Polychromophilus spp. (Haemosporida) in Malagasy bats: host specificity and insights on invertebrate vectors

Abstract

BackgroundBats are home to diverse haemosporidian parasites namely Plasmodium and Plasmodium-related. While information is available at a worldwide level, haemosporidian infection in bats from Madagascar is still scarce and recent changes in the taxonomy of the island’s bat fauna, particularly the description of several new species, require a reassessment of previously described patterns, including blood parasite ecology and vectorial transmission.MethodsA sample representing seven of the nine known bat families and 31 of the 46 currently recognized taxa from Madagascar and collected in the western and central portions of the island were screened by PCR for the presence of Polychromophilus. In addition, Nycteribiidae flies parasitizing Miniopteridae and Vespertilionidae were screened for parasites with the aim to better understand aspects of vector transmission. Phylogenetic reconstruction using the mitochondrial cytochrome b encoding gene was used in a Bayesian analysis to examine the relationship between Polychromophilus recovered from Malagasy bats and those identified elsewhere.ResultsPolychromophilus infection was restricted to Miniopterus spp. (Miniopteridae), Myotis goudoti (Vespertilionidae), and Paratriaenops furculus (Rhinonycteridae), with an overall infection rate of 13.5%. Polychromophilus melanipherus was found infecting Miniopterus spp. and P. furculus, whereas Polychromophilus murinus was only recovered from M. goudoti. These two protozoan parasites species were also detected in bat flies species known to parasitize Miniopterus spp. and M. goudoti, respectively. Generalized linear model analyses were conducted to elucidate the effect of species and sex on haemoparasites infection in Miniopterus spp., which revealed that males have higher risk of infection than females and prevalence differed according to the considered Miniopterus host. Molecular screening of nycteribiid flies revealed three positive species for Polychromophilus spp., including Penicillidia sp. (cf. fulvida), Penicillidia leptothrinax, and Nycteribia stylidiopsis. These three fly species are known to parasitize Miniopterus spp. and M. goudoti and should be considered as potential vectors of Polychromophilus spp.ConclusionPhylogenetic analyses demonstrated the existence of at least four distinct clades within the genus Polychromophilus, two of which were documented in the present study. The screening of nycteribiid flies overlaid on the highly diversified genus Miniopterus, provides considerable insight into parasite transmission, with bat infection being associated with their roosting behaviour and the occurrence of specific arthropod vectors.Electronic supplementary materialThe online version of this article (10.1186/s12936-018-2461-8) contains supplementary material, which is available to authorized users.

Diversity, Distribution, and Drivers of Polychromophilus Infection in Malagasy Bats

“…On the basis of the results presented herein including the analysis of seven different families of bats, Polychromophilus infection in Malagasy bats from the eastern portion of the island appears to be limited to two families (Miniopteridae and Vespertilionidae), while the other ve tested families (Pteropodidae, Hipposideridae, Emballonuridae, Myzopodidae, and Molossidae) were negative. Such host-parasite associations are in keeping with previous investigations carried out worldwide [10,17,18,27,43]. To date, 10 out of the 12 species of Miniopterus tested and occurring on Madagascar are infected by P. melanipherus based on morphological or molecular screenings.…”

“…The identi cation of variables controlling the distribution of P. melanipherus was conducted using the MaxEnt software version 3.3.3 k [35]. Modeling was carried out using occurrence records obtained in the present study, as well as another recent study [27]. Environmental variables for each of the capture sites [35,36] included the following nine bioclimatic variables: annual total evapotranspiration, maximum precipitation of the wettest month, minimum precipitation of the driest month, maximum temperature of the warmest month, minimum temperature of the coldest month, mean annual precipitation, mean annual temperature, numbers of months with a positive water balance, and annual water balance).…”

“…This parasite infects different species of Miniopterus without geographic or host species barriers [10,17,43,49]. Apart from Miniopterus spp., Paratriaenops furculus (Rhinonycteridae) has already been reported to be infected with Polychromophilus melanipherus [27], whereas a closely related member of this family, Triaenops menamena, which occurs in sympatry with Paratriaenops furculus in the same day roost sites [45,50] tested negative for this parasite [27].…”

“…fulvida, and Nycteribia stylidiopsis) revealed the presence of Polychromophilus spp. [27]. While no detailed work on the role of Nycteribiidae as vector of Polychromophilus has been achieved on Madagascar, three species of Nycteribiidae, namely Penicillidia lepthothrinax, Nycteribia stylidiopsis and Penicillidia sp.…”

“…and rarely Paratriaenops furculus (Rhinonycteridae) and P. murinus parasitizing Myotis goudoti (Vespertilionidae) [17,27]. While 32 species of bats occurring in the western and the central portion of Madagascar were already screened for the presence of Polychromophilus [16,17,27], knowledge on Polychromophilus in bats occurring in the eastern area is not well-known and aspects on biotic and abiotic drivers of infection is far from complete. In the present study, we explored Polychromophilus diversity and distribution in bats occurring in the oriental portion of the island and predict the potential drivers of Polychromophilus infection across the island based on new and previous records.…”