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Molecular diversity indices of bat ectoparasite species from Serbia and Bosnia and Herzegovina. Standard deviation values (± SD) for haplotype diversity (Hd) and nucleotide diversity (π) are given in parentheses
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Schreiber’s bent-winged bat Miniopterus schreibersii and the greater horseshoe bat Rhinolophus ferrumequinum are widespread and common cavernicolous species across southern Europe that host numerous specialized ectoparasite species. The objective of this study was to characterize the species assemblage, genetic diversity and host specificity of bat...
Contexts in source publication
Context 1
... data were aligned and edited using CodonCodeAligner 4.2.7 (www.codoncode.com) or ClustalW algorithm implemented in MEGA v.6 ( Tamura et al. 2013) and manually adjusted where needed. Ends were trimmed, with the final length given for every gene sequence/species in Table 2. Sequences were collapsed into haplotypes using DnaSP v.6 ( Rozas et al. 2017). ...Context 2
... DNA polymorphism indices for COI and 16S rRNA with the number of sequences used for analyses and their length in each species are given in Table 2. Unique sequences were uploaded to GenBank (accession numbers: N. ...Context 3
... MZ380293-MZ380313; P. conspicua: MZ396953-MZ396964; P. dufourii: MZ389896-MZ389898; S. psi: MZ390121-MZ390126; Ph. biarticulatum: MZ396965-MZ396970; E. euryalis: MZ389890-MZ389895; see S2 file for details). In flies, the number of recovered haplotypes ranged from 21 in N. schmidlii to three in P. dufourii ( Figure 2; Table 2). The highest haplotype diversity (Hd) and nucleotide diversity (π) values were observed in P. conspicua (Hd = 0.722; π = 0.00251), and lowest in Ph. biarticulatum (Hd = 0.289; π = 0.00179). ...Context 4
... haplotypes were detected in both wing mites species ( Figure 2D and 2F), of which five haplotypes in each species were newly reported. Haplotype and nucleotide diversity values were higher in E. euryalis (Hd = 0.147; π = 0.00044, respectively) than in S. psi (Hd = 0.122; π = 0.00035; Table 2). In both flies and wing mites, all haplotype networks show a star-like topology, radiating from a single common haplotype (H1), accounting for a majority of the sample (e.g. ...Context 5
... each ectoparasite species, recovered sequences were compared to those available on GenBank, originating from three previous studies: Bruyndonckx Table 2, Figure 2A), of which four (H1, H4, H7, and H18) corresponded to previously reported haplotypes from Romania and Hungary (McKee et al. 2019). Two haplotypes from the previous studies, H26 from Romania, and H27 from Kenya ( Tortosa et al. 2013) differed considerably from all others (27 and 20 bp from the hypothetical median vector respectively; Figure 2A). ...Context 6
... the mite Spinturnix psi (N = 111), collected from M. schreibersii, six haplotypes were detected (Table 2), of which one matched the only previously reported haplotype for this species (from France, Italy, and Switzerland). In order to merge the haplotypes with those available on GenBank, the sequence was trimmed from 354 bp to 313 bp, which resulted in the loss of H6, thus Figure 2D shows only five haplotypes. ...Context 7
... our study, all three bat fly species collected from M. schreibersii exhibited relatively high genetic diversity, while in the fly Ph. biarticulatum collected from the bat host R. ferrumequinum, it was notably lower (Table 2). ...Context 8
... mites, the genetic diversity of the investigated 16S rRNA gene was similarly low in the species from both hosts ( Table 2, Spinturnix psi and Eyndhovenia euryalis). However, the highly conserved nature of this sequence fragment makes comparing diversity within species at such scales difficult (De Rojas et al. 2002). ...Similar publications
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Citations
... Therefore, few fly species parasitize more than two hosts in cold caves, forming more modules of independent interactions and increasing SS. Roost sharing by hosts is not necessarily related to their sharing of parasitic flies in cold caves, causing flies dependence on their primary hosts for survival (Pejić et al., 2021). Thus, the representativeness of both systems appears in meta-network characterized by Phyllostomus discolor and Nycterophilia fairchildi, which appears fundamental for structuring interactions on a regional scale. ...
Caves provide relatively stable and advantageous roosting sites for bats compared to more open roosts, like tree foliage. This environment may have the drawback of facilitating interactions with their ectoparasites due to the confined spaces. Understanding the structure of interactions between bats, acting as hosts, and bat flies, serving as parasites in cave ecosystems, is a crucial first step in deciphering the roles of each species (pullers and pushers) within the networks that form in subterranean ecosystems. Here, we describe and evaluate the network structures of bat‐fly interactions in two distinct cave systems: cold caves ( n = 10), also known as bat caves, and hot caves ( n = 6). Based on the records of 700 bats from 16 species and 1.412 bat flies from 30 species we uncovered highly distinct topologies comparing hot and cold bat caves that differed also in terms of interactions, specializations, and modularity. We found relatively lower specialization and modularity in hot caves compared to the cold caves, which may be associated to the bat composition and the cave microclimate. Bat flies were highly species‐specific in relation to their bat hosts and dependent on the bats in both hot and cold caves systems. The differences in network structure and at the species level between the bat (cold) and hot caves systems suggest that bat‐fly interactions are shaped by the host species' composition and by the cave system type. Those differences stem from each bat species' adaptation to extreme cave microclimates and their species‐specific roosting behaviors.
Abstract in Portuguese is available with online material.
... Additionally, taxons N. (N) schmidlii, P. conspicua, and Ph. biarticulatum are associated with three species of the genus Rhinolophus and with M. schreibersii, showing a similar shelter preference [192,193]. ...
Current taxonomical keys are essential for better biodiversity knowledge. Moreover, accurate identification of groups of organisms known to act as disease vectors is vital in today's world of change and the spread of zoonotic disease threats. This is especially relevant to bats and their parasites, given the events of recent years. The available keys of European Nycteribiidae (Diptera) are outdated and do not cover all the species currently known from Europe. Therefore, a summary key of 16 European species is provided in this paper. Based on published data from Europe, a total of 173 host-parasite interactions were observed between 16 European bat fly species and 31 host species (bats). The highest number of associations with different host species and the lowest specialization was observed in Penicillidia (P.) dufourii dufourii, followed by Nycteribia (N.) kolenatii, N. (N.) schmidlii and Phthiridium biarticulatum; most of the other species also had low specialization. Most species are oligoxenous, parasitizing on several families, and three species are stenoxenosus. Only one nycteribiid species, Basilia daganiae, was linked with only one host (Pipistrellus kuhlii). Myotis myotis has 12 associations with different bat fly species, followed by Plecotus auritus and Myotis daubentonii with 12 associations. A relatively high number of bat species were associated with only one bat fly species. In addition, we performed a bipartite analysis complemented by network indices and host specificity at the species and whole network levels, yielding new information in terms of ecology and the host-parasite relationships related to these groups of potential vectors (Nycteribiidae) and sources of zoonoses (bats). The parasite-host network composed of 16 nycteribiid species and 31 bat host species was characterized by a low network level specialization, low modularity, and low nestedness. Our findings also suggest a high probability of associated Nycteribiidae in bat taxa with a similar roosting ecology and phylogenetic relationship.
... One difficulty of bat fly research for understudied regions is the identification of specimens based on a few taxonomic publications developed more than half a century ago [31][32][33][34] from a limited and incomplete pool of species, a problem more widely known as the Linnean shortfall [35,36]. Occurrences of cryptic species and phenotypic plasticity represent additional difficulties to morphologically distinguish bat fly species [33,37]. DNA barcoding was thus recommended as a potential approach to reliably separate bat fly species [13,37]. ...
... Occurrences of cryptic species and phenotypic plasticity represent additional difficulties to morphologically distinguish bat fly species [33,37]. DNA barcoding was thus recommended as a potential approach to reliably separate bat fly species [13,37]. In this study, we sought to determine the species richness, phylogenetic relationships, and host association patterns of bat flies found on 11 cavernicolous bat species occurring in China, using both morphological and DNA barcoding approaches. ...
... B and C, respectively, but revealed to be intraspecific variations by DNA barcoding results. Therefore, as suggested by some recent studies [13,37], we advocate identifying bat fly species using morphological characteristics with the support of DNA barcoding to discern bat-bat fly associations accurately in future studies. In addition to genetic data, provision of high-quality photos and formal species description with the development of new taxonomic keys will be crucial resources for efficient bat fly classification, which are especially important for understudied regions potentially with many undescribed species. ...
Background
Understanding 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.
Methods
We 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.
Results
We 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.
Conclusions
The 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.
Graphical Abstract
Background
Haemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.
Methods
We collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).
Results
Polychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.
Conclusions
The results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.
Graphical Abstract
