Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T12:44:01.876Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential patterns of molecular evolution among Haemosporidian parasite groups

Published online by Cambridge University Press:  29 October 2014

ROBERT K. OUTLAW ,
BRIAN COUNTERMAN  and
DIANA C. OUTLAW
ROBERT K. OUTLAW*
Affiliation:
Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA
BRIAN COUNTERMAN
Affiliation:
Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA
DIANA C. OUTLAW
Affiliation:
Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA
*
*Corresponding author: Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Malaria parasites have had profound effects on human populations for millennia, but other terrestrial vertebrates are impacted by malaria as well. Entire species of birds have been driven to extinction, and many others are threatened by population declines. Recent studies have shown that host-switching is quite common among malaria parasite lineages, and these switches often involve a significant shift in the environment in which the parasites find themselves, including nucleated vs non-nucleated red blood cells and red vs white blood cells. Therefore, it is important to understand how parasites adapt to these different host environments. The mitochondrial cytochrome b (cyt b) gene shows evidence of adaptive molecular evolution among malaria parasite groups, putatively because of its critical role in the electron transport chain (ETC) in cellular metabolism. Two hypotheses were addressed here: (1) mitochondrial components of the ETC (cyt b and cytochrome oxidase 1 [COI]) should show evidence of adaptive evolution (i.e. selection) and (2) selection should be evident in host switches. Overall we found a signature of constraint (e.g. purifying selection) across the four genes included here, but we also found evidence of positive selection associated with host switches in cyt b and, surprisingly, in (apicoplast) caseinolytic protease C. These results suggest that evidence of selection should be widespread across these parasite genomes.

Keywords

malariagene evolutiondN/dSωHaemosporida
Type
Research Article
Information
Parasitology , Volume 142 , Issue 4 , April 2015 , pp. 612 - 622
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

Atkinson, C. T. (2008 a). Haemoproteus . In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 13–34. Wiley-Blackwell, Oxford, UK.Google Scholar
Atkinson, C. T. (2008 b). Avian Malaria. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 35–53. Wiley-Blackwell, Oxford, UK.Google Scholar
Atkinson, C. T. and van Riper, C. III (1991). Epizootiology and pathogenicity of avian hematozoa: Plasmodium, Haemoproteus, and Leucocytozoon . In Bird-Parasite Interactions (ed. Loye, J. E. and Zuk, M.), pp. 19–48. Ecology, Evolution and Behavior, Oxford University Press, New York.Google Scholar
Ballard, J. W. O. and Kreitman, M. (1995) Is mitochondrial DNA a strictly neutral marker? Trends in Ecology and Evolution 10, 485–488.Google Scholar
Bensch, S., Hellgren, O., Križanauskienė, A., Palinauskas, V., Valkiūnas, G., Outlaw, D. and Ricklefs, R. E. (2013). How can we determine the molecular clock of malaria parasites? Trends in Parasitology 29, 363–369.Google Scholar
Chitnis, C. E. and Staines, H. M. (2013). Dealing with change: the different microenvironments faced by the malarial parasite. Molecular Microbiology 88, 1–4.Google Scholar
Delport, W., Poon, A. F., Frost, S. D. W. and Kosakovsky Pond, S. L. (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics. [Epub ahead of print; PMID: 20671151].Google Scholar
Escalante, A. A., Freeland, D. E., Collins, W. E. and 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 95, 8124–8129.Google Scholar
Forrester, D. J. and Greiner, E. C. (2009). Leucocytozoonosis. In Parasitic Diseases of Wild Birds (ed. Atkinson, C. T., Thomas, N. J. and Hunter, D. B.), pp. 54–107. Wiley-Blackwell, Oxford, UK.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Hagner, S. C., Misof, B., Maier, W. A. and Kampen, H. (2007). 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 . Parasitology Research 101, 493–503.Google Scholar
Hikosaka, K., Kita, K. and Tanabe, K. (2013). Diversity of mitochondrial genome structure in the phylum Apicomplexa. Molecular and Biochemical Parasitology 188, 6–33.Google Scholar
Hillis, D. M., Moritz, D. and Mable, B. K. (eds). (1996). Molecular Systematics. Sinauer Associates, Sunderland, Massachusetts, pp. 407–514.Google Scholar
Knowles, S. C. L., Wood, M. J., Alves, R., Wilkin, T. A., Bensch, S. and Sheldon, B. C. (2011). Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology 20, 1062–1076.Google Scholar
Kosakovsky Pond, S. L. and Frost, S. D. W. (2005). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.Google Scholar
Kwiatkowski, D. P. (2005). How malaria has affected the human genome and what human genetics can teach us about malaria. American Journal of Human Genetics 77, 171–192.Google Scholar
Martinsen, E. S., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.Google Scholar
Mather, M. W. and Vaidya, A. B. (2008). Mitochondria in malaria and related parasites: ancient, diverse and streamlined. Journal of Bioenergetics and Biomembranes 40, 425–433.Google Scholar
Mogi, T. and Kita, K. (2010). Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium . Parasitology International 59, 305–312.Google Scholar
Nabholz, B., Glémin, S. and Galtier, N. (2007). Strong variations of mitochondrial mutation rate across mammals – the longevity hypothesis. Molecular Biology and Evolution 25, 120–130.Google Scholar
Nunn, G. B. and Stanley, S. E. (1998). Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Molecular Biology and Evolution 15, 1360–1371.Google Scholar
Outlaw, D. C. and Ricklefs, R. E. (2010). Comparative gene evolution in Haemosporidian (Apicomplexa) parasites of birds and mammals. Molecular Biology and Evolution 27, 537–542.Google Scholar
Outlaw, D. C. and Ricklefs, R. E. (2011). Rerooting the evolutionary tree of malaria parasites. Proceedings of the National Academy of Sciences 108, 13183–13187.Google Scholar
Painter, H. J., Morrisey, J. M., Mather, M. W. and Vaidya, A. B. (2007). Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum . Nature 446, 88–91.Google Scholar
Perkins, S. L. (2014). Malaria's many mates: past, present, and future of the systematics of the order Haemosporida. Journal of Parasitology 100, 11–25.Google Scholar
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malaria parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle Scholar
Perkins, S. L., Martinsen, E. S. and Falk, B. G. (2011). Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674.Google Scholar
Rambaut, A. and Drummond, A. J. (2007). Tracer. http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226–229.Google Scholar
Ricklefs, R. E., Outlaw, D. C., Svensson-Coelho, M., Medeiros, M. C. L., Ellis, V. A. and Latta, S. (2014). Species formation by host switching in avian malaria parasites. Proceedings of the National Academy of Sciences 111, 14816–14821.CrossRefGoogle ScholarPubMed
Salcedo-Sora, J. E. and Ward, S. A. (2013). The folate metabolic network of Falciparum malaria. Molecular and Biochemical Parasitology 188, 51–62.Google Scholar
Schaer, J., Perkins, S. L., Decher, J., Leendertz, F. H., Fahr, J., Weber, N. and Matuschewski, K. (2013). High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proceedings of the National Academy of Sciences 110, 17415–17419.Google Scholar
Schall, J. J. (1996). Malarial parasites of lizards: diversity and ecology. Advances in Parasitology 37, 255–333.Google Scholar
Schall, J. J. (1990). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite-host association. Parasitology 100, S35–S52.Google Scholar
Slamovits, C. H., Saldarriaga, J. F., Larocque, A. and Keeling, P. J. (2007). The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both Apicomplexan and Dinoflagellate mitochondrial genomes. Journal of Molecular Biology 372, 356–368.Google Scholar
Suplick, K., Akella, R., Weidanz, W., Long, C. and Vaidya, A. (1987). Molecular genetic analysis of a highly conserved tandemly repeated gene-cluster of malarial parasites. In Federation Proceedings 46, 778–778.Google Scholar
Telford, S. R. (2009). Hemoparasites of the Reptilia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA, pp. 11.Google Scholar
Van Dooren, G. G., Stimmler, L. M. and McFadden, G. I. (2006). Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiology Reviews 30, 596–630.CrossRefGoogle ScholarPubMed
vanRiper, C. III. (1991). The impact of introduced vectors and avian malaria on insular passeriform bird populations in Hawaii. Bulletin of the Society of Vector Ecology 16, 59–83.Google Scholar
Witsenburg, F., Salamin, N. and Christe, P. (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. Malaria Journal 11, 53.Google Scholar
Yang, Z. (2007). PAML 4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591 (http://abacus.gene.ucl.ac.uk/software/paml.html).Google Scholar
Supplementary material: Image

Outlaw Supplementary Material

Figure S1

Download Outlaw Supplementary Material(Image)
Image 2.4 MB
Supplementary material: Image

Outlaw Supplementary Material

Figure S2

Download Outlaw Supplementary Material(Image)
Image 1.9 MB
Supplementary material: Image

Outlaw Supplementary Material

Figure S3

Download Outlaw Supplementary Material(Image)
Image 1.6 MB