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Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations.

ABSTRACT: The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position-induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.

SUBMITTER: Haelewaters D

PROVIDER: S-EPMC6145224 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundBat flies (Diptera: Nycteribiidae and Streblidae) are obligate, blood-sucking ectoparasites of bats with specialized morphology, life-cycle and ecology. Bat flies are occasionally infected by different species of Laboulbeniales (Fungi: Ascomycota), microscopic fungal ectoparasites belonging to three genera: Arthrorynchus spp. are restricted to the Eastern Hemisphere, while species of Gloeandromyces and Nycteromyces occur on Neotropical bat flies. Little is known about the distribution and host specificity of Arthrorynchus spp. on bat flies. In this study, we focused on sampling bat flies from the cave-dwelling bat species Miniopterus schreibersii. Bat and ectoparasite collection took place in Albania, Croatia, Hungary, Italy, Portugal, Slovakia, Spain and Switzerland. Flies were inspected for Laboulbeniales infections.ResultsSix hundred sixty seven bat flies of five species were collected: Nycteribia latreillii, N. pedicularia, N. schmidlii, Penicillidia conspicua, and P. dufourii. Laboulbeniales infection was observed on 60 specimens (prevalence = 9%). Two Laboulbeniales species, Arthrorhynchus eucampsipodae and A. nycteribiae, were present on three bat fly species. All observations of A. eucampsipodae were on N. schmidlii, and A. nycteribiae was present on P. conspicua and P dufourii. Arthrorhynchus eucampsipodae is, for the first time, reported from Slovakia and Spain. Arthrorhynchus nycteribiae represents a new country record for Portugal and Slovakia. There were no significant differences among infection rates in different countries. Females of N. schmidlii showed a higher infection rate than males with an observable trend (P = 0.0502). No sex differences in infection rate for P. conspicua and P. dufourii were detected. Finally, thallus density was significantly lower in N. schmidlii compared to P. conspicua and P. dufourii.ConclusionsWith this study, we contribute to the knowledge of the geographical distribution and host specificity of Laboulbeniales fungi associated with ectoparasitic bat flies within Europe. We discuss parasite prevalence and host specificity in the light of our findings and the available literature. Penicillidia conspicua is unambiguously the main host species for A. nycteribiae based on our and previous findings. Differences in parasite intensity and sex-biased infections of the fungi are possible depending on the species.

Project description:BackgroundBat flies (Streblidae and Nycteribiidae) are among the most specialized families of the order Diptera. Members of these two related families have an obligate ectoparasitic lifestyle on bats, and they are known disease vectors for their hosts. However, bat flies have their own ectoparasites: fungi of the order Laboulbeniales. In Europe, members of the Nycteribiidae are parasitized by four species belonging to the genus Arthrorhynchus. We carried out a systematic survey of the distribution and fungus-bat fly associations of the genus in central Europe (Hungary, Romania).ResultsWe encountered the bat fly Nycteribia pedicularia and the fungus Arthrorhynchus eucampsipodae as new country records for Hungary. The following bat-bat fly associations are for the first time reported: Nycteribia kolenatii on Miniopterus schreibersii, Myotis blythii, Myotis capaccinii and Rhinolophus ferrumequinum; Penicillidia conspicua on Myotis daubentonii; and Phthiridium biarticulatum on Myotis capaccinii. Laboulbeniales infections were found on 45 of 1,494 screened bat flies (3.0%). We report two fungal species: Arthrorhynchus eucampsipodae on Nycteribia schmidlii, and A. nycteribiae on N. schmidlii, Penicillidia conspicua, and P. dufourii. Penicillidia conspicua was infected with Laboulbeniales most frequently (25%, n = 152), followed by N. schmidlii (3.1%, n = 159) and P. dufourii (2.0%, n = 102). Laboulbeniales seem to prefer female bat fly hosts to males. We think this might be due to a combination of factors: female bat flies have a longer life span, while during pregnancy female bat flies are significantly larger than males and accumulate an excess of fat reserves. Finally, ribosomal DNA sequences for A. nycteribiae are presented.ConclusionsWe screened ectoparasitic bat flies from Hungary and Romania for the presence of ectoparasitic Laboulbeniales fungi. Arthrorhynchus eucampsipodae and A. nycteribiae were found on three species of bat flies. This study extends geographical and host ranges of both bat flies and Laboulbeniales fungi. The sequence data generated in this work contribute to molecular phylogenetic studies of the order Laboulbeniales. Our survey shows a complex network of bats, bat flies and Laboulbeniales fungi, of which the hyperparasitic fungi are rare and species-poor. Their host insects, on the other hand, are relatively abundant and diverse.

Project description:BackgroundUnderstanding the interactions between bat flies and host bats offer us fundamental insights into the coevolutionary and ecological processes in host-parasite relationships. Here, we investigated the identities, host specificity, and patterns of host association of bat flies in a subtropical region in East Asia, which is an understudied region for bat fly research.MethodsWe used both morphological characteristics and DNA barcoding to identify the bat fly species found on 11 cavernicolous bat species from five bat families inhabiting Hong Kong. We first determined the phylogenetic relationships among bat fly species. Then, we elucidated the patterns of bat-bat fly associations and calculated the host specificity of each bat fly species. Furthermore, we assembled the mitogenomes of three bat fly species from two families (Nycteribiidae and Streblidae) to contribute to the limited bat fly genetic resources available.ResultsWe examined 641 individuals of bat flies and found 20 species, of which many appeared to be new to science. Species of Nycteribiidae included five Nycteribia spp., three Penicillidia spp., two Phthiridium spp., one Basilia sp., and one species from a hitherto unknown genus, whereas Streblidae included Brachytarsina amboinensis, three Raymondia spp., and four additional Brachytarsina spp. Our bat-bat fly association network shows that certain closely related bat flies within Nycteribiidae and Streblidae only parasitized host bat species that are phylogenetically more closely related. For example, congenerics of Raymondia only parasitized hosts in Rhinolophus and Hipposideros, which are in two closely related families in Rhinolophoidea, but not other distantly related co-roosting species. A wide spectrum of host specificity of these bat fly species was also revealed, with some bat fly species being strictly monoxenous, e.g. nycteribiid Nycteribia sp. A, Phthiridium sp. A, and streblid Raymondia sp. A, while streblid B. amboinensis is polyxenous.ConclusionsThe bat fly diversity and specificity uncovered in this study have shed light on the complex bat-bat fly ecology in the region, but more bat-parasite association studies are still needed in East Asian regions like China as a huge number of unknown species likely exists. We highly recommend the use of DNA barcoding to support morphological identification to reveal accurate host-ectoparasite relationships for future studies.

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Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations.

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