Carl W. Dick

High host specificity of obligate ectoparasites

Abstract 1. Host specificity is the degree to which a parasite species occurs in association with a host species.

Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae)

Recently, a growing number Bartonella spp. have been identified as causative agents for a broadening spectrum of zoonotic diseases, emphasizing their medical importance. Many mammalian reservoirs and vectors however are still unknown, hindering our understanding of pathogen ecology and obscuring epidemiological connections. New Bartonella genotypes were detected in a global sampling of 19 species of blood-feeding bat flies (Diptera, Hippoboscoidea, Nycteribiidae, Streblidae) from 20 host bat species, suggesting an important role of bat flies in harboring bartonellae. Evolutionary relationships were explored in the context of currently known Bartonella species and genotypes. Phylogenetic and gene network analyses point to an early evolutionary association and subsequent radiation of bartonellae with bat flies and their hosts. The recovery of unique clades, uniting Bartonella genotypes from bat flies and bats, supports previous ideas of these flies potentially being vectors for Bartonella. Presence of bartonellae in some female bat flies and their pupae suggests vertical transmission across developmental stages. The specific function of bartonellae in bats and bat flies remains a subject of debate, but in addition to pathogenic interactions, parasitic, mutualistic, or reservoir functions need to be considered.

Parasitism by bat flies (Diptera: Streblidae) on neotropical bats : effects of host body size, distribution, and abundance

We examined the correlations between prevalence (proportion of infested individuals), mean intensity (number of parasites per infested individual), and the number of bat fly species parasitizing bats in Venezuela with host body mass, distribution, and abundance. Of 133 bat species sampled, 53 species in six families were captured frequently enough to allow estimation of their parasite loads. Over all species and six families, prevalence and mean intensity were uncorrelated with these variables, but the number of fly species was correlated with host body mass. Correlations of parasitism with body mass were strengthened among the 44 species of Phyllostomidae. Earlier studies showed that bat roosting habits influence their parasitism by bat flies with more permanent, enclosed roosts being with heavier parasitism. Multiple regressions of all measures of parasitism showed that roosting habits and host body mass, respectively, were the first variables to enter stepwise regressions, together accounting for 20–43% of the variation in measures of parasitism. Lack of correlation between proxies of distribution and abundance with parasitism is taken to indicate that proximate factors such as host-as-habitat, social groupings, and roost microhabitat take precedence over species-wide attributes like commonness and ubiquity.

Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism.

Environmental conditions, including anthropogenic disturbance, can significantly alter host and parasite communities. Yet, our current knowledge is based mainly on endoparasites, while ectoparasites remain little studied. We studied the indirect effects of anthropogenic disturbance (human population density) and climate (temperature, precipitation and elevation) on abundance of highly host-specific bat flies in four Neotropical bat species across 43 localities in Venezuela. We formulated a set of 11 a priori hypotheses that included a combination of the two effectors and host species. Statistically, each of these hypotheses was represented by a zero-inflated negative binomial mixture model, allowing us to control for excess zeros in the data. The best model was selected using Akaikes information criteria. Fly abundance was affected by anthropogenic disturbance in Artibeus planirostris, Carollia perspicillata and Pteronotus parnellii, but not Desmodus rotundus. Climate affected fly abundance in all bat species, suggesting mediation of these effects via the host or by direct effects on flies. We conclude that human disturbance may play a role in shaping bat-bat fly interactions. Different processes could determine fly abundance in the different bat species.

Pupal Deposition and Ecology of Bat Flies (Diptera: Streblidae): Trichobius sp. (Caecus Group) in a Mexican Cave Habitat

Abstract We studied the deposition of pupae of the winged bat fly Trichobius sp. (caecus group; Diptera), an ectoparasite of Natalus stramineus (Chiroptera, Natalidae), in a natural cave in Tamaulipas, Mexico. For the first time, we show a strong spatial segregation of populations of a streblid bat fly at different stages of development. Using molecular techniques we were able to match developmental stages to adults. Only 5 pupae were present in the main bat roosts. The overwhelming majority occurred exclusively in the bat flyway passages at a considerable distance from roosting bats. Pupal density corresponded positively with the average flight height of bats in the cave passage. Taken together, observations suggest that these ectoparasites must actively seek out their hosts by moving onto passing or roosting bats. The scarceness of pupae in the main roost may be dictated by environmental constraints for their development. The estimated population of viable pupae far exceeds the population of imagoes on the bats, and predation on adults by spiders is common.

An excess of males: skewed sex ratios in bat flies (Diptera: Streblidae)

Ectoparasitic insects often exhibit female-biased sex ratios, a pattern usually explained by greater female longevity and the likelihood that smaller, more active males will disperse or be groomed off the host. Theory predicts that unbalanced sex ratios should favor males when resources are abundant and predictable, and when males are the dispersing sex. Sex ratios of streblid bat flies were evaluated based on a large biodiversity survey in Venezuela–more than 25,000 bats representing 130 species were searched for flies, yielding more than 36,500 bat flies of 116 species. These samples allowed us to analyze sex ratios in 112 bat fly metapopulations. Our results indicate that fully one-third of these metapopulations were significantly male-biased. Traditional explanations for sex-ratio bias, such as sampling effects, unequal longevity between the sexes, and differential dispersal capability are refuted for bat flies in favor of an alternative hypothesis—selective host grooming. Because host grooming is the principal cause of mortality for these slow-reproducing parasites, and because females are larger than males and gravid for a significant portion of their adult life, host grooming activity is more likely to kill or remove females than males. Incomplete understanding of population dynamics, such as mating behavior, dispersal, and reproductive success, cloud applications of male-biased sex ratios in bat flies to support or refute theoretical predictions. Population studies of mating competition and sex-related dispersal dynamics of this male-dominated group should yield important insights into sex ratio theory.

Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia

BackgroundPopulation-level studies of parasites have the potential to elucidate patterns of host movement and cross-species interactions that are not evident from host genealogy alone. Bat flies are obligate and generally host-specific blood-feeding parasites of bats. Old-World flies in the family Nycteribiidae are entirely wingless and depend on their hosts for long-distance dispersal; their population genetics has been unstudied to date.MethodsWe collected a total of 125 bat flies from three Pteropus species (Pteropus vampyrus, P. hypomelanus, and P. lylei) from eight localities in Malaysia, Cambodia, and Vietnam. We identified specimens morphologically and then sequenced three mitochondrial DNA gene fragments (CoI, CoII, cytB; 1744 basepairs total) from a subset of 45 bat flies. We measured genetic diversity, molecular variance, and population genetic subdivision (FST), and used phylogenetic and haplotype network analyses to quantify parasite genetic structure across host species and localities.ResultsAll flies were identified as Cyclopodia horsfieldi with the exception of two individuals of Eucampsipoda sundaica. Low levels of population genetic structure were detected between populations of Cyclopodia horsfieldi from across a wide geographic range (~1000 km), and tests for isolation by distance were rejected. AMOVA results support a lack of geographic and host-specific population structure, with molecular variance primarily partitioned within populations. Pairwise FST values from flies collected from island populations of Pteropus hypomelanus in East and West Peninsular Malaysia supported predictions based on previous studies of host genetic structure.ConclusionsThe lack of population genetic structure and morphological variation observed in Cyclopodia horsfieldi is most likely due to frequent contact between flying fox species and subsequent high levels of parasite gene flow. Specifically, we suggest that Pteropus vampyrus may facilitate movement of bat flies between the three Pteropus species in the region. We demonstrate the utility of parasite genetics as an additional layer of information to measure host movement and interspecific host contact. These approaches may have wide implications for understanding zoonotic, epizootic, and enzootic disease dynamics. Bat flies may play a role as vectors of disease in bats, and their competence as vectors of bacterial and/or viral pathogens is in need of further investigation.

Evolution, multiple acquisition, and localization of endosymbionts in bat flies (Diptera: Hippoboscoidea: Streblidae and Nycteribiidae).

ABSTRACT Bat flies are a diverse clade of obligate ectoparasites on bats. Like most blood-feeding insects, they harbor endosymbiotic prokaryotes, but the origins and nature of these symbioses are still poorly understood. To expand the knowledge of bacterial associates in bat flies, the diversity and evolution of the dominant endosymbionts in six of eight nominal subfamilies of bat flies (Streblidae and Nycteribiidae) were studied. Furthermore, the localization of endosymbionts and their transmission across developmental stages within the family Streblidae were explored. The results show diverse microbial associates in bat flies, with at least four ancestral invasions of distantly related microbial lineages throughout bat fly evolution. Phylogenetic relationships support the presence of at least two novel symbiont lineages (here clades B and D), and extend the geographic and taxonomic range of a previously documented lineage (“Candidatus Aschnera chinzeii”; here clade A). Although these lineages show reciprocally monophyletic clusters with several bat fly host clades, their phylogenetic relationships generally do not reflect current bat fly taxonomy or phylogeny. However, within some endosymbiont clades, congruent patterns of symbiont-host divergence are apparent. Other sequences identified in this study fall into the widely distributed, highly invasive, insect-associated Arsenophonus lineage and may be the result of symbiont replacements and/or transient infections (here clade C). Vertical transmission of endosymbionts of clades B and D is supported by fluorescent signal (fluorescent in situ hybridization [FISH]) and microbial DNA detection across developmental stages. The fluorescent bacterial signal is consistently localized within structures resembling bacteriomes, although their anatomical position differs by host fly clade. In summary, the results suggest an obligate host-endosymbiont relationship for three of the four known symbiont clades associated with bat flies (clades A, B, and D).

Effects of Prior Infestation on Host Choice of Bat Flies (Diptera: Streblidae)

Abstract Experimental approaches provide insight into the dynamics of species competition and coexistence, but studies of ectoparasitic arthropods are rare. Host choice experiments were undertaken in Amazonian Peru, by using obligate bat fly parasites of Seba’s short-tailed bat, Carollia perspicillata (L.). The fly species Trichobius joblingi Wenzel strongly preferred clean hosts to those previously infested with individuals of T. joblingi. Abundance thresholds may limit conspecific parasites on host individuals, and similar morphologies and habitat use may increase intraspecific competition among individuals of T. joblingi. T. joblingi did not distinguish between clean hosts and those previously infested with flies of another species, Speiseria ambigua Kessel. Results suggest that the presence of a morphologically dissimilar species does not preclude subsequent colonization. Differential microhabitat selection, aided by adaptive morphology, may facilitate species coexistence among ectoparasitic bat fly species.

Assessing host specificity of obligate ectoparasites in the absence of dispersal barriers

Host specificity is a characteristic property of parasite-host associations and often is high among those involving obligate or permanent parasites. While many parasites are highly host-specific under natural conditions, specificity may break down in the absence of dispersal barriers. We tested the host specificity of obligate and permanent blood-feeding bat parasites (Hemiptera: Polyctenidae) under experimental conditions where parasite dispersal barriers had been removed. Under these conditions, parasites not only readily accepted a secondary host species but also remained there when a primary host was immediately available. Experiments with bat bugs and observations of streblid bat flies suggest that specificity may at least temporarily break down when dispersal barriers are removed. To affect long-term coevolutionary patterns, such transfers would necessarily entail the establishment of viable parasite populations on secondary host species.