Skip to main content

Advertisement

Log in

Comparison of beak and feather disease virus prevalence and immunity-associated genetic diversity over time in an island population of red-crowned parakeets

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Pathogen outbreaks in the wild can contribute to a population’s extinction risk. Concern over the effects of pathogen outbreaks in wildlife is amplified in small, threatened populations, where degradation of genetic diversity may hinder natural selection for enhanced immunocompetence. Beak and feather disease virus (BFDV) was detected for the first time in an island population of red-crowned parakeets (Cyanoramphus novaezelandiae) in 2008 on Little Barrier Island (Hauturu-o-Toi) of New Zealand. By 2013, the prevalence of the viral infection had significantly decreased within the population. We tested whether the population of red-crowned parakeets showed a selective response to BFDV, using neutral microsatellite and two immunity-associated genetic markers, the major histocompatibility complex (MHC) and Toll-like receptors (TLRs). We found evidence for selection at viral-associated TLR3; however, the ability of TLR3 to elicit an immune response in the presence of BFDV warrants confirmation. Alternatively, because red-crowned parakeet populations are prone to fluctuations in size, the decrease in BFDV prevalence over time may be attributed to the Little Barrier Island population dropping below the density threshold for viral maintenance. Our results highlight that natural processes such as adaptation for enhanced immunocompetence and/or density fluctuations are efficient mechanisms for reducing pathogen prevalence in a threatened, isolated population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259

    Article  PubMed  Google Scholar 

  2. de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126

    Article  Google Scholar 

  3. Skerratt LF, Berger L, Speare R et al (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125–134

    Article  Google Scholar 

  4. Heard MJ, Smith KF, Ripp KJ et al (2013) The threat of disease increases as species move toward extinction. Conserv Biol 27:1378–1388

    Article  PubMed  PubMed Central  Google Scholar 

  5. Lyles AM, Dobson AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wild Med 24:315–326

    Google Scholar 

  6. Westerdahl H, Hansson B, Bensch S et al (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J Evol Biol 17:485–492

    Article  CAS  PubMed  Google Scholar 

  7. Hawley DM, Fleischer RC (2012) Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird. PLoS One 7:e30222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988

    Article  CAS  Google Scholar 

  9. Ortiz-Catedral L, McInnes K, Hauber ME et al (2009) First report of beak and feather disease virus (BFDV) in wild red-fronted parakeets (Cyanoramphus novaezelandiae) in New Zealand. Emu 109:244–247

    Article  Google Scholar 

  10. Massaro M, Ortiz-Catedral L, Julian L et al (2012) Molecular characterisation of beak and feather disease virus (BFDV) in New Zealand and its implications for managing an infectious disease. Arch Virol 157:1651–1663

    Article  CAS  PubMed  Google Scholar 

  11. Pass DA, Perry RA (1984) The pathology of psittacine beak and feather disease. Aust Vet J 61:69–74

    Article  CAS  PubMed  Google Scholar 

  12. Raidal SR (1995) Viral skin diseases of birds. Semin Avian Exot Pet Med Viral Dis 4:72–82

    Article  Google Scholar 

  13. Todd D (2000) Circoviruses: immunosuppressive threats to avian species: a review. Avian Pathol 29:373–394

    Article  CAS  PubMed  Google Scholar 

  14. Ha HJ, Anderson IL, Alley MR et al (2007) The prevalence of beak and feather disease virus infection in wild populations of parrots and cockatoos in New Zealand. N Z Vet J 55:235–238

    Article  CAS  PubMed  Google Scholar 

  15. Harkins GW, Martin DP, Christoffels A et al (2014) Towards inferring the global movement of beak and feather disease virus. Virology 450–451:24–33

    Article  PubMed  Google Scholar 

  16. Jackson B, Varsani A, Holyoake C et al (2015) Emerging infectious disease or evidence of endemicity? A multi-season study of Beak and feather disease virus in wild Red-crowned Parakeets (Cyanoramphus novaezelandiae). Arch Virol. 160:2283–2292

    Article  CAS  PubMed  Google Scholar 

  17. Ritchie BW, Niagro FD, Latimer KS et al (1991) Routes of prevalence of shedding of psittacine beak and feather disease virus. Am J Vet Res 52:1804–1809

    CAS  PubMed  Google Scholar 

  18. Rahaus M, Desloges N, Probst S et al (2008) Detection of beak and feather disease virus DNA in embryonated eggs of psittacine birds. Vet Med 53:53–58

    CAS  Google Scholar 

  19. Jarne P, Lagoda PJ (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429

    Article  CAS  PubMed  Google Scholar 

  20. Garstka MA, Fish A, Celie PHN et al (2015) The first step of peptide selection in antigen presentation by MHC class I molecules. Proc Natl Acad Sci USA 112:1505–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Alcaide M, Edwards SV, Cadahía L et al (2009) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355

    Article  CAS  Google Scholar 

  22. Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145

    Article  CAS  PubMed  Google Scholar 

  23. Brownlie R, Allan B (2011) Avian toll-like receptors. Cell Tissue Res 343:121–130

    Article  CAS  PubMed  Google Scholar 

  24. Ritchie BW, Niagro FD, Lukert PD et al (1989) Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology 171:83–88

    Article  CAS  PubMed  Google Scholar 

  25. Ortiz-Catedral L, Brunton DH (2009) Nesting sites and nesting success of reintroduced red-crowned parakeets (Cyanoramphus novaezelandiae) on Tiritiri Matangi Island, New Zealand. N Z J Zool 35:1–10

    Article  Google Scholar 

  26. Ortiz-Catedral L, Hauber ME, Brunton DH (2013) Growth and survival of nestlings in a population of red-crowned parakeets (Cyanoramphus novaezelandiae) free of introduced mammalian nest predators on Tiritiri Matangi Island, New Zealand. N Z J Ecol 37:370–378

    Google Scholar 

  27. Taylor RH (1985) Status, habits and conservation of Cyanoramphus parakeets in the New Zealand region. ICBP Tech Publ 3:195–211

    Google Scholar 

  28. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158

    Article  Google Scholar 

  29. Ortiz-Catedral L, Kurenbach B, Massaro M et al (2010) A new isolate of Beak and feather disease virus from endemic wild Red-fronted parakeets (Cyanoramphus novaezelandiae) in New Zealand. Arch Virol 155:613–620

    Article  CAS  PubMed  Google Scholar 

  30. Chan C, Ballantyne KN, Lambert DM et al (2005) Characterization of variable microsatellite loci in Forbes’ parakeet (Cyanoramphus forbesi) and their use in other parrots. Conserv Genet 6:651–654

    Article  Google Scholar 

  31. Andrews BJ, Hale ML, Steeves TE (2012) Characterisation of microsatellite loci in the critically endangered orange-fronted kākāriki (Cyanoramphus malherbi) isolated using genomic next generation sequencing. Conserv Genet Resour 5:235–237

    Article  Google Scholar 

  32. Knafler GJ, Jamieson IG, Robertson BC (2014) Microsatellite primers for the red-crowned parakeet (Cyanoramphus novaezelandiae). Conserv Genet Resour 7:419–421

    Article  Google Scholar 

  33. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  34. van Oosterhout C, Hutchinson WF, Wills DPM et al (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  35. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  36. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  37. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/

  38. Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci-implications for evolutionary analysis. Gene 427:117–123

    Article  CAS  PubMed  Google Scholar 

  39. Knafler GJ, Jamieson IG (2014) Primers for the amplification of major histocompatibility complex class I and II loci in the recovering red-crowned parakeet. Conserv Genet Resour 6:37–39

    Article  Google Scholar 

  40. Yuhki N, O’Brien SJ (1990) DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA 87:836–840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  42. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  43. Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  44. Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  Google Scholar 

  45. Delport W, Poon AFY, Frost SDW et al (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kosakovsky Pond SL, Posada D, Gravenor MB et al (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098

    Article  PubMed  Google Scholar 

  47. Kosakovsky Pond SL, Frost SDW (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222

    Article  PubMed  Google Scholar 

  48. Sutton JT, Robertson BC, Grueber CE et al (2013) Characterization of MHC class II B polymorphism in bottlenecked New Zealand saddlebacks reveals low levels of genetic diversity. Immunogenetics 65:619–633

    Article  CAS  PubMed  Google Scholar 

  49. Sandberg M, Eriksson L, Sjo M (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 2623:2481–2491

    Article  Google Scholar 

  50. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  51. Sepil I, Moghadam HK, Huchard E et al (2012) Characterization and 454 pyrosequencing of major histocompatibility complex class I genes in the great tit reveal complexity in a passerine system. BMC Evol Biol 12:68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sutton JT, Robertson BC, Jamieson IG (2015) MHC variation reflects the bottleneck histories of New Zealand passerines. Mol Ecol 24:362–373

    Article  PubMed  Google Scholar 

  53. Grueber CE, Jamieson IG (2013) Primers for amplification of innate immunity toll-like receptor loci in threatened birds of the Apterygiformes, Gruiformes, Psittaciformes and Passeriformes. Conserv Genet Resour 5:1043–1047

    Article  Google Scholar 

  54. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Kundu S, Faulkes CG, Greenwood AG et al (2012) Tracking viral evolution during a disease outbreak: the rapid and complete selective sweep of a circovirus in the endangered Echo parakeet. J Virol 86:5221–5229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Jackson B, Lorenzo A, Theuerkauf J et al (2014) Preliminary surveillance for beak and feather disease virus in wild parrots of New Caledonia: implications of a reservoir species for Ouvea Parakeets. Emu 114:283–289

    Article  Google Scholar 

  59. Peters A, Patterson EI, Baker BGB et al (2014) Evidence of psittacine beak and feather disease virus spillover into wild critically endangered orange-bellied parrots (Neophema chrysogaster). J Wildl Dis 50:288–296

    Article  CAS  PubMed  Google Scholar 

  60. Sarker S, Ghorashi S, Forwood J et al (2014) Phylogeny of beak and feather disease virus in cockatoos demonstrates host generalism and multiple-variant infections within Psittaciformes. Virol 460:72–82

    Article  Google Scholar 

  61. Regnard G, Rutledge S, Martin R et al (2015) Beak and feather disease virus: correlation between viral load and clinical signs in wild Cape parrots (Poicephalus robustus) in South Africa. Arch Virol 160:339–344

    Article  CAS  PubMed  Google Scholar 

  62. Wobeser G (2002) Disease management strategies for wildlife disease management—important concepts. Rev Sci Tech Off Int Epiz 21:159–178

    Article  CAS  Google Scholar 

  63. Shim E, Galvani AP (2009) Evolutionary repercussions of avian culling on host resistance and influenza virulence. PLoS One 4:e5508

    Article  Google Scholar 

  64. Lane-deGraaf KE, Amish SJ, Gardipee F et al (2014) Signatures of natural and unnatural selection: evidence from an immune system gene in African buffalo. Conserv Genet 16:289–300

    Article  Google Scholar 

  65. Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19:3894–3908

    Article  PubMed  Google Scholar 

  66. Sutton JT, Nakagawa S, Robertson BC et al (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420

    Article  PubMed  Google Scholar 

  67. Grueber CE, Knafler GJ, King TM et al (2015) Toll-like receptor diversity in 10 threatened bird species : relationship with microsatellite heterozygosity. Conserv Genet 16:595–611

    Article  CAS  Google Scholar 

  68. Greene TC (2013) Red-crowned parakeet. In: Miskelly CM (ed) New Zealand Birds Online. http://www.nzbirdsonline.org.nz

  69. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52

    Article  CAS  PubMed  Google Scholar 

  70. Takahata N, Nei M (1990) Allelic genealogy under over- dominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544

    Article  Google Scholar 

  72. Strand TM, Segelbacher G, Quintela M et al (2012) Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse? Ecol Evol 2:341–353

    Article  PubMed  PubMed Central  Google Scholar 

  73. Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll-like receptor (TLR) immunity loci in a re-introduced population of a threatened species. Mol Ecol 22:4470–4482

    Article  CAS  PubMed  Google Scholar 

  74. Aguilar A, Roemer G, Debenham S et al (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. van Oosterhout C, Joyce DA, Cummings SM et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulate). Evolution 60:2562–2574

    Article  PubMed  Google Scholar 

  76. Abdul-Careem MF, Haq K, Shanmuganathan S et al (2009) Induction of innate host responses in the lungs of chickens following infection with a very virulent strain of Marek’s disease virus. Virology 393:250–257

    Article  CAS  PubMed  Google Scholar 

  77. Wagner H, Bauer S (2006) All is not Toll: new pathways in DNA recognition. J Exp Med 203:265–268

    Article  PubMed  PubMed Central  Google Scholar 

  78. Altschul S, Gish W, Miller W (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  79. Raidal SR, Cross GM (1995) Acute necrotizing hepatitis caused by experimental infection with psittacine beak and feather disease virus. J Avian Med Surg 9:36–40

    Google Scholar 

  80. Schoemaker NJ, Dorrestein GM, Latimer KS et al (2000) Severe leukopenia and liver necrosis in young African Grey Parrots (Psittacus erithacus erithacus) infected with psittacine circovirus. Avian Dis 44:470–478

    Article  CAS  PubMed  Google Scholar 

  81. Doneley RJT (2003) Acute beak and feather disease in juvenile African Grey parrots—an uncommon presentation of a common disease. Aust Vet J 81:206–207

    Article  CAS  PubMed  Google Scholar 

  82. Robino P, Grego E, Rossi G et al (2014) Molecular analysis and associated pathology of beak and feather disease virus isolated in Italy from young Congo African grey parrots (Psittacus erithacus) with an “atypical peracute form” of the disease. Avian Pathol 43:333–344

    Article  PubMed  Google Scholar 

  83. Fellah JS, Jaffredo T, Dunon D (2008) Development of the avian immune system. Avian Immunol 4:51–66

    Article  Google Scholar 

  84. Lloyd-Smith JO, Cross PC, Briggs CJ et al (2005) Should we expect population thresholds for wildlife disease? Trends Ecol Evol 20:511–519

    Article  PubMed  Google Scholar 

  85. Elliott GP, Dilks PJ, O’Donnell CFJ (1996) The ecology of yellow-crowned parakeets (Cyanoramphus auriceps) in Nothofagus forest in Fiordland, New Zealand. New Zeal J Zool 23:249–265

    Article  Google Scholar 

  86. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Gregory Gimenez, Les McNoe, and Monika Zavodna at Otago Genomics and Bioinformatics Facility for their valuable NGS advice. Capture and sampling of red-crowned parakeets was conducted under approved permits by the New Zealand Department of Conservation (permits AK-15300-RES, AK-20666-FAU, AK-22857-FAU). This research was supported by an Allan Wilson Centre grant to IGJ and University of Otago scholarship to GJK.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabrielle J. Knafler.

Additional information

I. G. Jamieson: Deceased February 2, 2015.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 12 kb)

Supplementary material 2 (DOCX 168 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Knafler, G.J., Ortiz-Catedral, L., Jackson, B. et al. Comparison of beak and feather disease virus prevalence and immunity-associated genetic diversity over time in an island population of red-crowned parakeets. Arch Virol 161, 811–820 (2016). https://doi.org/10.1007/s00705-015-2717-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2717-3

Keywords

Navigation