Apparent vector-mediated parent-to-offspring transmission in an avian malaria-like parasite

Molecular Ecology

Volumn 24, Issue 6, 2015, Pages 1355-1363

  Chakarov, Nayden ^a   Linke, Burkhard ^a,b   Boerner, Martina ^a   Goesmann, Alexander ^a   Krüger, Oliver ^a   Hoffman, Joseph I ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

avian blood parasites; high throughput sequencing; horizontal and vertical transmission; Leucocytozoon; local transmission; vector

Indexed keywords

AVES; LEUCOCYTOZOON; RAPTORES;

GENETIC MARKER; MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; AVIAN MALARIA; DNA SEQUENCE; GENETIC MARKER; GENETICS; GENOTYPE; GERMANY; HAEMOSPORIDA; HOST PARASITE INTERACTION; MOLECULAR GENETICS; PARASITOLOGY; RAPTOR; TRANSMISSION;

ANIMALS; DNA, MITOCHONDRIAL; GENETIC MARKERS; GENOTYPE; GERMANY; HAEMOSPORIDA; HOST-PARASITE INTERACTIONS; MALARIA, AVIAN; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; RAPTORS; SEQUENCE ANALYSIS, DNA;

EID: 84924974694     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13115     Document Type: Article

References (54)

1. Anderson TJC, Haubold B, Williams JT, et al,. (2000a) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution, 17, 1467-1482.
2. Anderson TJC, Su XZ, Roddam A, Day KP, (2000b) Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Molecular Ecology, 9, 1599-1608.
3. Ashford RW, Green EE, Holmes PR, Lucas AJ, (1991) Leucocytozoon toddi in British sparrowhawks Accipiter nisus-Patterns of infection in nestlings. Journal of Natural History, 25, 269-277.
4. Awadalla P, Walliker D, Babiker H, Mackinnon M, (2001) The question of Plasmodium falciparum population structure. Trends in Parasitology, 17, 351-353.
5. Bensch S, Hellgren O, Pérez-Tris J, (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353-1358.
6. Bergstrom CT, Antia R, (2006) How do adaptive immune systems control pathogens while avoiding autoimmunity? Trends in Ecology & Evolution, 21, 22-28.
7. Boerner M, Krüger O, (2009) Aggression and fitness differences between plumage morphs in the common buzzard (Buteo buteo). Behavioral Ecology, 20, 180-185.
8. Boots M, Hudson PJ, Sasaki A, (2004) Large shifts in pathogen virulence relate to host population structure. Science, 303, 842-844.
9. Bruce MC, Donnelly CA, Alpers MP, et al,. (2000) Cross-species interactions between malaria parasites in humans. Science, 287, 845-848.
10. Bruvo R, Michiels NK, D'Souza TG, Schulenburg H, (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Molecular Ecology, 13, 2101-2106.
11. Busenberg S, Cooke K, (1993) Vertically Transmitted Diseases. Models and Dynamics. Springer, Berlin, Heidelberg.
12. Chakarov N, Krüger O, (2010) Mesopredator release by an emergent superpredator: A natural experiment of predation in a three level guild. PLoS ONE, 5, e15229.
13. Chakarov N, Boerner M, Krüger O, (2008) Fitness in common buzzards at the cross-point of opposite melanin-parasite interactions. Functional Ecology, 22, 1062-1069.
14. Chakarov N, Greiner JFW, Hauser S, et al,. (2012) Label-free enrichment of avian Leucocytozoon using flow cytometric sorting. Parasitology, 139, 1547-1552.
15. Chakarov N, Jonker RM, Boerner M, Hoffman JI, Krüger O, (2013) Variation at phenological candidate genes correlates with timing of dispersal and plumage morph in a sedentary bird of prey. Molecular Ecology, 22, 5430-5440.
16. Clark LV, Jasieniuk M, (2011) polysat: an R package for polyploid microsatellite analysis. Molecular Ecology Resources, 11, 562-566.
17. Clayton DH, Tompkins DM, (1994) Ectoparasite virulence is linked to mode of transmission. Proceedings of the Royal Society B-Biological Sciences, 256, 211-217.
18. Crosskey RW, (1990) The Natural History of Blackflies. Wiley, Chickester.
19. Dybdahl MF, Storfer A, (2003) Parasite local adaptation: red Queen versus Suicide King. Trends in Ecology & Evolution, 18, 523-530.
20. Ferreira MU, Karunaweera ND, da Silva-Nunes M, et al,. (2007) Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. Journal of Infectious Diseases, 195, 1218-1226.
21. Frank SA, (1996) Models of parasite virulence. Quarterly Review of Biology, 71, 37-78.
22. Galeotti P, Sacchi R, (2003) Differential parasitaemia in the tawny owl (Strix aluco): effects of colour morph and habitat. Journal of Zoology, 261, 91-99.
23. Gangoso L, Grande JM, Ducrest AL, et al,. (2011) MC1R-dependent, melanin-based colour polymorphism is associated with cell-mediated response in the Eleonora's falcon. Journal of Evolutionary Biology, 24, 2055-2063.
24. Gasparini J, Piault R, Bize P, Roulin A, (2009) Synergistic and antagonistic interaction between different branches of the immune system is related to melanin-based coloration in nestling tawny owls. Journal of Evolutionary Biology, 22, 2348-2353.
25. Gavin TA, Reynolds RT, Joy SM, Leslie D, May B, (1998) Genetic evidence for low frequency of extra-pair fertilizations in northern Goshawks. Condor, 100, 556-560.
26. Glutz von Blotzheim U, Bauer K, Bezzel E, (1971) Handbuch der Vögel Mitteleuropas. Aula-Verlag, Wiesbaden.
27. Goslee SC, Urban DL, (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22, 1-19.
28. Grech K, Chan BHK, Anders RF, Read AF, (2008) The impact of immunization on competition within Plasmodium infections. Evolution, 62, 2359-2371.
29. Hamilton WD, Axelrod R, Tanese R, (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566-3573.
30. Hellgren O, Waldenström J, Bensch S, (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology, 90, 797-802.
31. Hellgren O, Bensch S, Malmqvist B, (2008) Bird hosts, blood parasites and their vectors-associations uncovered by molecular analyses of blackfly blood meals. Molecular Ecology, 17, 1605-1613.
32. Henry CW, Dick JW, (1978) Separation of gametocytes of Leucocytozoon smithi from whole peripheral turkey blood. Avian Diseases, 22, 542-546.
33. Holleley CE, Geerts PG, (2009) multiplex manager 1.0: a cross-platform computer program that plans and optimizes multiplex PCR. BioTechniques, 46, 511-517.
34. Kamvar ZN, Tabima JF, Grünwald NJ, (2014) poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.
35. Knowles SCL, Wood MJ, Alves R, et al,. (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Molecular Ecology, 20, 1062-1076.
36. Krüger O, (2002) Analysis of nest occupancy and nest reproduction in two sympatric raptors: common buzzard Buteo buteo and goshawk Accipiter gentilis. Ecography, 25, 523-532.
37. Krüger O, (2008) Engines of speciation: a comparative study in birds of prey. Journal of Evolutionary Biology, 21, 861-872.
38. Krüger O, Lindström J, Amos W, (2001) Maladaptive mate choice maintained by heterozygote advantage. Evolution, 55, 1207-1214.
39. Lalubin F, Delédevant A, Glaizot O, Christe P, (2014) Natural malaria infection reduces starvation resistance of nutritionally stressed mosquitoes. Journal of Animal Ecology, 83, 850-857.
40. Levin II, Parker PG, (2014) Infection with Haemoproteus iwa affects vector movement in a hippoboscid fly-frigatebird system. Molecular Ecology, 23, 947-953.
41. Lion S, Boots M, (2010) Are parasites "prudent" in space? Ecology Letters, 13, 1245-1255.
42. Martins WS, Lucas DCS, Neves KFS, Bertioli DJ, (2009) websat-a web software for microsatellite marker development. Bioinformation, 3, 282-283.
43. Omori S, Sato Y, Toda H, et al,. (2010) Use of flow cytometry to separate Leucocytozoon caulleryi gametocytes from avian blood. Parasitology, 137, 1899-1903.
44. Palinauskas V, Dolnik OV, Valkiunas G, Bensch S, (2010) Laser microdissection microscopy and single cell PCR of avian hemosporidians. Journal of Parasitology, 96, 420-424.
45. Palinauskas V, Krizanauskiene A, Iezhova TA, et al,. (2013) A new method for isolation of purified genomic DNA from haemosporidian parasites inhabiting nucleated red blood cells. Experimental Parasitology, 133, 275-280.
46. Ricklefs RE, Fallon SM, (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London Series B-Biological Sciences, 269, 885-892.
47. Schall JJ, Vardo AM, (2007) Identification of microsatellite markers in Plasmodium mexicanum, a lizard malaria parasite that infects nucleated erythrocytes. Molecular Ecology Notes, 7, 227-229.
48. Untergasser A, Cutcutache I, Koressaar T, et al,. (2012) Primer3-new capabilities and interfaces. Nucleic Acids Research, 40, e115.
49. Valkiunas G, (2005) Avian malarial parasites and other haemosporidia. CRC Press, Boca Raton, Florida, USA.
50. Valkiunas G, Sehgal RNM, Iezhova TA, Hull AC, (2010) Identification of Leucocytozoon toddi group (Haemosporida: Leucocytozoidae), with remarks on the species taxonomy of Leucocytozoids. Journal of Parasitology, 96, 170-177.
51. Waite JL, Henry AR, Adler FR, Clayton DH, (2012) Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis. Ecology, 93, 2448-2455.
52. Waite JL, Henry AR, Owen JP, Clayton DH, (2014) An experimental test of the effects of behavioral and immunological defenses against vectors: do they interact to protect birds from blood parasites? Parasites & Vectors, 7, 104.
53. Walls SS, Kenward RE, (2001) Spatial consequences of relatedness and age in buzzards. Animal Behaviour, 61, 1069-1078.
54. Wood MJ, Cosgrove CL, Wilkin TA, et al,. (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, 16, 3263-3273.