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01.12.2012 | Research | Ausgabe 1/2012 Open Access

Malaria Journal 1/2012

The evolutionary host switches of Polychromophilus: a multi-gene phylogeny of the bat malaria genus suggests a second invasion of mammals by a haemosporidian parasite

Zeitschrift:
Malaria Journal > Ausgabe 1/2012
Autoren:
Fardo Witsenburg, Nicolas Salamin, Philippe Christe
Wichtige Hinweise

Electronic supplementary material

The online version of this article (doi:10.​1186/​1475-2875-11-53) contains supplementary material, which is available to authorized users.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

FW collected the samples, carried out the molecular work, performed the phylogenetic analyses and drafted the manuscript. NS participated in the phylogenetic analyses. PC conceived the study, collected the samples and interpreted the results. All authors read and approved the final manuscript.

Abstract

Background

The majority of Haemosporida species infect birds or reptiles, but many important genera, including Plasmodium, infect mammals. Dipteran vectors shared by avian, reptilian and mammalian Haemosporida, suggest multiple invasions of Mammalia during haemosporidian evolution; yet, phylogenetic analyses have detected only a single invasion event. Until now, several important mammal-infecting genera have been absent in these analyses. This study focuses on the evolutionary origin of Polychromophilus, a unique malaria genus that only infects bats (Microchiroptera) and is transmitted by bat flies (Nycteribiidae).

Methods

Two species of Polychromophilus were obtained from wild bats caught in Switzerland. These were molecularly characterized using four genes (asl, clpc, coI, cytb) from the three different genomes (nucleus, apicoplast, mitochondrion). These data were then combined with data of 60 taxa of Haemosporida available in GenBank. Bayesian inference, maximum likelihood and a range of rooting methods were used to test specific hypotheses concerning the phylogenetic relationships between Polychromophilus and the other haemosporidian genera.

Results

The Polychromophilus melanipherus and Polychromophilus murinus samples show genetically distinct patterns and group according to species. The Bayesian tree topology suggests that the monophyletic clade of Polychromophilus falls within the avian/saurian clade of Plasmodium and directed hypothesis testing confirms the Plasmodium origin.

Conclusion

Polychromophilus' ancestor was most likely a bird- or reptile-infecting Plasmodium before it switched to bats. The invasion of mammals as hosts has, therefore, not been a unique event in the evolutionary history of Haemosporida, despite the suspected costs of adapting to a new host. This was, moreover, accompanied by a switch in dipteran host.
Zusatzmaterial
Additional file 1: Species name, host and accession numbers of sequences retrieved from GenBank for the phylogenetic reconstructions. This table contains additional host information and the GenBank accession numbers of all genes used for the phylogenetic analyses. Not all gene sequences are available for all species, missing sequences are denoted by '-'. (XLS 36 KB)
12936_2011_2057_MOESM1_ESM.XLS
Additional file 2: Changing topologies for alternative rooting methods. Changing topologies acquired by different methods of phylogenetic reconstruction. Irrespective of the root, Polychromophilus remains nested within the sauropsid Plasmodium clade. a. The original best tree from maximum likelihood reconstruction, but now rooted with the mammalian Plasmodium/Hepatocystis, as suggested by Outlaw and Ricklefs [ 16]. Topologies b. and c. are acquired using a relaxed molecular clock with no predefined root, GTR + Γ + I substitution model, 20 million generations sampling every 2,000 generations and two independent MCMC runs using BEAST. All nodes have clade credibilities > 0.5 b. Topology acquired with the Yule tree prior and an exponential relaxed clock. c. Topology acquired with the birth-death tree prior and a log-normal relaxed clock. The different haemosporidian clades are represented by the coloured triangles. The clade height represents the number of containing taxa. (PDF 164 KB)
Additional file 3: A topology rooted with Babesia provides little information. The amino acid alignment provides too little contrast to construct a tree with high support as most nodes are unsupported. A very long branch separates the Babesia species from all Haemosporida. Shown is the best tree of a ML analysis using a JTT + Γ + I substitution model and bootstrapping a 1,000 times. Closed dots: bootstrap value > 90; Open dots: bootstrap values > 50. (PDF 65 KB)
12936_2011_2057_MOESM3_ESM.PDF
Authors’ original file for figure 1
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Authors’ original file for figure 2
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Authors’ original file for figure 3
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