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Mitochondrial genes support a common origin of rodent malaria parasites and Plasmodium falciparum's relatives infecting great apes

Samuel Blanquart123* and Olivier Gascuel1

Author Affiliations

1 Méthodes et Algorithmes pour la Bioinformatique, LIRMM, UMR 5506, CNRS-Université de Montpellier 2, 161 rue Ada, 34392 Montpellier Cedex 5, France

2 Goldman Group, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK

3 Equipe Bonsai, Institut National de Recherche en Informatique et en Automatique, INRIA Lille Nord Europe, 40 avenue Halley, 59650 Villeneuve d'Ascq, France

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BMC Evolutionary Biology 2011, 11:70  doi:10.1186/1471-2148-11-70

Published: 15 March 2011

Additional files

Additional file 1:

Supplementary Table S1, Accession numbers of 33 mitochondrial genomes, species and host names. Accession numbers of 33 complete mitochondrial genomes of Haemosporidian parasites, parasite names, and host names retrieved from NCBI annotations (b: host names complemented from Leclerc et al. 2004 [11]). "P.": Plasmodium species, "Ha.": Haemoproteus species, "Pa.": Parahaemoproteus species, "L.": Leucocytozoon species.

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Additional file 2:

Supplementary Figure S1, Saturation plot of codon positions. Saturation plot of codon positions of the 33 taxa and 3 concatenated genes data set, computed with a Bio++ script [80]. Each dot represents the comparison of the similarity distance (y coordinate) versus the tree distance (x coordinate), for a pair of taxa. Tree branch lengths were estimated under the GTRnt + Γ4 model (PhyloBayes 3.0, [43]), for 3 data sets corresponding to each codon position, and using the tree topology estimated from the whole nucleotide data set (Figure 2).

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Additional file 3:

Supplementary Table S2, Analyses of the 33 taxa and 3 mitochondrial gene data sets. Dependency of clade support on codon positions ("Cod. pos."), amino-acid translation and on assumptions of various probabilistic models of substitution (GTRnt, GTRaa and JTT: single matrix model, CAT: site heterogeneous mixture model, BP: time heterogeneous model). Rates across site model components are defined as + Γ4 + I under maximum-likelihood (ML) and as + Γ4 under Bayesian (BI) methods. Cells display support as [PP, SH, BS], with PP: posterior probability (BI), SH: Shimodaira-Hasegawa-like support (ML), and BS: bootstrap support (ML). "*": not applicable. Main lineages of mammal parasites are defined according to their host preference: "Rodent", "Primate" and "Great Ape" (see Additional file 1, Table S1).

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Additional file 4:

Supplementary Table S3, Fit of Bayesian models. Cross-validation estimations of the fit of Bayesian models to the 33 taxa and the three concatenated gene data sets. Models applied to the nucleotide and amino-acid data set are compared to the best fitting ML models, GTRnt + Γ4 and JTT + Γ4, respectively. Models are defined according to their components. Substitution model: GTRnt, GTRaa, MtREV and JTT, exchange rate parameters; CAT, UL2 and UL3, site heterogeneous mixture models. Rates across sites models: + Γ4, discretized gamma rates (Yang 1994, [42]); +COV, covarion model (Tuffley and Steel 1998, [71]).

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Additional file 5:

Supplementary Table S4, p-values of posterior predictive tests performed on the 33 taxa and 3 mitochondrial gene data sets. Data sets were analyzed under various probabilistic models of substitution (GTRnt, GTRaa and JTT: single matrix model, CAT: site heterogeneous mixture model, BP: time heterogeneous model, + Γ4: Rates across site model component). Posterior predictive test "Composition" measures compositional heterogeneity across taxa, "Site Diversity" and "Homoplasy" measure the level of saturation of the phylogenetic signal. "Cod. pos.": codon positions. "*": not applicable.

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Additional file 6:

Supplementary Figure S2, Phylogenetic tree of first and second codon positions analyzed under CAT + GTR + Γ4. Bayesian phylogenetic reconstruction using PhyloBayes 3.0 [43]. The CAT + GTRnt + Γ4 substitution model was applied to first and second codon positions of the 33 taxa data set. P. falciparum and 2 of its relatives infecting great ape hosts, P. reichenowi and P. gaboni, formed a monophyletic clade with 3 rodent parasites, P. yoelii, P. berghei and P. chabaudi (posterior probability PP = 0.92). Posterior probabilities equal to 1 were removed.

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Additional file 7:

Supplementary Table S5, Robustness of the support to the removal and addition of taxa. All codon positions were analyzed under GTR + Γ4 and GTR + Γ4 + I models, for Bayesian and ML methods, respectively. Addition or removal of taxa to the complete nucleotide data set comprising 33 taxa and 3 concatenated genes, 3308 sites. Phylogenetic analyses were performed under models GTRnt + Γ4 + I and GTRnt + Γ4, for maximum-likelihood (ML) and Bayesian (BI) methods, respectively. Cells display support as [PP, SH, BS], with PP: posterior probability (BI), SH: Shimodaira-Hasegawa-like support (ML), and BS: bootstrap support (ML). "*": not applicable. (a): PP and BS are summed over various positions of Hepatocystis species. Main lineages of mammal parasites are defined according to their host preference: "Rodent", "Primate" and "Great Ape" (see Additional file 1 and 8, Tables S1 and S6). "-" removal of species. "+" addition of species. "P. fal.": P. falciparum; "P. rei.": P. reichenowi; "P. gab.": P. gaboni; "P. yoe.": P. yoelii; "P. ber.": P. berghei; "P. cha.": P. chabaudi; "Hum": human primate parasites P. malariae and P. ovale; "Afr.": African primate parasites P. gonderi and P. DAJ-2004; "Asi": 10 Asian primate parasites; "Pla.": Plasmodium species infecting saurian hosts; "Hae.": Haemoproteus and Parahaemoproteus species; "Leu.": Leucocytozoon species; "Haemo." Haemosporidian species.

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Additional file 8:

Supplementary Table S6, Additional mitochondrial genes. Accession numbers of 51, 41 and 1 additional CytB, Cox1 and Cox3 genes, respectively, and parasite and host names (1 partial CytB genes). References: (a) Perkins and Schall (2002) [6]; (b) Perkins et al. (2007) [37]; (c) Cheesman et al. (2009) [76]; (d) Hall et al. (2005) [77]; (e) Escalante et al. (1998) [21]; (f) Seethamchai et al. (2008) [78]; (g) Martinsen et al. (2008) [36]; (h) Martinsen et al. (2007) [79]; (i) CytB + Cox1 + Cox3, Perkins (2008) [23]; (j) Rich et al. (2009) [26]. Abbreviation: "P.": Plasmodium species, "He.": Hepatocystis species.

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Additional file 9:

Supplementary Table S7, Accession numbers of ClpC and ASL genes. Accession numbers of 27 ClpC and 18 ASL genes. (a): Taxa used for the estimation of the length of the 7-taxa tree.

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Additional file 10:

Supplementary Figure S3, Phylogenetic tree of 18 ASL genes. Bayesian reconstruction under the GTRnt + Γ4 model. Edges with PP < 0.9 were collapsed, and PP = 1 are not shown. The ASL phylogeny is not congruent with a monophyly of mammal malaria parasites.

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Additional file 11:

Supplementary Figure S4, Phylogenetic tree of 27 ClpC genes. Bayesian reconstruction under the GTRnt + Γ4 model. Edges with PP < 0.9 were collapsed, and PP = 1 are not shown. The ClpC phylogeny supports the monophyly of mammalian malaria parasites (PP = 0.99).

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Additional file 12:

Supplementary Table S8, Robustness of clade support in trees designed to display long branches. Each of the 9 taxon samples comprised the three most distantly related Leucocytozoon species, the 14 primate parasites, and two single representatives of parasites of great apes and of rodents, respectively. In each case, 14 taxa were removed from the complete nucleotide data-set comprising 33 taxa and 3 concatenated genes, 3308 sites. Phylogenetic analyses were performed under models GTRnt + Γ4 + I and GTRnt + Γ4, for maximum likelihood (ML) and Bayesian (BI) methods, respectively. Cells display support as follows: [PP, SH, BS], with PP: posterior probability (BI), SH: Shimodaira-Hasegawa-like support ("*": not applicable, ML), and BS: bootstrap support (ML). Main lineages of mammal parasites are defined according to their host preference: "Rodent", "Primate" and "Great Ape" (see Additional file 1, Table S1). "P. fal.": P. falciparum; "P. rei.": P. reichenowi; "P. gab.": P. gaboni; "P. yoe.": P. yoelii; "P. ber.": P. berghei; "P. cha.": P. chabaudi.

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