Parasitology: Hidden in plain sight: Cryptic and endemic malaria parasites in North American White-Tailed deer (Odocoileus virginianus)

Science Advances

Volumn 2, Issue 2, 2016, Pages

  Martinsen, Ellen S ^a   McInerney, Nancy ^a   Brightman, Heidi ^a   Ferebee, Ken ^b   Walsh, Tim ^a   McShea, William J ^c   Forrester, Tavis D ^c   Ware, Lisa ^c   Joyner, Priscilla H ^c   Perkins, Susan L ^d   Latch, Emily K ^e   Yabsley, Michael J ^f   Schall, Joseph J ^g   Fleischer, Robert C ^a  

^a SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^b Wooded Heart of Washington   (United States)

^c SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^d DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^e UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

^g UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; POLYMERASE CHAIN REACTION;

CYTOCHROME B GENES; MALARIA PARASITE; MAMMALIAN ORDERS; NORTH AMERICAN; PHYLOGENETIC ANALYSIS; PHYLOGEOGRAPHY; PLASMODIUM PARASITES; WHITE-TAILED DEER;

DISEASES;

ANIMAL; ANOPHELES; CLASSIFICATION; DEER; DISEASE CARRIER; GENETICS; HOST RANGE; ISOLATION AND PURIFICATION; MALARIA; PARASITOLOGY; PHYLOGENY; PHYLOGEOGRAPHY; PLASMODIUM; UNITED STATES; VETERINARY;

ANIMALS; ANOPHELES; DEER; HOST SPECIFICITY; INSECT VECTORS; MALARIA; PHYLOGENY; PHYLOGEOGRAPHY; PLASMODIUM; UNITED STATES;

EID: 84964967399     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1501486     Document Type: Article

References (34)

1. N. D. Levine, The Protozoan Phylum Apicomplexa (CRC Press, Boca Raton, FL, 1988).
2. G. Valkiunas, Avian Malaria Parasites and other Haemosporidia (CRC Press, Boca Raton, FL, 2005).
3. P. C. C. Garnham, Malaria parasites and other Haemosporidia (Blackwell Scientific Publication, Oxford, 1966).
4. E. S. Martinsen, S. L. Perkins, J. J. Schall, A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Mol. Phylogenet. Evol. 47, 261-273 (2008).
5. J. Schaer, S. L. Perkins, J. Decher, F. H. Leendertz, J. Fahr, N. Weber, K. Matuschewskia, High diversity of West African bat malaria parasites and a tight link with rodent Plasmodium taxa. Proc. Natl. Acad. Sci. U. S. A. 110, 17415-17419 (2013).
6. W. Liu, Y. Li, K. S. Shaw, G. H. Learn, L. J. Plenderleith, J. A. Malenke, S. A. Sundararaman, M. A. Ramirez, P. A. Crystal, A. G. Smith, F. Bibollet-Ruche, A. Ayouba, S. Locatelli, A. Esteban, F. Mouacha, E. Guichet, C. Butel, S. Ahuka-Mundeke, B.-I. Inogwabini, J.-B. N. Ndjango, S. Speede, C. M. Sanz, D. B. Morgan, M. K. Gonder, P. J. Kranzusch, P. D. Walsh, A. V. Georgiev, M. N. Muller, A. K. Piel, F. A. Stewart, M. L. Wilson, A. E. Pusey, L. Cui, Z. Wang, A. Färnert, C. J. Sutherland, D. Nolder, J. A. Hart, T. B. Hart, P. Bertolani, A. Gillis, M. LeBreton, B. Tafon, J. Kiyang, C. F. Djoko, B. S. Schneider, N. D. Wolfe, E. Mpoudi-Ngole, E. Delaporte, R. Carter, R. L. Culleton, G. M. Shaw, J. C. Rayner, M. Peeters, B. H. Hahn, P. M. Sharp, African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).
7. K. L. Kuttler, R. M. Robinson, W. P. Rogers, Exacerbation of latent erythrocytic infections in deer following splenectomy. Can. J. Comp. Med. Vet. Sci. 31, 317-319 (1967).
8. P. C. C. Garnham, K. L. Kuttler, A malaria parasite of the white-tailed deer (Odocoileus virginianus) and its relation with known species of Plasmodium in other ungulates. Proc. R. Soc. Lond. B. Biol. Sci. 206, 395-402 (1980).
9. P. C. C. Garnham, A. J. Duggan, Catalogue of the Garnham collection of malaria parasites and other haemosporidia (Cambridge Univ. Press, Cambridge, 1986).
10. W. R. Davidson, J. M. Crum, J. L. Blue, D. W. Sharp, J. H. Phillips, Parasites, diseases, and health status of sympatric populations of fallow deer and white-tailed deer in Kentucky. J. Wildl. Dis. 21, 153-159 (1985).
11. W. R. Davidson, C. B. Crow, J. M. Crum, R. R. Gerrish, Observations on Theileria cervi and Trypanosoma cervi in white-tailed deer (Odocoileus virginianus) from the Southeastern United States. Proc. Helminthol. Soc. Wash. 50, 165-169 (1983).
12. L. O. Howard, H. G. Dyar, F. Khab, The Mosquitoes of North and Central America and the West Indies (Carnegie Institution of Washington, Washington, DC, 1912).
13. W. V. King, Experiments on the development of malaria parasites in three American species of Anopheles. J. Exp. Med. 23, 703-716 (1916).
14. G. Valkinas, S. Bensch, T. A. Iezhova, A. Križanauskien, O. Hellgren, C. V. Bolshakov, Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: Microscopy is still essential. J. Parasitol. 92, 418-422 (2006).
15. G. Valkinas, V. Palinauskas, M. Ilgnas, D. Bukauskait, D. Dimitrov, R. Bernotien, P. Zehtindjiev, M. Ilieva, T. A. Iezhova, Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitol. Res. 113, 2251-2263 (2014).
16. S. Bensch, J. Pérez-Tris, J. Waldenström, O. Hellgren, Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation Evolution 58, 1617-1621 (2004).
17. R. E. Ricklefs, D. C. Outlaw, A molecular clock for malaria parasites. Science 329, 226-229 (2010).
18. M. A. Pacheco, F. U. Battistuzzi, R. E. Junge, O. E. Cornejo, C. V. Williams, I. Landau, L. Rabetafika, G. Snounou, L. Jones-Engel, A. A. Escalante, Timing the origin of human malarias: The lemur puzzle. BMC Evol. Biol. 11, 299-316 (2011).
19. J. C. Silva, A. Egan, C. Arze, J. L. Spouge, D. G. Harris, A new method for estimating species age supports the coexistence of malaria parasites and their mammalian hosts. Mol. Biol. Evol. 32, 1354-1364 (2015).
20. C. Gilbert, A. Ropiquet, A. Hassanin, Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): Systematics, morphology, and biogeography. Mol. Phyl. Evol. 40, 101-117 (2006).
21. E. K. Latch, J. R. Heffelfinger, J. A. Fike, O. E. Rhodes Jr., Species-wide phylogeography of North American mule deer (Odocoileus hemionus): Cryptic glacial refugia and postglacial recolonization. Mol. Ecol. 18, 1730-1745 (2009).
22. E. K. Latch, D. M. Reding, J. R. Heffelfinger, C. H. Alcalá-Galván, O. E. Rhodes Jr., Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography. Mol. Ecol. 23, 3171-3190 (2014).
23. D. L. Ellsworth, R. L. Honeycutt, N. J. Silvy, J. W. Bickham, W. D. Klimstra, Historical biogeography and contemporary patterns of mitochondrial DNA variation in white-tailed deer from the Southeastern United States. Evolution 48, 122-136 (1994).
24. E. S. Martinsen, J. L. Waite, J. J. Schall, Morphologically defined subgenera of Plasmodium from avian hosts: Test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology 134, 483-490 (2007).
25. G. M. Jeffery, Blood meal volume in Anopheles quadrimaculatua, A. albimanus and A. aegypti. Exp. Parasitol. 5, 371-375 (1956).
26. M. C. Powell, G. D. DelGiudice, Birth, morphologic, and blood characteristics of free-ranging white-tailed deer neonates. J. Wildl. Dis. 41, 171-183 (2005).
27. M. B. Crabtree, H. M. Savage, B. R. Miller, Development of a species-diagnostic polymerase chain reaction assay for the identification of Culex vectors of St. Louis Encephalitis virus based on interspecies sequence variation in ribosomal DNA spacers. Am. J. Trop. Med. Hyg. 53, 105-109 (1995).
28. E. S. Martinsen, I. Paperna, J. J. Schall, Morphological versus molecular identification of avian Haemosporidia: An exploration of three species concepts. Parasitology 133, 279-288 (2006).
29. A. J. Drummond, A. Rambaut, BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214-222 (2007).
30. R. Lanfear, B. Calcott, S. Y. W. Ho, S. Guindon, PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695-1701 (2012).
31. D. Silvestro, I. Michalak, raxmlGUI: A graphical front-end for RAxML. Org. Divers. Evol. 12, 335-337 (2012).
32. A. J. Drummond, S. Y. W. Ho, M. J. Phillips, A. Rambaut, Relaxed phylogenetics and dating with confidence. PLOS Biol. 4, e88 (2006).
33. A. Rambaut, A. J. Drummond, TreeAnnotator (2007); available at http://beast. bio. ed. ac. uk/TreeAnnotator.
34. R.-J. den Tex, R. Thorington, J. E. Maldonado, J. A. Leonard, Speciation dynamics in the SE Asian tropics: Putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. Mol. Phylogenet. Evol. 55, 711-720 (2010).