Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-22T11:57:42.912Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary relationships between 15 Plasmodium species from New and Old World primates (including humans): a 18S rDNA cladistic analysis

Published online by Cambridge University Press:  18 November 2004

M. C. LECLERC ,
J. P. HUGOT ,
P. DURAND  and
F. RENAUD
M. C. LECLERC
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, IRD, Equipe ‘Evolution des Systèmes Symbiotiques’, 911 Avenue Agropolis, 34394 Montpellier cedex 5, France
J. P. HUGOT
Affiliation:
Mahidol University, Research Center for Emerging Viral Diseases/Center for Vaccine Development, UR IRD 034, Institute of Sciences and Technology, Mahidol University at Salaya 25/25 Phutthamonthon 4, Nakhonpathom 73170, Thailand
P. DURAND
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, IRD, Equipe ‘Evolution des Systèmes Symbiotiques’, 911 Avenue Agropolis, 34394 Montpellier cedex 5, France
F. RENAUD
Affiliation:
Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, IRD, Equipe ‘Evolution des Systèmes Symbiotiques’, 911 Avenue Agropolis, 34394 Montpellier cedex 5, France
Get access Rights & Permissions [Opens in a new window]

Abstract

We present a new phylogenetic analysis of 15 primate Plasmodium species based on 18S rDNA sequences including new sequences of Plasmodium coatneyi, P. fieldi, P. gonderi, P. hylobati and P. simium. The results are discussed in the context of the parasite host species and their geographical distribution. Contrary to other phylogenies constructed with this 18S rDNA molecule, we observed that the topology of phylogenetic trees was not affected either by the quality of the nucleotide matrices, or by the species present in the outgroup. This analysis showed the following. (1) The polyphyly of human Plasmodium is confirmed. (2) The monophyly of Plasmodium from Old World monkeys is confirmed by the new added sequences and P. gonderi, an African species, possibly could be at the root of this group. (3) The most parsimonious biogeographical hypothesis is that P. vivax originated in Asia; thus, its related species P. simium appears to be derived through a transfer from the human P. vivax to New World monkey species in South America. (4) Sampling efforts of non-human primate Plasmodium could permit improvement of the knowledge of primate Plasmodium phylogeny and also consideration of the risks of malaria emergence from monkey reservoirs.

Keywords

primate Plasmodium18S rDNAcladistic analysis
Type
Research Article
Information
Parasitology , Volume 129 , Issue 6 , December 2004 , pp. 677 - 684
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

BARRIEL, V. ( 1994). Phylogénies moléculaires et insertions-délétions de nucléotides. C.R.A.S. Paris, Sciences Vie/Life Sciences 317, 693–701.Google Scholar
CARNEVALE, P., BAUDON, D., MOLEZ, J. F. & GUIGUEMDE, T. R. ( 1984). Aspects classiques et modernes des cycles de développement des plasmodiums humains. Etudes Médicales 2, 61–78.Google Scholar
CARTER, R. ( 2003). Speculations on the origins of Plasmodium vivax malaria. Trends in Parasitology 19, 214–219.CrossRefGoogle Scholar
COLLINS, W. E. & AIKAWA, M. ( 1993). Plasmodia of nonhuman primates. In Parasitic Protozoa (ed. Kreier, J. P.), Vol. 5, pp. 105–133. Academic Press, New York.
ESCALANTE, A. A. & AYALA, F. J. ( 1994). Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proceedings of National Academy of the Sciences, USA 91, 11373–11377.CrossRefGoogle Scholar
ESCALANTE, A. A., BARRIO, E. & AYALA, F. J. ( 1995). Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Molecular Biology and Evolution 12, 616–626.Google Scholar
ESCALANTE, A. A., GOLDMAN, I. F., DE RIJK, P., DE WACHTER, R., COLLINS, W. E., QARI, S. H. & LAL, A. A. ( 1997). Phylogenetic study of the genus Plasmodium based on the secondary structure-based alignment of the small subunit ribosomal RNA. Molecular and Biochemical Parasitology 90, 317–321.CrossRefGoogle Scholar
ESCALANTE, A. E., FREELAND, D. E., COLLINS, W. E. & LAL, A. A. ( 1998). The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proceedings of the National Academy of Sciences, USA 95, 8124–8129.CrossRefGoogle Scholar
FANDEUR, T., VOLNEY, B., PENEAU, C. & de THOISY, B. ( 2000). Monkeys of the rainforest in French Guinea are natural reservoirs for P. brasilianum/P. malariae malaria. Parasitology 120, 11–21.Google Scholar
FELSENSTEIN, J. ( 1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle Scholar
GARDNER, M. J., HALL, N., FUNG, E., WHITE, O., BERRIMAN, M., HYMAN, R. W., CARLTON, J. M., PAIN, A., NELSON, K. E., BOWMAN, S., PAULSEN, I. T., JAMES, K., EISEN, J. A., RUTHERFORD, K., SALZBERG, S. L., CRAIG, A., KYES, S., CHAN, M. S., NENE, V., SHALLOM, S. J., SUH, B., PETERSON, J., ANGIUOLI, S., PERTEA, M., ALLEN, J., SELENGUT, J., HAFT, D., MATHER, M. W., VAIDYA, A. B., MARTIN, D. M., FAIRLAMB, A. H., FRAUNHOLZ, M. J., ROOS, D. S., RALPH, S. A., McFADDEN, G. L., CUMMINGS, L. M., SUBRAMANIAN, G. M., MUNGALL, C., VENTER, J. C., CARUCCI, D. J., HOFFMAN, S. L., NEWBOLD, C., DAVIS, R. W., FRASER, C. M. & BARRELL, B. ( 2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, Genetics 419, 498–511.CrossRefGoogle Scholar
GARNHAM, P. C. C. ( 1966). Malaria Parasites and Other Haemosporidia. Blackwell Scientific Publications, Oxford.
GROVES, C. P. ( 1993). Order Primates. In Mammal Species of the World: A Taxonomic and Geographic Reference (ed. DonWilson, E. & Reeder, D. M.), pp. 243–277. Smithsonian Institution Press, Washington, D.C.
GUNDERSON, J. H., SOGIN, M. L., WOLLETT, G., HOLLINGDALE, M., de la CRUZ, V. H., WATERS, A. P. & McCUTCHAN, T. F. ( 1987). Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238, 933–937.CrossRefGoogle Scholar
GYSIN, J. ( 1998). Animal models: primates. In Malaria: Parasite Biology, Pathogenesis and Protection (ed. Sherman, I. W.), pp. 419–441. ASM Press, Washington, DC.
HOLT, R. A., SUBRAMANIAN, G. M., HALPERN, A., SUTTON, G. G., CHARLAB, R., NUSSKERN, D. R., WINCKER, P., CLARK, A. G., RIBEIRO, J. M., WIDES, R., SALZBERG, S. L., LOFTUS, B., YANDELL, M., MAJOROS, W. H., RUSCH, D. B., LAI, Z., KRAFT, C. L., ABRIL, J. F., ANTHOUARD, V., ARENSBURGER, P., ATKINSON, P. W., BADEN, H., de BERARDINIS, V., BALDWIN, D., BENES, V., BIEDLER, J., BLASS, C., BOLANOS, R., BOSCUS, D., BARNSTEAD, M., CAI, S., CENTER, A., CHATURVERDI, K., CHRISTOPHIDES, G. K., CHRYSTAL, M. A., CLAMP, M., CRAVCHIK, A., CURWEN, V., DANA, A., DELCHER, A., DEW, I., EVANS, C. A., FLANIGAN, M., GRUNDSCHOBER-FREIMOSER, A., FRIEDLI, L., GU, Z., GUAN, P., GUIGO, R., HILLENMEYER, M. E., HLADUN, S. L., HOGAN, J. R., HONG, Y. S., HOOVER, J., JAILLON, O., KE, Z., KODIRA, C., KOKOZA, E., KOUTSOS, A., LETUNIC, I., LEVITSKY, A., LIANG, Y., LIN, J. J., LOBO, N. F., LOPEZ, J. R., MALEK, J. A., McINTOSH, T. C., MEISTER, S., MILLER, J., MOBARRY, C., MONGIN, E., MURPHY, S. D., O'BROCHTA, D. A., PFANNKOCH, C., QI, R., REGIER, M. A., REMINGTON, K., SHAO, H., SHARAKHOVA, M. V., SITTER, C. D., SHETTY, J., SMITH, T. J., STRONG, R., SUN, J., THOMASOVA, D., TON, L. Q., TOPALIS, P., TU, Z., UNGER, M. F., WALENZ, B., WANG, A., WANG, J., WANG, M., WANG, X., WOODFORD, K. J., WORTMAN, J. R., WU, M., YAO, A., ZDOBNOV, E. M., ZHANG, H., ZHAO, Q., ZHAO, S., ZHU, S. C., ZHIMULEV, I., COLUZZI, M., della TORRE, A., ROTH, C. W., LOUIS, C., KALUSH, F., MURAL, R. J., MYERS, E. W., ADAMS, M. D., SMITH, H. O., BRODER, S., GARDNER, M. J., FRASER, C. M., BIRNEY, E., BORK, P., BREY, P. T., VENTER, J. C., WEISSENBACH, J., KAFATOS, F. C., COLLINS, F. H. & HOFFMAN, S. L. ( 2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.CrossRefGoogle Scholar
LI, J., GUTELL, R. R., DAMBERGER, S. H., WIRTZ, R. A., KISSINGER, J. C., ROGERS, M. J., SATTABONGKOT, J. & McCUTCHAN, T. F. ( 1997). Regulation and trafficking of three distinct 18S ribosomal RNAs during development of the malaria parasite. Journal of Molecular Biology 269, 203–213.CrossRefGoogle Scholar
LI, J., COLLINS, W. E., WIRTZ, R. A., RATHORE, D., LAL, A. & McCUTCHAN, T. F. ( 2001). Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerging Infectious Diseases 7, 35–42.CrossRefGoogle Scholar
McCUTCHAN, T. F., de la CRUZ, V. F., LAL, A. A., GUNDERSON, J. H., ELWOOD, H. J. & SOGIN, M. L. ( 1988). Primary sequences of two subunit ribosomal RNA genes from Plasmodium falciparum. Molecular and Biochemical Parasitology 28, 63–68.CrossRefGoogle Scholar
PERKINS, S. L. & SCHALL, J. J. ( 2002). A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle Scholar
PHILIPPE, H. ( 1993). MUST: a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Research 21, 5264–5272.CrossRefGoogle Scholar
POIRRIEZ, J., DEI-CAS, E., DUJARDIN, L. & LANDAU, I., ( 1995). The blood-stage of Plasmodium georgesi, P. gonderi and P. petersi: course of untreated infection in their natural hosts and additional morphological distinctive features. Parasitology 111, 547–554.Google Scholar
PURVIS, A. ( 1995). A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London, B 348, 405–421.CrossRefGoogle Scholar
QARI, S. H., SHI, Y. P., PIENIAZEK, N. J., COLLINS, W. E. & LAL, A. A. ( 1996). Phylogenetic relationships among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum. Molecular Phylogenetics and Evolution 6, 157–165.CrossRefGoogle Scholar
RATHORE, D., WAHL, A. M., SULLIVAN, M. & McCUTCHAN, T. F. ( 2001). A phylogenetic comparison of gene trees constructed from plastid mitochondrial and genome DNA of Plasmodium species. Molecular and Biochemical Parasitology 114, 89–94.CrossRefGoogle Scholar
RICKLEFS, R. E. & FALLON, S. M. ( 2002). Diversification of host switching avian malaria parasites. Proceedings of the Royal Society of London, B 269, 885–892.CrossRefGoogle Scholar
SINA, B. ( 2002). Focus on Plasmodium vivax. Trends in Parasitology 18, 287–289.CrossRefGoogle Scholar
SNOUNOU, G., VIRIYAKOSOL, S., ZHU, X. P., JARRA, W., PINHEIRO, L., do ROSARIO, V. E., THAITHONG, S. & BROWN, K. N. ( 1993). High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Molecular and Biochemical Parasitology 61, 315–320.CrossRefGoogle Scholar
SWOFFORD, D. L. ( 1999). PAUP: Phylogenetic Analysis Using Parsimony (and other Methods), Version 4. Sinauer, Sunderland, Massachusetts.
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. ( 1997). The clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
WATERS, A. P., HIGGINS, D. G. & McCUTCHAN, T. F. ( 1991). Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proceedings of the National Academy of Sciences, USA 88, 3140–3144.CrossRefGoogle Scholar
WATERS, A. P., HIGGINS, D. G. & McCUTCHAN, T. F. ( 1993). Evolutionary relatedness of some primate models of Plasmodium. Molecular Biology and Evolution 10, 914–923.Google Scholar
WOLFE, N. D., ESCALANTE, A. A., KARESH, W. B., KILBOURN, A., SPIELMAN, A. & LAL, A. A. ( 1998). Wild primate population in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4, 149–158.Google Scholar
WORLD HEALTH ORGANIZATION ( 1998). Malaria. Unpublished document. Available from http://www.Who.ch/.