Bedbugs Evolved before Their Bat Hosts and Did Not Co-speciate with Ancient Humans.

All 100+ bedbug species (Cimicidae) are obligate blood-sucking parasites [1, 2]. In general, blood sucking (hematophagy) is thought to have evolved in generalist feeders adventitiously taking blood meals [3, 4], but those cimicid taxa currently considered ancestral are putative host specialists [1, 5]. Bats are believed to be the ancestral hosts of cimicids [1], but a cimicid fossil [6] predates the oldest known bat fossil [7] by >30 million years (Ma). The bedbugs that parasitize humans [1, 8] are host generalists, so their evolution from specialist ancestors is incompatible with the "resource efficiency" hypothesis and only partially consistent with the "oscillation" hypothesis [9-16]. Because quantifying host shift frequencies of hematophagous specialists and generalists may help to predict host associations when vertebrate ranges expand by climate change [17], livestock, and pet trade in general and because of the previously proposed role of human pre-history in parasite speciation [18-20], we constructed a fossil-dated, molecular phylogeny of the Cimicidae. This phylogeny places ancestral Cimicidae to 115 mya as hematophagous specialists with lineages that later frequently populated bat and bird lineages. We also found that the clades, including the two major current urban pests, Cimex lectularius and C. hemipterus, separated 47 mya, rejecting the notion that the evolutionary trajectories of Homo caused their divergence [18-21]. VIDEO ABSTRACT.

Parasites favour intermediate nestling mass and brood size in cliff swallows.

A challenge of life-history theory is to explain why animal body size does not continue to increase, given various advantages of larger size. In birds, body size of nestlings and the number of nestlings produced (brood size) have occasionally been shown to be constrained by higher predation on larger nestlings and those from larger broods. Parasites also are known to have strong effects on life-history traits in birds, but whether parasitism can be a driver for stabilizing selection on nestling body size or brood size is unknown. We studied patterns of first-year survival in cliff swallows (Petrochelidon pyrrhonota) in western Nebraska in relation to brood size and nestling body mass in nests under natural conditions and in those in which hematophagous ectoparasites had been removed by fumigation. Birds from parasitized nests showed highest first-year survival at the most common, intermediate brood-size and nestling-mass categories, but cliff swallows from nonparasitized nests had highest survival at the heaviest nestling masses and no relationship with brood size. A survival analysis suggested stabilizing selection on brood size and nestling mass in the presence (but not in the absence) of parasites. Parasites apparently favour intermediate offspring size and number in cliff swallows and produce the observed distributions of these traits, although the mechanisms are unclear. Our results emphasize the importance of parasites in life-history evolution.

Dispersing hemipteran vectors have reduced arbovirus prevalence.

A challenge in managing vector-borne zoonotic diseases in human and wildlife populations is predicting where epidemics or epizootics are likely to occur, and this requires knowing in part the likelihood of infected insect vectors dispersing pathogens from existing infection foci to novel areas. We measured prevalence of an arbovirus, Buggy Creek virus, in dispersing and resident individuals of its exclusive vector, the ectoparasitic swallow bug (Oeciacus vicarius), that occupies cliff swallow (Petrochelidon pyrrhonota) colonies in western Nebraska. Bugs colonizing new colony sites and immigrating into established colonies by clinging to the swallows' legs and feet had significantly lower virus prevalence than bugs in established colonies and those that were clustering in established colonies before dispersing. The reduced likelihood of infected bugs dispersing to new colony sites indicates that even heavily infected sites may not always export virus to nearby foci at a high rate. Infected arthropods should not be assumed to exhibit the same dispersal or movement behaviour as uninfected individuals, and these differences in dispersal should perhaps be considered in the epidemiology of vector-borne pathogens such as arboviruses.

New family host and records of Acanthocrios furnarii (Cordero & Vogelsang, 1928) (Hemiptera: Cimicidae) from Argentina, and implications in the transmission mechanism of cimicid bugs among birds' nests.

Acanthocrios furnarii (Cordero & Vogelsang, 1928) [Hemiptera: Cimicidae: Haematosiphoninae] is an ectoparasite on avian hosts from Argentina and Uruguay. It has been mostly found in mud nests of Furnarius rufus (Gmelin, 1788) [Aves: Furnariidae], but its true hosts are some of the inquiline birds that use F. rufus nests. These inquiline hosts belong to the families Emberizidae, Hirundinidae, Icteridae, Passeridae, and Troglodytidae. Outside F. rufus mud nests, A. furnarii has been found in nests of other Furnariidae, Hirundinidae, and Passeridae. The present work adds the first nonpasserine host (Falconidae) of A. furnarii, together with new records in La Pampa, Argentina. The transmission mechanism of A. furnarii, together with all other cimicid bugs from Argentina and adjacent countries, is increased considering this new host; and we also take into account the birds that nidificate in nest boxes, the cavity-nesting birds in trees and earth, and the inquiline birds in stick nests of Furnariidae and Psittacidae.

Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity.

Optimal mating frequencies differ between sexes as a consequence of the sexual differentiation of reproductive costs per mating, where mating is normally more costly to females than males. In mating systems where sexual reproduction is costly to females, sexual conflict may cause both direct (i.e. by reducing female fecundity or causing mortality) and indirect (i.e. increased risk of mortality, reduced offspring viability) reductions in lifetime reproductive success of females, which have individual and population consequences. We investigated the direct and indirect costs of multiple mating in a traumatically inseminating (TI) predatory Warehouse pirate bug, Xylocoris flavipes (Reuter) (Hemiptera: Anthocoridae), where the male penetrates the female's abdomen during copulation. This study aimed to quantify the effects of TI on female fecundity, egg viability, the lifetime fecundity schedule, longevity and prey consumption in this cosmopolitan biocontrol agent. We found no difference in the total reproductive output between mating treatments in terms of total eggs laid or offspring viability, but there were significant differences found in daily fecundity schedules and adult longevity. In terms of lifetime reproduction, female Warehouse pirate bugs appear to be adapted to compensate for the costs of TI mating to their longevity.

An enzootic vector-borne virus is amplified at epizootic levels by an invasive avian host.

Determining the effect of an invasive species on enzootic pathogen dynamics is critical for understanding both human epidemics and wildlife epizootics. Theoretical models suggest that when a naive species enters an established host-parasite system, the new host may either reduce ('dilute') or increase ('spillback') pathogen transmission to native hosts. There are few empirical data to evaluate these possibilities, especially for animal pathogens. Buggy Creek virus (BCRV) is an arthropod-borne alphavirus that is enzootically transmitted by the swallow bug (Oeciacus vicarius) to colonially nesting cliff swallows (Petrochelidon pyrrhonota). In western Nebraska, introduced house sparrows (Passer domesticus) invaded cliff swallow colonies approximately 40 years ago and were exposed to BCRV. We evaluated how the addition of house sparrows to this host-parasite system affected the prevalence and amplification of a bird-associated BCRV lineage. The infection prevalence in house sparrows was eight times that of cliff swallows. Nestling house sparrows in mixed-species colonies were significantly less likely to be infected than sparrows in single-species colonies. Infected house sparrows circulated BCRV at higher viraemia titres than cliff swallows. BCRV detected in bug vectors at a site was positively associated with virus prevalence in house sparrows but not with virus prevalence in cliff swallows. The addition of a highly susceptible invasive host species has led to perennial BCRV epizootics at cliff swallow colony sites. The native cliff swallow host confers a dilution advantage to invasive sparrow hosts in mixed colonies, while at the same sites house sparrows may increase the likelihood that swallows become infected.

Off-host aggregation behavior and sensory basis of arrestment by Cimex lectularius (Heteroptera: Cimicidae).

The bed bug, Cimex lectularius, aggregates under filter paper disks previously stained by adults. A multiple choice assay was used to determine differences in aggregation behavior among two strains, multiple lifestages, and levels of starvation. There were no differences in level of aggregation between established and recently derived strains, or among adults and nymphs of different instars. Propensity to aggregate decreased with time since feeding, but preference for stained disks remained high. We also examined which sensory structures mediate aggregation, and whether antennectomy affected movement, orientation, and arrestment under stained disks. Bed bugs that were left intact, blinded, or surgically altered by the removal of probosci or the distal antennal segments exhibited high levels of aggregation under stained disks. However, the removal of the pedicel significantly reduced aggregation compared to intact bugs. Video recordings of movement and orientation by bugs with intact, partial and complete antennectomies demonstrated that neither partial nor complete antennectomies affected walking speed, path straightness, direction of movement or frequency of encounters with either stained or clean disks. However, complete removal of both antennae significantly reduced the percentage of encounters with stained disks that resulted in arrestment. These findings suggest aggregation by bed bugs is a result of arrestment mediated by direct, close-range contact between sensilla on the pedicel and stained disks.

Host and vector movement affects genetic diversity and spatial structure of Buggy Creek virus (Togaviridae).

Determining the degree of genetic variability and spatial structure of arthropod-borne viruses (arboviruses) may help in identifying where strains that potentially cause epidemics or epizootics occur. Genetic diversity in arboviruses is assumed to reflect relative mobility of their vertebrate hosts (and invertebrate vectors), with highly mobile hosts such as birds leading to genetic similarity of viruses over large areas. There are no empirical studies that have directly related host or vector movement to virus genetic diversity and spatial structure. Using the entire E2 glycoprotein-coding region of 377 Buggy Creek virus isolates taken from cimicid swallow bugs (Oeciacus vicarius), the principal invertebrate vector for this virus, we show that genetic diversity between sampling sites could be predicted by the extent of movement by transient cliff swallows (Petrochelidon pyrrhonota) between nesting colonies where the virus and vectors occur. Pairwise F(ST) values between colony sites declined significantly with increasing likelihood of a swallow moving between those sites per 2-day interval during the summer nesting season. Sites with more bird movement between them had virus more similar genetically than did pairs of sites with limited or no bird movement. For one virus lineage, Buggy Creek virus showed greater haplotype and nucleotide diversity at sites that had high probabilities of birds moving into or through them during the summer; these sites likely accumulated haplotypes by virtue of frequent virus introductions by birds. Cliff swallows probably move Buggy Creek virus by transporting infected bugs on their feet. The results provide the first empirical demonstration that genetic structure of an arbovirus is strongly associated with host/vector movement, and suggest caution in assuming that bird-dispersed arboviruses always have low genetic differentiation across different sites.

Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect.

Sexual conflict can produce several evolutionary outcomes, one of which is female-limited trait polymorphism. We examine the African bat bug Afrocimex constrictus (Cimicidae), a species where both sexes are subjected to traumatic intromission from males. We show that males possess female genital structures that in related species ameliorate the costs of traumatic insemination. Moreover, the male form of these structures differs morphologically from the standard female form. Examination of females in our isolated study population revealed a discrete polymorphism in female genitalia. Some females had the typical cimicid form, while others had genitalia that more closely resembled the distinctive male form. Males, as well as females with the distinctive male form, experienced fewer traumatic copulations than the typical female morph. We propose that some females mimic the bizarre male condition in order to reduce the frequency of costly traumatic inseminations. To our knowledge this is the first example of a distinct female-limited genital polymorphism: its nature, as well as its association with traumatic sexual interactions, strongly suggests that sexual conflict underpins this unique phenomenon.

Biology of the bed bugs (Cimicidae).

The cimicids, or bed bugs, belong to a highly specialized hematophagous taxon that parasitizes primarily humans, birds, and bats. Their best-known member is the bed bug, Cimex lectularius. This group demonstrates some bizarre but evolutionarily important biology. All members of the family Cimicidae show traumatic insemination and a suite of female adaptations to this male trait. Cimicids therefore constitute an ideal model system for examining the extreme causes and consequences of sexual selection. Our dual goal in re-examining the extensive literature on this group is to identify issues relevant to pest control, such as dispersal ecology and the recent global spread, and to understand the selective forces that have shaped the unique aspects of this insect's biology.

The incidence of American swallow bugs (Oeciacus vicarius) in barn swallow (Hirundo rustica) colonies in northeast Texas.

The American swallow bug (Oeciacus vicarius) is an important ectoparasite of cliff swallows (Petrochelidon pyrrhonota) and is known to harbor several types of arbovirus. A recent study in northeast Texas suggested that O. vicarius might occur in barn swallows (Hirundo rustica) at rates much higher than previously thought. The purpose of this study was to determine the extent to which barn swallows in northeast Texas are parasitized by O. vicarius and how well this parasite is adapting to this novel host. A sample of 498 nests at 54 colonies was inspected for O. vicarius. Forty colonies (74.1%) were infected, while 310 nests (62.2%) were infected. Large colonies were more likely to be infected than small colonies. Colonies that also contained cliff swallows were more likely to be infected than colonies without cliff swallows. Infection levels in barn swallow nests were comparable to those reported for cliff swallows, though age and sex class ratios differed. Demographic changes among swallow species, including range expansions, increased colony sizes, and more frequent interspecific nesting associations have likely facilitated the movement of O. vicarius from the cliff swallow into a novel host, the barn swallow.

Photophase influence on the reproductive diapause, seasonal morphs, and feeding activity of Euschistus heros (Fabr., 1798) (Hemiptera: Pentatomidae).

Laboratory studies were conducted to verify the influence of photophase on diapause incidence in the Neotropical brown stink bug, Euschistus heros (Fabr., 1798), fed with soybean [Glycine max (L.)] Merrill pods. Nymphs were maintained at three different photophases: 10 h, 12 h, and 14 h, with constant temperature of 25 +/- 1 degree C and relative humidity of 65 +/- 5%. With 14 h, approximately 100% of the adults showed mature reproductive organs; the shoulder (spine) length was significantly greater (2.96 and 2.79 mm for females and males, respectively) than those of bugs maintained at the photophase of 12 h (2.60 mm for females and males) and 10 h (2.59 and 2.53 mm for females and males). At the longer photophase (14 h), E. heros showed better reproductive performance and greater feeding activity than insects reared at 10 h and 12 h; in all photophases bugs tended to reduce feeding from the 1st to the 6th week of life. Body color was considered an unreliable parameter to indicate diapause incidence. However, at 14 h, 60% of the insects were dark brown and 40% were reddish brown. These results indicate that E. heros enters reproductive diapause with photophase of 12 hours or less, showing immature reproductive organs or with intermediate development, with shoulder (spine) less developed and reduced feeding activity.