated Reference 54 from Russian. I am indebted to Daniel Briceno, Don Colless, Ed Cupp, Theresa Jones, Gary Fritz, Phil Lounibos, and Steve Schutz, who patiently answered queries. Comments by Marc Klowden, Bart Knols, Sharon Shafir, and Todd Shelly greatly improved previous versions of this review.

The Annual Review of Entomology is online at http://ento.annualreviews.org

LITERATURE CITED 1. Adler PH, Adler CRL. 1991. Mating be- meal on the mating drive of males and its havior and the evolutionary significance necessity as a prerequisite for proper in- of mate guarding in three species of crane semination of females. J. Econ. Entomol. flies (Diptera, Tipulidae). J. Insect Behav. 71:379–86 4:619–32 8. Arnqvist G. 1998. Comparative evidence 2. Adlington D, Randolph SE, Rogers DJ. for the evolution of genitalia by sexual se- 1996. Flying to feed or flying to mate: lection. Nature 393:784–86 gender differences in the flight activity of 9. Bailey NS. 1948. The hovering and mat- tsetse (Glossina palpalis). Physiol. Ento- ing of Tabanidae: a review of the literature mol. 21:85–92 with some original observations. Ann. En- 3. Alcock J. 1987. Leks and hilltopping in tomol. Soc. Am. 41:403–12 insects. J. Nat. Hist. 21:319–28 10. Baimai V, Green AC. 1987. Monandry 4. Allan JD, Flecker AS. 1989. The mat- (monogamy) in natural populations of Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org ing biology of a mass-swarming mayfly. anopheline mosquitoes. J. Am. Mosq.

by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. Anim. Behav. 37:361–71 Control Assoc. 3:481–84 5. Allan SA, Day JF, Edman JD. 1987. Vi- 11. Bates M. 1949. The Natural History of sual ecology of biting flies. Annu. Rev. En- Mosquitoes.New York: Macmillan. 379 tomol. 32:297–316 pp. 6. Anderson JR. 1974. Symposium on re- 12. Beach R, Young DG, Mutinga MJ. 1983. production of arthropods of medical and New phlebotomine sand fly colonies: veterinary importance. II. Meeting of the rearing Phlebotomus martini, Sergento- sexes. J. Med. Entomol. 11:7–19 myia schwetzi, and Sergentomyia africana 7. Anderson JR. 1978. Mating behavior of (Diptera: Psychodidae). J. Med. Entomol. Stomoxys calcitrans: effects of a blood 20:579–84 27 Oct 2005 13:30 AR ANRV263-EN51-18.tex XMLPublishSM(2004/02/24) P1: OKZ

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13. Beckenbach AT, Borkent A. 2003. Molec- havior of stable flies under field condi- ular analysis of the biting midges tions. Environ. Entomol. 10:16–21 (Diptera: Ceratopogonidae) based on mi- 24. Calkins CO. 1998. Review of the codling tochondrial cytochrome oxidase subunit moth areawide suppression program in the 2. Mol. Phylogenet. Evol. 27:21–35 western United States. J. Agric. Entomol. 14. Belkin JN, Ehman N, Reid G. 1951. Pre- 15:327–33 liminary field observations on the behav- 25. Campbell MM, Kettle DS. 1979. Swarm- ior of adults of Anopheles franciscanus ing of Culicoides brevitarsis Kieffer McCracken in Southern California. Mosq. (Diptera: Ceratopogonidae) with refer- News 11:23–31 ence to markers, swarm size, proximity to 15. Blackwell A, Luntz AJM, Mordue W. cattle and weather. Aust. J. Zool. 27:17– 1992. Morphology of the antennae of two 30 species of biting midge—Culicoides im- 26. Carlson DA, Langley PA, Huyton PM. punctatus (Goetghebuer) and Culicoides 1978. Sex pheromone of the tsetse fly: iso- nubeculosus (Meigen) (Diptera, Cerato- lation, identification, and synthesis of con- pogonidae). J. Morphol. 213:85–103 tact aphrodisiacs. Science 201:750–54 16. Blackwell A, Mordue AJ, Young M, Mor- 27. Catts EP, Olkowski W. 1972. Biology of due W. 1992. The swarming behavior Tabanidae (Diptera): mating and feeding of the Scottish biting midge, Culicoides behavior of Chrysops fuliginosus. Envi- impunctatus (Diptera: Ceratopogonidae). ron. Entomol. 1:448–53 Ecol. Entomol. 17:319–25 28. Chaniotis BN. 1967. The biology of Cal- 17. Boakye DA, Back C, Brakefield PM. ifornia Phlebotomus (Diptera: Psychodi- 2000. Evidence of multiple mating and dae) under laboratory conditions. J. Med. hybridization in Simulium damnosum s.l. Entomol. 4:221–33 (Diptera: Simuliidae) in nature. J. Med. 29. Charlwood JD, Jones MDR. 1980. Mat- Entomol. 37:29–34 ing in the mosquito Anopheles gambiae 18. Bolton HT, Butler JF, Carlson DA. 1980. s.l. II. Swarming behaviour. Physiol. En- A mating stimulant pheromone of the horn tomol. 5:315–20 fly, Haematobia irritans (L.): demonstra- 30. Charlwood JD, Pinto J, Sousa CA, Fer- tion of biological activity in separated cu- reira C, do Rosario VE. 2002. Male ticular components. J. Chem. Ecol. 6:951– size does not affect mating success (of 64 Anopheles gambiae in Sao Tome). Med. 19. Brady J. 1991. Flying mate detection and Vet. Entomol. 16:109–11 chasing by tsetse flies (Glossina). Physiol. 31. Charlwood JD, Pinto J, Sousa CA, Mad- Entomol. 16:153–61 sen H, Ferreira C, do Rosario VE. 2002. 20. Brogdon WG. 1994. Measurement of The swarming and mating behaviour of

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167. Yeates DK, Wiegmann BM. 1999. Con- in mosquito swarms. Oecologia 95:65– gruence and controversy: toward a higher- 69 level phylogeny of Diptera. Annu. Rev. 174. Yuval B, Fritz GN. 1994. Multiple mat- Entomol. 44:397–428 ing in female mosquitoes: evidence from 168. Yeh CC, Chuang YY. 1996. Colonization a field population of Anopheles freeborni and bionomics of Forcipomyia taiwana (Diptera: Culicidae). Bull. Entomol. Res. (Diptera: Ceratopogonidae) in the labo- 84:137–40 ratory. J. Med. Entomol. 33:445–48 175. Yuval B, Holliday-Hanson M, Washino 169. Young ADM, Downe AER. 1987. Male RK. 1994. Energy budget of swarming accessory gland substance and the con- male mosquitoes. Ecol. Entomol. 19:74– trol of sexual receptivity in female Culex 78 tarsalis. Physiol. Entomol. 12:233–39 176. Yuval B, Schlein Y. 1986. Evidence 170. Yuval B. 1987. Aspects of the behavior, in for polygamy in Phlebotomus papatasi the laboratory and the field of the sand Scopoli. Ann. Parasitol. Hum. Comp. fly Phlebotomus papatasi (Diptera: Psy- 61:693–94 chodidae), the main vector of leishmani- 177. Yuval B, Schlein Y. 1986. Leishmaniasis asis in Israel. PhD thesis. Hebrew Univ., in the Jordan Valley. III. Nocturnal activ- Jerusalem. 96 pp. ity of Phlebotomus papatasi in relation 171. Yuval B. 1991. Populations of Phleboto- to nutrition and ovarian development. J. mus papatasi (Diptera: Psychodidae) and Med. Entomol. 23:411–15 risk of Leishmania major transmission in 178. Yuval B, Wekesa JW, Washino RK. three Jordan Valley habitats. J. Med. En- 1993. Effects of body size on swarming tomol. 4:492–95 behavior and mating success of male 172. Yuval B. 1994. The vertebrate host as Anopheles freeborni (Diptera: Culicidae). mating encounter site for its ectopara- J. Insect Behav. 6:333–42 sites: ecological and evolutionary consid- 179. Zimmerman RH, Barker SJ, Turner ECJr. erations. Bull. Soc. Vector Ecol. 19:115– 1982. Swarming and mating behavior of a 20 natural population of Culicoides variipen- 173. Yuval B, Bouskila A. 1993. Tempo- nis (Diptera: Ceratopogonidae). J. Med. ral dynamics of mating and predation Entomol. 19:151–56 Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. P1: JRX November 2, 2005 13:47 Annual Reviews AR263-FM

Annual Review of Entomology Volume 51, 2006

CONTENTS

SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS, Qi Wu and Mark R. Brown 1 PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS:BIOLOGICAL SIGNIFICANCE, David Stanley 25 BOTANICAL INSECTICIDES,DETERRENTS, AND REPELLENTS IN MODERN AGRICULTURE AND AN INCREASINGLY REGULATED WORLD, Murray B. Isman 45 INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67 INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintraub and LeAnn Beanland 91 INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, Anupama Dahanukar, and John R. Carlson 113 INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzer and Hugh V. Danks 137 PLANT CHEMISTRY AND NATURAL ENEMY FITNESS:EFFECTS ON HERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163 APPARENT COMPETITION,QUANTITATIVE FOOD WEBS, AND THE STRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES, F. J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187 STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN, Susan E. Fahrbach 209 EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233 DOPA DECARBOXYLASE:AMODEL GENE-ENZYME SYSTEM FOR by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. STUDYING DEVELOPMENT,BEHAVIOR, AND SYSTEMATICS, Ross B. Hodgetts and Sandra L. O’Keefe 259 CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PEST MANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285 HOST PLANT SELECTION BY APHIDS:BEHAVIORAL,EVOLUTIONARY, AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh, and Jim Hardie 309

vii P1: JRX November 2, 2005 13:47 Annual Reviews AR263-FM

viii CONTENTS

BIZARRE INTERACTIONS AND ENDGAMES:ENTOMOPATHOGENIC FUNGI AND THEIR HOSTS, H.E. Roy, D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331 CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follett and Lisa G. Neven 359 THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIE ARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387 MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413 CANNIBALISM,FOOD LIMITATION,INTRASPECIFIC COMPETITION, AND THE REGULATION OF POPULATIONS, David H. Wise 441 BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICA AND THE CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC AND CLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467 DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING:A COMPARATIVE ANALYSIS OF RECENT APPROACHES, Nuria« Bonada, Narc«õs Prat, Vincent H. Resh, and Bernhard Statzner 495 TACHINIDAE:EVOLUTION,BEHAVIOR, AND ECOLOGY, John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525 TICK PHEROMONES AND THEIR USE IN TICK CONTROL, Daniel E. Sonenshine 557 CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks, Kevin R. Foster, and Tom Wenseleers 581 ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL AGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler, H.M.T. Hokkanen, and A.J.M. Loomans 609 DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635 PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC MICROORGANISMS AND HERBIVOROUS ARTHROPODS, Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663

Annu. Rev. Entomol. 2006.51:413-440. Downloaded from arjournals.annualreviews.org INDEXES Subject Index 691 by UNIVERSITY OF CALIFORNIA - RIVERSIDE LIBRARY on 05/16/07. For personal use only. Cumulative Index of Contributing Authors, Volumes 42Ð51 717 Cumulative Index of Chapter Titles, Volumes 42Ð51 722

ERRATA An online log of corrections to Annual Review of Entomology chapters may be found at http://ento.annualreviews.org/errata.shtml