Conservation Genetics

, Volume 9, Issue 6, pp 1577–1588 | Cite as

Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas)

  • K. M. Pagenkopp
  • J. Klicka
  • K. L. Durrant
  • J. C. Garvin
  • R. C. Fleischer
Research Article

Abstract

Our current understanding of migration routes of many birds is limited and researchers have employed various methods to determine migratory patterns. Recently, parasites have been used to track migratory birds. The objective of this study was to determine whether haemosporidian parasite lineages detect significant geographic structure in common yellowthroats (Geothlypis trichas). We examined liver tissue or blood from 552 birds sampled from multiple locations throughout the continental United States, southern Canada, and the Bahamas. We found a 52.7% overall prevalence of haematozoan infection. We identified 86.1% of these infections to genus: 81% were Plasmodium; 5% were Haemoproteus; and 0.1% were Leucocytozoon. There were significant differences in the prevalence of different parasite genera among regions (χ2 = 36.82, P < 0.0001) and in the proportion of Plasmodium infections versus other parasites among regions (χ2 = 35.52, P < 0.0001). Sequence information identified three Haemoproteus lineages, two Leucocytozoon lineages, and thirteen Plasmodium lineages. Due to the low number of Haemoproteus and Leucocytozoon, only Plasmodium lineages were used in the geographic comparison of lineages. Six Plasmodium lineages were found in eight or more birds and the prevalence of these varied significantly among regions (χ2 = 172.33, P < 0.0001). Additionally, 45 juvenile birds were sampled to determine what parasites could be obtained in the breeding grounds and we found only one lineage. In conclusion, parasite lineages show some geographic structure, with some lineages being more geographically specific than others, but are not useful for determining migratory connectivity in this species.

Keywords

Plasmodium Common yellowthroat Migratory connectivity mtDNA Geothlypis 

Supplementary material

References

  1. Alavi Y, Arai M, Mendoza J et al (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 33:933–943PubMedCrossRefGoogle Scholar
  2. Atkinson CT, van Riper C III (1991) Pathogenicity and epizootiology of avian hematozoa: plasmodium, leucocytozoon, and haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions. Oxford University Press, Oxford, pp 19–48Google Scholar
  3. Atkinson C, Forrester D, Greiner E (1988) Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: seasonal transmission and vector abundance. J Med Entomol 25:45–51PubMedGoogle Scholar
  4. Ball RM Jr, Avise J (1992) Mitochondrial DNA phylogeographic differentiation among avian populations and the evolutionary significance of subspecies. Auk 109:626–636Google Scholar
  5. Ballard G, Geupei G, Nur N et al (2003) Long-term declines and decadal patterns in population trends of songbirds in western North America, 1979–1999. Condor 105:737–755CrossRefGoogle Scholar
  6. Beadell J, Fleischer R (2005) A restriction enzyme-based assay to distinguish between avian hemosporidians. J Parasitol 91:683–685CrossRefGoogle Scholar
  7. Beadell J, Gering E, Austin J et al (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844PubMedCrossRefGoogle Scholar
  8. Beadell JS, Ishtiaq F, Covas R et al (2006) Global phylogeographic limits in Hawaii’s avian malaria. Proc R Soc Lond B 273:2935–2944CrossRefGoogle Scholar
  9. Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian Willow Warblers. J Parasitol 89:388–391PubMedCrossRefGoogle Scholar
  10. Bensch S, Stjernman M, Hasselquist D et al (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B 267:1583–1589CrossRefGoogle Scholar
  11. Bensch S, Perez-Tris J, Waldenström J et al (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617–1621PubMedGoogle Scholar
  12. Bensch S, Waldenström J, Jonzén N et al (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122PubMedCrossRefGoogle Scholar
  13. Biek R, Drummond A, Poss M (2006) A virus reveals populations structure and recent demographic history of its carnivore host. Science 311:538–541PubMedCrossRefGoogle Scholar
  14. Blouin M, Yowell C, Courtney C et al (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014PubMedGoogle Scholar
  15. Booth C, Elliott P (2003) Hematological responses to hematozoa in North America and neotropical songbirds. Comp Biochem Physiol 133:451–467Google Scholar
  16. Chamberlain CP, Blum JD, Holmes RT et al (1997) The use of stable isotope tracers for identifying populations of migratory birds. Oecologia 109:132–141CrossRefGoogle Scholar
  17. Cosgrove CL, Knowles SCL, Day KP et al (2006) No evidence for avian malaria infection during the nestling phase in a passerine bird. J Parasitol 92:1302–1304PubMedCrossRefGoogle Scholar
  18. Criscione C, Blouin M (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198–202PubMedGoogle Scholar
  19. Davidar P, Morton E (1993) Living with parasites: prevalence of a blood parasite and its effect on survivorship in the Purple Martin. Auk 110:109–116Google Scholar
  20. Dumbacher J, Pratt T, Fleischer R (2003) Phylogeny of the owlet-nightjars (Aves: Aegothelidae) based on mitochondrial DNA sequence. Mol Phylogenet Evol 29:540–549PubMedCrossRefGoogle Scholar
  21. Durrant KL, Beadell JS, Ishtiaq F et al (2006) Avian Hematozoa in South America: a comparison of temperate and tropical zones. Ornithol Monogr 60:98–111CrossRefGoogle Scholar
  22. Escalante A, Freeland D, Collins W et al (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc R Soc Lond B 95:8124–8129Google Scholar
  23. Fallon SM, Ricklefs RE, Swanson BL, Bermingham E (2003) Detecting avian malaria: an improved polymerase chain reaction diagnostic. J Parasitol 89:1044–1047PubMedCrossRefGoogle Scholar
  24. Fallon S, Fleischer R, Graves G (2006) Malarial parasites as geographical markers in migratory birds? Biol Lett 2:213–216PubMedCrossRefGoogle Scholar
  25. Falush D, Wirth T, Linz B et al (2003) Traces of human migrations in helicobacter pylori populations. Science 299:1582–1585PubMedCrossRefGoogle Scholar
  26. Greiner E, Bennett G, White E et al (1975) Distribution of the avian hematozoa of North America. Can J Zool 53:1762–1787PubMedCrossRefGoogle Scholar
  27. Gylfe A, Bergström S, Lundström J et al (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725PubMedCrossRefGoogle Scholar
  28. Haig SM, Gratto-Trevor CL, Mullins TD et al (1997) Population identification of western hemisphere shorebirds throughout the annual cycle. Mol Ecol 6:413–427CrossRefGoogle Scholar
  29. Hasselquist D, Östman Ö, Waldenström J et al (2007) Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. J Ornithol. Early Online PublishingGoogle Scholar
  30. Hellgren O, Waldenström J, Peréz-Tris J et al (2007) Detecting shifts of transmission in avian blood parasites – a phylogenetic approach. Mol Ecol 16:1281–1290PubMedCrossRefGoogle Scholar
  31. Hobson K, Wassenaar L (1997) Linking breeding and wintering grounds of Neotropical migrant songbirds using stable isotopic analysis of feathers. Oecologia 109:142–148CrossRefGoogle Scholar
  32. Hobson K, McFarland K, Wassenaar L et al (2001) Linking breeding and wintering grounds of Bicknell’s thrushes using stable isotope analyses of feathers. Auk 118:16–23CrossRefGoogle Scholar
  33. Hobson K, Aubry Y, Wassenaar L (2004) Migratory connectivity in Bicknell’s thrush: locating missing populations with hydrogen isotopes. Condor 106:905–909CrossRefGoogle Scholar
  34. Hubalek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659PubMedGoogle Scholar
  35. Ishtiaq F, Beadell JS, Baker AJ et al (2006) Prevalence and evolutionary relationships of haemotozoan parasites in native versus introduced populations of common myna Acridotheres tristis. Proc R Soc B: Biol Sci 273:587–594CrossRefGoogle Scholar
  36. Jarvi S, Atkinson CT, Fleischer RC (2001) Immunogenetics and resistance to avian malaria in Hawaiian honeycreepers (Drepanidinae). Stud Avian Biol 22:254–263Google Scholar
  37. Kimura M, Clegg SM, Lovette IJ et al. (2002) Phylogeographical approaches to assessing demographic connectivity between breeding and overwintering regions in the Nearctic-Neotropical warbler (Wilsonia pusilla). Mol Ecol 11:1605–1616PubMedCrossRefGoogle Scholar
  38. Klei T, DeGiusti D (1975) Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. J Wildl Dis 11:130–134PubMedGoogle Scholar
  39. Latta SC, Baltz ME (1997) Population limitation in neotropical migratory birds: comments on Rappole and McDonald (1994). Auk 114:754–762Google Scholar
  40. Lovette IJ, Clegg SM, Smith TB (2004) Limited utility of mtDNA markers for determining connectivity among breeding and overwintering locations in three neotropical migrant birds. Conserv Biol 18:156–166CrossRefGoogle Scholar
  41. Marra P, Hobson K, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886PubMedCrossRefGoogle Scholar
  42. Martell MS, Henny C, Nye P et al (2001) Fall migration routes, timing, and wintering sites of North American Ospreys as determined by satellite telemetry. Condor 103:715–724CrossRefGoogle Scholar
  43. Merino S, Potti J (1995) High prevalence of Hematozoa in Nestlings of a Passerine Species, the Pied Flycatcher (Ficedula hypoleuca). Auk 112:1041–1043Google Scholar
  44. Merino S, Potti J (1995) High prevalence of hematozoa in nestlings of a passerine species, the Pied Flycatcher (Ficedula hypoleuca). Auk 112:1041–1043Google Scholar
  45. Milot E, Gibbs HL, Hobson K (2000) Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia). Mol Ecol 9:667–681PubMedCrossRefGoogle Scholar
  46. Paul R, Nu VAT, Krettli AU et al (2002) Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proc R Soc Lond B 269:2551–2557CrossRefGoogle Scholar
  47. Pérez-Tris J, Bensch S (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8:838–845CrossRefGoogle Scholar
  48. Peterson AT, Vieglais DA, Andreasen JK (2003) Migratory birds modeled as critical transport agents for West Nile virus in North America. Vector-Borne Zoonotic Dis 3:27–37PubMedCrossRefGoogle Scholar
  49. Pitra C, D’Aloia MA, Lieckfeldt D et al (2004) Genetic variation across the current range of the Asian houbara bustard (Chlamydotis undulate macqueeni), Conserv Genet 5:205–215CrossRefGoogle Scholar
  50. Richard FA, Sehgal RNM, Jones HI et al (2002) A comparative analysis of PCR-based detection methods for avian malaria. J Parasitol 88:819–822PubMedGoogle Scholar
  51. Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B 269:885–892CrossRefGoogle Scholar
  52. Rintamäki PT, Ojanen O, Pakkala H et al (1998) Blood parasites of migrating Willow Warblers (Phylloscopus trochilus) at a stopover site. Can J Zool 76:984–988CrossRefGoogle Scholar
  53. Robbins CS, Sauer JR, Greenberg RS et al (1989) Population declines in North American birds that migrate to the neotropics. Proc Natl Acad Sci USA 86:7658–7662PubMedCrossRefGoogle Scholar
  54. Robinson S, Thompson F III, Donovan T et al (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990PubMedCrossRefGoogle Scholar
  55. Rubenstein DR, Chamberlain CP, Holmes RT et al (2002) Linking breeding and wintering ranges of a migratory songbird using stable isotopes. Science 295:1062–1065PubMedCrossRefGoogle Scholar
  56. Sillett TS, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. J Anim Ecol 71:296–308CrossRefGoogle Scholar
  57. Slatkin M (2004) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefGoogle Scholar
  58. Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23:307–314CrossRefGoogle Scholar
  59. Super P, van Riper C III (1995) A comparison of avian hematozoan epizootiology in two California coastal scrub communities. J Wildl Dis 31:447–461PubMedGoogle Scholar
  60. Swofford DL (1999) paup*: Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MAGoogle Scholar
  61. Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774PubMedCrossRefGoogle Scholar
  62. Tankersley R, Orvis K (2003) Modeling the geography of migratory pathways and stopover habitats for neotropical migratory birds. Conserv Ecol 7(1):7Google Scholar
  63. Valkiunas G (2004) Avian malarial parasites and other haemosporidians. CRC PressGoogle Scholar
  64. Waldenström J, Bensch S, Kiboi S et al (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554PubMedCrossRefGoogle Scholar
  65. Waldenström J, Bensch S, Hasselquist D et al (2004) A new nested polymerase chain reaction method very efficient in detecting plasmodium and haemoproteus infections from avian blood. J Parasitol 90:191–194PubMedCrossRefGoogle Scholar
  66. Wassenaar L, Hobson K (2000) Stable-carbon and hydrogen isotope ratios reveal breeding origins of red-winged blackbirds. Ecol Appl 10:911–916CrossRefGoogle Scholar
  67. Weatherhead P, Bennet G (1992) Ecology of parasitism of brown-headed cowbirds by haematozoa. Can J Zool 70:1–7CrossRefGoogle Scholar
  68. Webster MS, Marra PP, Haig SM et al (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83CrossRefGoogle Scholar
  69. Wennerberg L, Klaassen M, Lindstrom A (2002) Geographical variation and population structure in the white-rumped sandpiper Calidris fuscicollis as shown by morphology, mitochondrial DNA and carbon isotope ratios. Oecoloiga 131:390–390Google Scholar
  70. Wiersch SC, Maier WA, Kampen H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitol Res 95:90–94CrossRefGoogle Scholar
  71. Wirth T, Meyer A, Achtman M (2005) Deciphering host migrations and origins by means of their microbes. Mol Ecol 14:3289–3306PubMedCrossRefGoogle Scholar
  72. Woodworth B, Atkinson CT, LaPointe D et al (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci USA 102:1531–1536PubMedCrossRefGoogle Scholar

Copyright information

© US Government 2008

Authors and Affiliations

  • K. M. Pagenkopp
    • 1
    • 2
    • 3
  • J. Klicka
    • 4
  • K. L. Durrant
    • 1
  • J. C. Garvin
    • 5
  • R. C. Fleischer
    • 1
    • 2
  1. 1.Genetics ProgramNational Museum of Natural History and National Zoological Park, Smithsonian InstitutionWashingtonUSA
  2. 2.Department of BiologyAmerican UniversityWashingtonUSA
  3. 3.Department of Environmental and Aquatic Animal HealthVirginia Institute of Marine Science, The College of William and MaryGloucester PointUSA
  4. 4.Marjorie Barrick Museum of Natural HistoryUniversity of Nevada Las VegasLas VegasUSA
  5. 5.Department of Biological SciencesUniversity of Wisconsin-MilwaukeeMilwaukeeUSA

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