Disease in the dark: molecular characterization of Polychromophilus murinus in temperate zone bats revealed a worldwide distribution of this malaria‐like disease

Abstract

For a better understanding of the complex coevolutionary processes between hosts and parasites, accurate identification of the actors involved in the interaction is of fundamental importance. Blood parasites of the Order Haemosporidia, responsible for malaria, have become the focus of a broad range of studies in evolutionary biology. Interestingly, molecular-based studies on avian malaria have revealed much higher species diversity than previously inferred with morphology. Meanwhile, studies on bat haemosporidian have been largely neglected. In Europe, only one genus (Polychromophilus) and two species have been morphologically described. To evaluate the presence of potential cryptic species and parasite prevalence, we undertook a molecular characterization of Polychromophilus in temperate zone bats. We used a nested-PCR approach on the cytochrome b mitochondrial gene to detect the presence of parasites in 237 bats belonging to four different species and in the dipteran bat fly Nycteribia kolenatii, previously described as being the vector of Polychromophilus. Polychromophilus murinus was found in the four bat species and in the insect vector with prevalence ranging from 4% for Myotis myotis to 51% for M. daubentoni. By sequencing 682 bp, we then investigated the phylogenetic relationships of Polychromophilus to other published malarial lineages. Seven haplotypes were found, all very closely related, suggesting the presence of a single species in our samples. These haplotypes formed a well-defined clade together with Haemosporidia of tropical bats, revealing a worldwide distribution of this parasite mostly neglected by malarial studies since the 1980s.

Rerooting the evolutionary tree of malaria parasites

“…The two major subgroups are clearly associated with vertebrate host: mammalian Plasmodium and Hepatocystis versus avian/reptilian Plasmodium and avian Leucocytozoon, Haemoproteus, and Parahaemoproteus. The chiropteran (bat) parasites Polychromophilus evidently were derived from parasites of birds or reptiles (3,20). Increasing the taxon sampling in the ingroup and in the putative outgroup (i.e., Leucocytozoon) for the mitochondrial cyt b gene (for which large samples are available) and using the same outgroup-free rooting approach also places Leucocytozoon inside the hemosporidian phylogeny, in this case as sister to Haemoproteus, which together are sister to Parahaemoproteus (Figs.…”

Bats as Potential Reservoir Hosts for Vector-Borne Diseases

“…A total of 34 % (n ¼ 70) was infected with Plasmodium murinus. In detail, Myotis daubentonii was the most parasitized species (51 %), followed by Eptesicus serotinus (11 %), Nyctalus noctula (7 %) and Myotis myotis (4 %) (Megali et al 2011). The prevalence (P) of P. murinus in M. daubentonii was twice as great as found by Gardner and Molyneux (1988) in England and Scotland.…”

“…With the exception of Rayella, all haemosporidia genera are known to infect insectivorous bats in temperate and tropical regions (Duval et al 2012). Megali et al (2011) investigated 237 bats of four species from Switzerland to obtain a better understanding of the complex co-evolutionary processes between hosts and parasites. A total of 34 % (n ¼ 70) was infected with Plasmodium murinus.…”

Epidemiological traits of the malaria-like parasite Polychromophilus murinus in the Daubenton¿s bat Myotis daubentonii

“…have seen a particular rise in attention. The increasing ease and efficiency of molecular techniques has facilitated the detection of these parasites, enabling studies on its prevalence [5,6], phylogenetic origins [7] and the discovery of new species [8]. However its development in a host population both through time and between host classes and other ecological measures are lacking, keeping large parts of its biology still a mystery.…”

“…The aim of the current study is to describe these parameters for a temperate-zone member of the Polychromophilus genus, P. murinus. Its type host is Vespertilio murinus, but an important reservoir species seems to be Myotis daubentonii, the Daubenton's bat, a common bat species spread across the Palearctic [1,6,9].…”