Diverse avian malaria and other haemosporidian parasites in Andean house wrens: Evidence for regional co-diversification by host-switching

Journal of Avian Biology

Volumn 45, Issue 4, 2014, Pages 374-386

  Galen, Spencer C ^a   Witt, Christopher C ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COEVOLUTION; GENERALIST; GENETIC STRUCTURE; GEOGRAPHICAL VARIATION; HOST SPECIFICITY; HOST-PARASITE INTERACTION; MALARIA; MITOCHONDRIAL DNA; PASSERINE;

ANDES; PERU;

AVES; HAEMOPROTEUS; HAEMOSPORIDA; LEUCOCYTOZOON; TROGLODYTES; TROGLODYTES AEDON;

EID: 84904062686     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/jav.00375     Document Type: Article

References (83)

1. Beadell J. S., Gering E., Austin J., Dumbacher J. P., Peirce M. A., Pratt T. K., Atkinson C. T. and Fleischer R. C. 2004. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. - Mol. Ecol. 13: 3829-3844.
2. Beadell J. S., Covas R., Gebhard C., Ishtiaq F., Melo M., Schmidt B. K., Perkins S. L., Graves G. R. and Fleischer R. C. 2009. Host associations and evolutionary relationships of avian blood parasites from west Africa. - Int. J. Parasitol. 39: 257-266.
3. Benham P. M., Beckman E. J., DuBay S. G., Flores L. M., Johnson A. B., Lelevier M. J., Schmitt C. J., Wright N. A. and Witt C. C. 2011. Satellite imagery reveals new critical habitat for endangered bird species in the high Andes of Peru. - Endang. Species Res. 13: 145-157.
4. Bensch S., Stjernman M., Hasselquist D., Östman Ö., Hansson B., Westerdahl H. and Pinheiro R. T. 2000. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. - Proc. R. Soc. B 267: 1583-1589.
5. Bensch S., Pérez-Tris J., Waldenström J. and Hellgren O. 2004. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? - Evolution 58: 1617-1621.
6. Bensch S., Hellgren O. and Pérez-Tris J. 2009. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. - Mol. Ecol. Resour. 9: 1353-1358.
7. Bensch S., Hellgren O., Križanauskiene A., Palinauskas V., Valkiunas G., Outlaw D. and Ricklefs R. E. 2013. How can we determine the molecular clock of malaria parasites? - Trends Parasitol. 29: 363-369.
8. Bond J. 1956. Notes on Peruvian birds II. - Proc. Acad. Nat. Sci. Phil. 108: 227-247.
9. Brown J. H. 1984. On the relationship between abundance and distribution of species. - Am. Nat. 124: 255-279.
10. Burney C. W. and Brumfield R. T. 2009. Ecology predicts levels of genetic differentiation in neotropical birds. - Am. Nat. 174: 358-368.
11. Chapman F. M. and Griscom L. 1924. The house wrens of the genus Troglodytes. - Bull. Am. Mus. Nat. Hist. 50: 279-304.
12. Chaves J. A., Pollinger J. P., Smith T. B. and LeBuhn G. 2007. The role of geography and ecology in shaping the phylogeography of the speckled hummingbird (Adelomyia melanogenys) in Ecuador. - Mol. Phylogenet. Evol. 43: 795-807.
13. Clement M., Posada D. and Crandall K. 2000. TCS: a computer program to estimate gene genealogies. - Mol. Ecol. 9: 1657-1660.
14. Darriba D., Taboada G. L., Doallo R. and Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. - Nat. Methods 9: 772.
15. de Rodriguez M. C. and Wirth W. W. 1986. A new species of man-biting Culicoides from the high Andes of Colombia (Diptera: Ceratopogonidae). - Fla. Entomol. 69: 311-314.
16. de Vienne D. M., Refrégier G., López-Villavicencio M., Tellier A., Hood M. E. and Giraud T. 2013. Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. - New Phytol. 198: 347-385.
17. Dickinson E. C. 2003. The Howard and Moore complete checklist of the birds of the world. - Princeton Univ. Press.
18. Donovan T. A., Schrenzel M., Tucker T. A., Pessier A. P. and Stalis I. H. 2008. Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases. - J. Vet. Diagn. Invest. 20: 304-313.
19. Drummond A. J., Suchard M. A., Xie D. and Rambaut A. 2012. Bayesian Phylogenetics with BEAUti and the BEAST1.7. - Mol. Biol. Evol. 29: 1969-1973.
20. Durrant K. L., Reed J. L., Jones P. J., Dallimer M., Cheke R. A., McWilliam A. N. and Fleischer R. C. 2007. Variation in haematozoan parasitism at local and landscape levels in the red-billed quelea Quelea quelea. - J. Avian Biol. 38: 662-671.
21. Durrant K. L., Marra P. P., Fallon S. M., Colbeck G. J., Gibbs H. L., Hobson K. A., Norris D. R., Bernik B., Lloyd V. L. and Fleischer R. C. 2008. Parasite assemblages distinguish populations of a migratory passerine on its breeding grounds. - J. Zool. 274: 318-326.
22. Fallon S. M., Bermingham E. and Ricklefs R. E. 2005. Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. - Am. Nat. 165: 466-480.
23. Fallon S. M., Fleischer R. C. and Graves G. R. 2006. Malarial parasites as geographical markers in migratory birds? - Biol. Lett. 2: 213-216.
24. Fecchio A., Lima M. R., Svensson-Coelho M., Marini M. Â. and Ricklefs R. E. 2013. Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. - Parasitology 140: 181-192.
25. Ferrell S. T., Snowden K., Marlar A. B., Garner M. and Lung N. P. 2007. Fatal hemoprotozoal infections in multiple avian species in a zoological park. - J. Zool. Wildl. Med. 38: 309-316.
26. Fjeldså J. and Krabbe N. 1990. Birds of the High Andes. - Zool. Mus., Univ. of Copenhagen.
27. Futuyma D. J. and Moreno G. 1988. The evolution of ecological specialization. - Annu. Rev. Ecol. Syst. 19: 207-233.
28. Guindon S. and Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. - Syst. Biol. 52: 696-704.
29. Harmon L. J., Weir J. T., Brock C. D., Glor R. E. and Challenger W. 2008. GEIGER: investigating evolutionary radiations. - Bioinformatics 24: 129-131.
30. Hellgren O., Waldenström J. and Bensch S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. - J. Parasitol. 90: 797-802.
31. Hellgren O., Waldenström J., Pérez-Tris J., Szöllosi E., Hasselquist D., Križanauskiene A., Ottosson U. and Bensch S. 2007. Detecting shifts of transmission areas in avian blood parasites - a phylogenetic approach. - Mol. Ecol. 16: 1281-1290.
32. Hellgren O., Pérez-Tris J. and Bensch S. 2009. A jack- of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. - Ecology 90: 2840-2849.
33. Hijmans R. J., Cameron S. E., Parra J. L., Jones P. G. and Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. - Int. J. Climatol. 25: 1965-1978.
34. Hoekstra H. E., Krenz J. G. and Nachman M. W. 2005. Local adaptation in the rock pock mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. - Heredity 94: 217-228.
35. Janzen D. H. 1980. When is it coevolution? - Evolution 34: 611-612.
36. Jenkins T. and Owens I. P. F. 2011. Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance-occupancy relationship? - Mol. Ecol. 20: 3910-3920.
37. Jenkins T., Thomas G. H., Hellgren O. and Owens I. P. F. 2012. Migratory behavior of birds affects their coevolu tionary relationship with blood parasites. - Evolution 66: 740-751.
38. Johnson K. P., Adams R. J., Page R. D. and Clayton D. H. 2003. When do parasites fail to speciate in response to host speciation? - Syst. Biol. 52: 37-47.
39. Johnson M. T. J. and Stinchcombe J. R. 2007. An emerging synthesis between community ecology and evolutionary biology. - Trends Ecol. Evol. 22: 250-257.
40. Jombart T. 2008. adegenet: a R package for the multivariate analysis of genetic markers. - Bioinformatics 24: 1403-1405.
41. Kembel S. W., Cowan P. D., Helmus M. R., Cornwell W. K., Morlon H., Ackerly D. D., Blomberg S. P. and Webb C. O. 2010. Picante: R tools for integrating phylogenies and ecology. - Bioinformatics 26: 1463-1464.
42. Lacorte G. A., Félix G. M. F., Pinheiro R. R. B., Chaves A. V., Almeida-Neto G., Neves F. S., Leite L. O., Santos F. R. and Braga É. M. 2013. Exploring the diversity and distribution of neotropical avian malaria parasites - a molecular survey from southeast Brazil. - PLoS One 8: e57770.
43. LaPointe D. A., Lee Goff M. and Atkinson C. T. 2010. Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. - J. Parasitol. 96: 318-324.
44. Lerner H. R. L., Meyer M., James H. F., Hofreiter M. and Fleischer R. C. 2011. Multi-locus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. - Curr. Biol. 21: 1-7.
45. Librado P. and Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. - Bioinformatics 25: 1451-1452.
46. Loiseau C., Harrigan R. J., Cornel A. J., Guers S. L., Dodge M., Marzec T., Carlson J. S., Seppi B. and Sehgal R. N. M. 2012. First evidence and predictions of Plasmodium transmission in Alaskan bird populations. - PLoS One 7: e44729.
47. Maddison W. P. and Maddison D. R. 2011. Mesquite: a modular system for evolutionary analysis, ver. 2.75. - .
48. McCracken K. G., Bulgarella M., Johnson K. P., Kuhner M. K., Trucco J., Valqui T. H., Wilson R. E. and Peters J. L. 2009. Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the βA hemoglobin subunit of yellow-billed pintails in the Andes. - Mol. Biol. Evol. 26: 815-827.
49. Medeiros M. C. I., Hamer G. L. and Ricklefs R. E. 2013. Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites. - Proc. R. Soc. B 280: 20122947.
50. Merino S., Moreno J., Vásquez R. A., Martínez J., Sánchez-Monsálvez I., Estades C. F., Ippi S., Sabat P., Rozzi R. and McGehee S. 2008. Hematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. - Austral Ecol. 33: 329-340.
51. Milá B., Wayne R. K., Fitze P. and Smith T. B. 2009. Divergence with gene flow and fine-scale phylogeographical structure in the wedge-billed woodcreeper, Glyphorynchus spirurus, a neotropical rainforest bird. - Mol. Ecol. 18: 2979-2995.
52. Nieberding C. M. and Olivieri I. 2007. Parasites: proxies for host genealogy and ecology? - Trends Ecol. Evol. 22: 156-165.
53. Nyári Á. S. 2007. Phylogeographic patterns, molecular and vocal differentiation, and species limits in Schiffornis turdina (Aves). - Mol. Phylogenet. Evol. 44: 154-164.
54. Olias P., Wegelin M., Zenker W., Freter S., Gruber A. D. and Klopfleisch R. 2011. Avian malaria deaths in parrots, Europe. - Emerg. Infect. Dis. 17: 950-952.
55. Outlaw D. C. and Ricklefs R. E. 2011. Rerooting the evolutionary tree of malaria parasites. - Proc. Natl Acad. Sci. USA 108: 13183-13187.
56. Page R. D. M. 2003. Tangled trees: phylogeny, cospeciation and coevolution. - Univ. of Chicago Press.
57. Palinauskas V., Valkiunas G., Bolshakov C. V. and Bensch S. 2008. Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. - Exp. Parasitol. 120: 372-380.
58. Palinauskas V., Valkiunas G., Križanauskiene A., Bensch S. and Bolshakov C. V. 2009. Plasmodium relictum (lineage P-SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on treatment with Malarone. - Exp. Parasitol. 123: 134-139.
59. Parker D. M., Zavortink T. J., Billo T. J., Valdez U. and Edwards J. S. 2012. Mosquitoes and other arthropod macro fauna associated with tank bromeliads in a Peruvian cloud forest. - J. Am. Mosq. Control Assoc. 28: 45-46.
60. Pérez-Rodríguez A., Fernández-González S., de la Hera I. and Pérez-Tris J. 2013. Finding the appropriate variables to model the distribution of vector-borne parasites with different environmental preferences: climate is not enough. - Global Change Biol. 19: 3245-3253.
61. Pérez-Tris J., Hellgren O. and Križanauskiene A. 2007. Within-host speciation of malaria parasites. - PLoS One 2: e235.
62. Rambaut A. and Drummond A. J. 2007. Tracer ver. 1.4. - .
63. Rees P. H. 1994. Highland malaria. - East Afr. Med. J. 71: 1.
64. Remsen J. V. Jr, Cadena C. D., Jaramillo A., Nores M., Pacheco J. F., Perez-Eman J., Robbins M. B., Stiles F. G., Stotz D. F. and Zimmer K. J. 2013. A classification of the bird species of South America. - Am. Ornithol. Union, Ver. 7 Feb 2013.
65. Ricklefs R. E. and Fallon S. M. 2002. Diversification and host switching in avian malaria parasites. - Proc. R. Soc. B 269: 885-892.
66. Ricklefs R. E. and Outlaw D. C. 2010. A molecular clock for malaria parasites. - Science 329: 226-229.
67. Ricklefs R. E., Fallon S. M. and Bermingham E. 2004. Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. - Syst. Biol. 53: 111-119.
68. Ricklefs R. E., Swanson B. L., Fallon S. M., MartÍnez-AbraÍn A., Scheuerlein A., Gray J. and Latta S. C. 2005. Community relationships of avian malaria parasites in southern Missouri. - Ecol. Monogr. 75: 543-559.
69. Ricklefs R. E., Dodge Gray J., Latta S. C. and Svensson-Coelho M. 2011. Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles. - J. Avian Biol. 42: 570-584.
70. Ronquist F. and Huelsenbeck J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574.
71. Santiago-Alarcon D., Bloch R., Rolshausen G., Schaefer H. M. and Segelbacher G. 2011. Prevalence, diversity, and interaction patterns of avian haemosporidians in a four-year study of blackcaps in a migratory divide. - Parasitology 138: 824-835.
72. Schall J. J. and St Denis K. M. 2010. Lack of sequence variation of the mitochondrial cytochrome b gene from a malaria parasite, Plasmodium mexicanum. - J. Parasitol. 96: 827-829.
73. Schulenberg T. S., Stotz D. F., Lane D. F., O'neill J. P. and Parker T. A. 2007. Birds of Peru: revised and updated edition. - Princeton Univ. Press.
74. Sehgal R. N. M., Buermann W., Harrigan R. J., Bonneaud C., Loiseau C., Chasar A., Sepil I., Valkiunas G., Iezhova T., Saatchi S. and Smith T. B. 2011. Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. - Proc. R. Soc. B 278: 1025-1033.
75. Smith B. T. and Klicka J. 2010. The profound influence of the Late Pliocene Panamanian uplift on the exchange, diversification, and distribution of New World birds. - Ecography 33: 333-342.
76. Sol D., Jovani R. and Torres J. 2000. Geographical variation in blood parasites in feral pigeons: the role of vectors. - Ecography 23: 307-314.
77. Sorenson M. D., Ast J. C., Dimcheff D. E., Yuri T. and Mindell D. P. 1999. Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. - Mol. Phylogenet. Evol. 12: 105-114.
78. Szöllosi E., Cichoń M., Eens M., Hasselquist D., Kempenaers B., Merino S., Nilsson J.-A, Rosivall B., Rytkönen S., Török J., Wood M. J. and Garamszegi L. Z. 2011. Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. - J. Evol. Biol. 24: 2014-2024.
79. Tamura K., Peterson D., Peterson N., Stecher G., Nei M. and Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739.
80. Valkiunas G. 2005. Avian malaria parasites and other haemosporida. - CRC Press.
81. Valkiunas G., Iezhova T. A., Križanauskiene A., Palinauskas V., Sehgal R. N. M. and Bensch S. 2008. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. - J. Parasitol. 94: 1395-1401.
82. Waldenström J., Bensch S., Hasselquist D. and Östman Ö. 2004. A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. - J. Parasitol. 90: 191-194.
83. Wygodzinsky P. W. and Coscarón S. 1979. Description of a black fly of the subgenus Simulium (Pternaspatha) from the high Andes of Ecuador (Diptera, Simuliidae). - Am. Mus. Novit. 2670: 1-9.