Abstract
Molecular systematic studies published during the last 15 years to clarify the phylogenetic relationships among the malaria parasites have led to two major hypotheses on the descent of Plasmodium falciparum: One supports an avian origin as a result of a relatively recent host switch, and another one favours the evolutionary development of P. falciparum together with its human host from primate ancestors. In this paper, we present phylogenetic analyses of three different Plasmodium genes, the nuclear 18 small sub-unit (SSU) ribosomal ribonucleic acid (rRNA), the mitochondrial cytochrome b (cyt b) and the plastid caseinolytic protease C (ClpC) gene, using numerous haemosporidian parasite DNA sequences obtained from the GenBank as well as several new sequences for major malaria parasites including the avian one Plasmodium cathemerium, which has never been considered in molecular phylogenetic analyses before. Most modern and sophisticated DNA substitution models based on Bayesian inference analysis were applied to estimate the cyt b and ClpC phylogenetic trees, whereas the 18 SSU rRNA gene was examined with regards to its secondary structure using PHASE software. Our results indicate that the data presently available are generally neither sufficient in number nor in information to solve the problem of the phylogenetic origin of P. falciparum.
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References
Ayala FJ, Escalante AA, Rich SM (1999) Evolution of Plasmodium and the recent origin of the world populations of Plasmodium falciparum. Parassitologia 41:55–68
Ayala FJ, Fitch WM (1992) Phylogeny of Plasmodium falciparum. Parasitol Today 8:74–75
Ayala FJ, Rich SM (2000) Genetic variation and the recent worldwide expansion of Plasmodium falciparum. Gene 261:161–170
Babiker HA, Walliker D (1997) Current views on the population structure of Plasmodium falciparum: implications for control. Parasitol Today 13:262–267
Bennett GF, Bishop MA, Peirce MA (1993) Checklist of the avian species of Plasmodium Marchiafava & Celli, 1885 Apicomplexa and their distribution by avian family and Wallacean life zones. Syst Parasitol 26:171–179
Carter R, Mendis KN (2002) Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev 15:564–594
Carter R (2003) Speculations of the origins of Plasmodium vivax malaria. Trends Parasitol 19:214–219
Chauhan VS, Bhardwaj D (2003) Current status of malaria vaccine development. Adv Biochem Eng Biotech 84:143–182
Coatney GR, Collins WE, Warren M, Contacos PG (1971) The primate malarias. National Institutes of Health, Bethesda, MD
Coluzzi M (1999) The clay feet of the malaria giant and its African roots: hypothesis and inferences about origin, spread and control of Plasmodium falciparum. Parassitologia 41:277–283
Conway DJ, Baum J (2002) In the blood—the remarkable ancestry of Plasmodium falciparum. Trends Parasitol 18:351–355
Corradetti A, Garnham PCC, Laird M (1963) New classification of the avian malaria parasites. Parasitology 5:1–4
Egea N, Lang-Unnasch N (1995) Phylogeny of the large extrachromosomal DNA of organisms in the phylum Apicomplexa. J Eukaryot Microbiol 42:679–684
Escalante AA, Ayala FJ (1994) Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci USA 91:11373–11377
Escalante AA, Ayala FJ (1995) Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci USA 92:5793–5797
Escalante AA, Barrio E, Ayala FJ (1995) Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol 12:616–626
Escalante AA, Goldman IF, de Rijk P, de Wachter R, Collins WE, Qari SH, Lal AA (1997) Phylogenetic study of the genus Plasmodium based on the secondary structure-based alignment of the small subunit ribosomal RNA. Mol Biochem Parasitol 90:317–321
Escalante AA, Freeland DE, Collins WE, Lal A (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA 95:8124–8129
Fink E, Dann O (1967) Eine Weiterentwicklung des Roehl-Test zur Prüfung von Malariamitteln an Plasmodium cathemerium beim Kanarienvogel durch intravenöse Verabreichung. Z Tropenmed Parasitol 18:466–474
Galtier N (2004) Sampling properties of the bootstrap support in molecular phylogeny: influence of nonindependence among sites. Syst Biol 53:38–46
Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW et al (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511
Garnham PCC (1966) Malaria parasites and other haemosporidia. Blackwell, Oxford
Gehring CU (1974) Versuche zur Übertragung von Plasmodium cathemerium, einem der Vogelmalariaerreger, auf weiße Mäuse. PhD thesis, Med. Faculty, University of Bonn, Germany
Greenwood B, Mutabingwa T (2002) Malaria in 2002. Nature 415:670–672
Greenwood B, Bojang K, Whitty CJM, Targett GAT (2005) Malaria. Lancet 365:1487–1498
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149
Huelsenbeck JP (2001) MrBayes V3 b4 v2win: Bayesian inference of phylogeny. University of California—San Diego, La Jolla
Hughes A, Verra F (2002) Extensive polymorphism and ancient origin of Plasmodium falciparum. Trends Parasitol 18:348–351
Hume JCC, Lyons EL, Day KP (2003) Human migration, mosquitoes and the evolution of Plasmodium falciparum. Trends Parasitol 19:144–149
Jow H, Hudelot C, Rattray M, Higgs PG (2002) Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol 19:1591–1601
Jow H, Gowri-Shankar V, Guillard B (2005) PHASE: a software package for phylogenetics and sequence evolution. University of Manchester, UK
Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerli P, Su X-Z (2003) Early origin and recent expansion of Plasmodium falciparum. Science 300:318–321
Kedzierski L, Escalante AA, Isea R, Black CG, Barnwell JW, Coppel RL (2002) Phylogenetic analysis of the genus Plasmodium based on the gene encoding adenylosuccinate lyase. Infect Genet Evol 1:297–301
Killick-Kendrick R, Peters W (1978) Rodent malaria. Academic, London
Kissinger JC, Souza PC, Soares CO, Paul R, Wahl AM, Rathore D, McCutchan TF, Krettli AU (2002) Molecular phylogenetic analysis of the avian malarial parasite Plasmodium Novyella juxtanucleare. J Parasitol 88:769–773
Landau I (1965) Description de Plasmodium chabaudi n. sp. de rongeur africains. C R Hebd Séances Acad Sci 260:3758–3761
Landau I, Killick-Kendrick R (1966) Note préliminaire sur le cycle évolutif des deux Plasmodium du rongeur Thamnonmys rutilans de la République Centrafricaine. C R Hebd Séances Acad Sci 262:1113–1116
Leclerc MC, Hugot JP, Durand P, Renaud F (2004) Evolutionary relationships between 15 Plasmodium species from new and old world primates (including humans): an 18S rDNA cladistic analysis. Parasitology 129:677–684
Maitland K, Bejon P, Newton CRJC (2003) Malaria. Curr Opin Infect Dis 16:389–395
McCutchan TF, Dame JB, Miller LH, Barnwell J (1984) Evolutionary relatedness of Plasmodium species as determined by the structure of DNA. Science 225:808–811
McCutchan TF, Kissinger JC, Touray MG, Rogers MJ, Li J, Sullivan M, Braga EM, Krettli AU, Miller LH (1996) Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. Proc Natl Acad Sci USA 93:11889–11894
McGhee RB (1951) The adaption of the avian malaria parasite Plasmodium lophurae to a continuous existence in infant mice. J Infect Dis 88:86–97
McManus DP, Bowles J (1996) Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. Int J Parasitol 26:687–704
Misof B, Anderson CL, Buckley TR, Erpenbeck D, Rickert A, Misof K (2002) An empirical analysis of mt 16S rRNA covarion-like evolution in insects: site-specific rate variation is clustered and frequently detected. J Mol Evol 55:460–469
Misof B, Fleck G (2003) Comparative analysis of mt 16S rRNA secondary structures of odonates and its relevance to phylogenetic problems in insect systematics. Insect Mol Biol 12:535–547
Mu J, Ferdig MT, Feng X, Joy DA, Duan J, Furuya T, Subramanian G, Aravind L, Cooper RA, Wootton JJ, Xiong M, Su XZ (2003) Multiple transporters associated with malaria responses to chloroquine and quinine. Mol Microbiol 49:977–989
Newbold C, Craig A, Kyes S, Rowe A, Fernandez-Reyes D, Fagan T (1999) Cytoadherence, pathogenesis and the infected red cell surface in Plasmodium falciparum. Int J Parasitol 29:927–937
Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:972–978
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Qari SH, Shi YP, Pieniazek NJ, Collins WE, Lal AA (1996) Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. Mol Phylogenet Evol 6:157–165
Rathore D, Wahl AM, Sullivan M, McCutchan TF (2001) A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Mol Biochem Parasitol 114:89–94
Rich SM, Ayala FJ (2003) Phylogenetics in malaria research: the case for phylogenetics. Adv Parasitol 54:255–280
Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119
Roehl W (1926) Die Wirkung des Plasmochins auf die Vogelmalaria. Naturwissenschaften 14:1156–1159
Schall JJ (1996) Malarial parasites of lizards: diversity and ecology. Adv Parasitol 37:255–333
Swofford DL (1999) Phylogenetic analysis using parsimony, version 4. Sinauer, Sunderland, MA
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tillier ERM, Collins RA (1998) High apparent rate of simultaneous compensatory base pair substitutions in ribosomal RNA. Genetics 148:1993–2002
Vargas-Serrato E, Corredor V, Galinski MR (2003) Phylogenetic analysis of CSP and MSP-9 gene sequences demonstrates the close relationship of Plasmodium coatneyi and Plasmodium knowlesi. Infect Genet Evol 3:67–73
Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG et al (2001) The sequence of the human genome. Science 292:1305–1351
Vincke IH, Lips M (1948) Un nouveau Plasmodium d’un rongeur sauvage du Congo, Plasmodium berghei n. sp. Ann Soc Belge Med Trop 28:97–104
Walker HA, Richardson AP (1948) Potentiation of the curative action of 8-aminoquinolines and naphthoquinones in avian malaria. J Natl Mal Soc 7:4–11
Wang L, Kedzierski L, Wesselingh SL, Coppel RL (2003) Oral immunization with a recombinant malaria protein induces conformational antibodies and protects mice against lethal malaria. Infect Immun 71:2356–2364
Waters AP, Higgins DG, McCutchan TF (1991) Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc Natl Acad Sci USA 88:3140–3144
Waters AP, Higgins DG, McCutchan TF (1993) Evolutionary relatedness of some primate models of Plasmodium. Mol Biol Evol 10:914–923
Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 96:90–94
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Hagner, S.C., Misof, B., Maier, W.A. et al. Bayesian analysis of new and old malaria parasite DNA sequence data demonstrates the need for more phylogenetic signal to clarify the descent of Plasmodium falciparum . Parasitol Res 101, 493–503 (2007). https://doi.org/10.1007/s00436-007-0499-6
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DOI: https://doi.org/10.1007/s00436-007-0499-6