An eco-epidemiological study of Morbilli-related paramyxovirus infection in Madagascar bats reveals host-switching as the dominant macro-evolutionary mechanism

Abstract

An eco-epidemiological investigation was carried out on Madagascar bat communities to better understand the evolutionary mechanisms and environmental factors that affect virus transmission among bat species in closely related members of the genus Morbillivirus, currently referred to as Unclassified Morbilli-related paramyxoviruses (UMRVs). A total of 947 bats were investigated originating from 52 capture sites (22 caves, 18 buildings, and 12 outdoor sites) distributed over different bioclimatic zones of the island. Using RT-PCR targeting the L-polymerase gene of the Paramyxoviridae family, we found that 10.5% of sampled bats were infected, representing six out of seven families and 15 out of 31 species analyzed. Univariate analysis indicates that both abiotic and biotic factors may promote viral infection. Using generalized linear modeling of UMRV infection overlaid on biotic and abiotic variables, we demonstrate that sympatric occurrence of bats is a major factor for virus transmission. Phylogenetic analyses revealed that all paramyxoviruses infecting Malagasy bats are UMRVs and showed little host specificity. Analyses using the maximum parsimony reconciliation tool CoRe-PA, indicate that host-switching, rather than co-speciation, is the dominant macro-evolutionary mechanism of UMRVs among Malagasy bats.

Figure 1. PVs detection rates among the sites sampled on Madagascar.

Only sites containing positive bats are represented. Abbreviations refer to the names of sampling sites (e.g. ANDRF for “Andrafiabe”). n, numerator = the number of individuals that tested positive for PVs and denominator = the number of individuals tested. Provincial capitals are indicated by black squares. QGIS, an open-source GIS software (http://qgis.osgeo.org/en/site/), was used to generate the map for visualizing bioclimatic regions of Madagascar proposed by Cornet.

Figure 2. Proportion of infected bats depending on species diversity at each sampling site and the context of the where the samples were collected.

Individual outlying data points are displayed as circles.

Figure 3. Phylogeny of the UMRVs detected in bats from Madagascar.

A global phylogeny of 99 partial L-gene sequences calculated in 50,000,000 iterations in MrBayes with the GTR+G evolutionary model and a 10% burn-in rooted with a Mumps virus sequence (GenBank number AY309060). Only Bayesian with posterior probabilities >0.7 were represented. Host switching events were highlighted in blue and host-specificity for bats sharing the same sites in green. Bat species occurring at distant sites are highlighted in red. Bats living at distant sites and hosting with low level of UMRVs nucleotide similarity are highlighted in yellow.

Figure 4

The first preferred reconstruction with the first best-cost model fit of the co-evolutionary history for the set of (A) 24 OTUs and (B) 39 OTUs and associated bat-species retrieved from CoRe-PA software. Host tree is represented in black; parasite tree is represented in grey.

Figure 5

Frequency of co-speciation (A) and host-switches (B) events for the set of 24 OTUs obtained by random reconstructions. The number of co-speciation and host-switches events expected in the most parsimonious reconstructions by CoRe-PA, 8 and 15, respectively (framed in red; also in Table 3) were compared to the random reconstructions events below. The macro-evolutionary events showing lower random reconstruction events than expected (8 or 15) was determined as the predominant event.