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Mating Systems of Blood-Feeding Flies

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Mating Systems of Blood-Feeding Flies 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 FLIES Boaz Yuval Department of Entomology, Hebrew University of Jerusalem, Rehovot 76100, Israel; email: [email protected] KeyWords Diptera, sexual behavior, swarm, female choice ■ Abstract The mating system 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 animal’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 414 YUVAL (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 insects. 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 MATING OF BLOOD-FEEDING FLIES 415 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 copulation 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 416 YUVAL 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).
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