Virus Genes

, Volume 55, Issue 6, pp 802–814 | Cite as

Assessing circovirus gene flow in multiple spill-over events

  • Shubhagata Das
  • Kate Smith
  • Subir Sarker
  • Andrew Peters
  • Katherine Adriaanse
  • Paul Eden
  • Seyed A. Ghorashi
  • Jade K. Forwood
  • Shane R. RaidalEmail author
Original Paper


The establishment of viral pathogens in new host environments following spillover events probably requires adaptive changes within both the new host and pathogen. After many generations, signals for ancient cross-species transmission may become lost and a strictly host-adapted phylogeny may mimic true co-divergence while the virus may retain an inherent ability to jump host species. The mechanistic basis for such processes remains poorly understood. To study the dynamics of virus–host co-divergence and the arbitrary chances of spillover in various reservoir hosts with equal ecological opportunity, we examined structural constraints of capsid protein in extant populations of Beak and feather disease virus (BFDV) during known spillover events. By assessing reservoir-based genotype stratification, we identified co-divergence defying signatures in the evolution BFDV which highlighted primordial processes of cryptic host adaptation and competing forces of host co-divergence and cross-species transmission. We demonstrate that, despite extensive surface plasticity gathered over a longer span of evolution, structural constraints of the capsid protein allow opportunistic host switching in host-adapted populations. This study provides new insights into how small populations of endangered psittacine species may face multidirectional forces of infection from reservoirs with apparently co-diverging genotypes.


Circovirus Psittacine beak and feather disease PBFD Microbiome Viral ecology 



The authors would like to thank the contributions of Peter Copley, Sheryl Hamilton, Jocelyn Hockley, Kristy Penrose, Judy Clark and Annika Everaardt of the Orange-bellied Parrot Recovery Team, and the staff of the Australian Wildlife Health Centre (Healesville Sanctuary). SD received Charles Sturt University writing up award for completion of this manuscript.

Author contributions

The submitting author confirms that all individual co-authors have met the criteria of authorship. SD, SS, SRR, AP, JKF contributed to the conception and design. KA, PE contributed to sample collection and data analysis. SD, SS, SRR, AP, SAG contributed to method development, data analysis and interpretation. SD, SRR, AP, drafted the manuscript. SR and AP critically revised the manuscript. SRR and JKF gave final approval and agree to be accountable for all aspects of work ensuring accuracy and integrity.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial or other conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Animal sampling was obtained using guidelines set by the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (1997) and authorised by the Charles Sturt University Animal Care and Ethics Committee (permit 09/046). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

11262_2019_1702_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 24 kb)


  1. 1.
    Holmes EC, Zhang YZ (2015) The evolution and emergence of hantaviruses. Curr Opin Virol 10:27–33PubMedGoogle Scholar
  2. 2.
    Geoghegan JL, Duchene S, Holmes EC (2017) Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog 13:e1006215PubMedPubMedCentralGoogle Scholar
  3. 3.
    Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS, Calisher CH, Laughlin CA, Saif LJ, Daszak P (2008) Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72:457–470PubMedPubMedCentralGoogle Scholar
  4. 4.
    Murthy S, Couacy-Hymann E, Metzger S, Nowak K, De Nys H, Boesch C, Wittig R, Jarvis MA, Leendertz FH, Ehlers B (2013) Absence of frequent herpesvirus transmission in a nonhuman primate predator-prey system in the wild. J Virol 87:10651–10659PubMedPubMedCentralGoogle Scholar
  5. 5.
    Redman EM, Wilson K, Cory JS (2016) Trade-offs and mixed infections in an obligate-killing insect pathogen. J Anim Ecol 85:1200–1209PubMedPubMedCentralGoogle Scholar
  6. 6.
    Sullivan J, Joyce P (2005) Model selection in phylogenetics. Annu Rev Ecol Evol Syst 36:445–466Google Scholar
  7. 7.
    Page RDM (2004) In: Page RDM (ed) 2003: tangled trees. phylogeny, cospeciation and coevolution. The University of Chicago Press, Chicago. Paperback: $28. ISBN 0-226-64467-7. Ethology 110, 577–578Google Scholar
  8. 8.
    Pepin KM, Lass S, Pulliam JR, Read AF, Lloyd-Smith JO (2010) Identifying genetic markers of adaptation for surveillance of viral host jumps. Nat Rev Microbiol 8:802–813PubMedGoogle Scholar
  9. 9.
    Dennehy JJ, Friedenberg NA, Yang YW, Turner PE (2007) Virus population extinction via ecological traps. Ecol Lett 10:230–240PubMedGoogle Scholar
  10. 10.
    Shin J, MacCarthy T (2016) Potential for evolution of complex defense strategies in a multi-scale model of virus-host coevolution. BMC Evolut Biol 16:233Google Scholar
  11. 11.
    Abedon ST (1999) Bacteriophage T4 resistance to lysis-inhibition collapse. Genet Res 74:1–11PubMedGoogle Scholar
  12. 12.
    Turner PE, Elena SF (2000) Cost of host radiation in an RNA virus. Genetics 156:1465–1470PubMedPubMedCentralGoogle Scholar
  13. 13.
    Weaver SC, Brault AC, Kang W, Holland JJ (1999) Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73:4316–4326PubMedPubMedCentralGoogle Scholar
  14. 14.
    Peters A, Patterson EI, Baker BG, Holdsworth M, Sarker S, Ghorashi SA, Raidal SR (2014) Evidence of psittacine beak and feather disease virus spillover into wild critically endangered orange-bellied parrots (Neophema chrysogaster). J Wildl Dis 50:288–296PubMedGoogle Scholar
  15. 15.
    Sarker S, Patterson EI, Peters A, Baker BG, Forwood JK, Ghorashi SA, Holdsworth M, Baker R, Murray N, Raidal SR (2014) Mutability dynamics of an emergent single stranded DNA virus in a naïve host. PLoS ONE 9:e85370PubMedPubMedCentralGoogle Scholar
  16. 16.
    Sarker S, Terrón MC, Khandokar Y, Aragão D, Hardy JM, Radjainia M, Jiménez-Zaragoza M, de Pablo PJ, Coulibaly F, Luque D, Raidal SR, Forwood JK (2016) Structural insights into the assembly and regulation of distinct viral capsid complexes. Nat Commun 7:13014PubMedPubMedCentralGoogle Scholar
  17. 17.
    Khalesi B, Bonne N, Stewart M, Sharp M, Raidal SR (2005) A comparison of haemagglutination, haemagglutination inhibition and PCR for the detection of psittacine beak and feather disease virus infection and a comparison of isolates obtained from loriids. J Gen Virol 86:3039–3046PubMedGoogle Scholar
  18. 18.
    Sarker S, Ghorashi SA, Forwood JK, Bent JS, Peters A, Raidal SR (2014) Phylogeny of beak and feather disease virus in cockatoos demonstrates host generalism and multiple-variant infections within Psittaciformes. Virology 460–461:72–82PubMedGoogle Scholar
  19. 19.
    Sarker S, Forwood JK, Ghorashi SA, Peters A, Raidal SR (2015) Beak and feather disease virus genotypes in Australian parrots reveal flexible host-switching. Aust Vet J 93:471–475PubMedGoogle Scholar
  20. 20.
    Das S, Sarker S, Peters A, Ghorashi SA, Phalen D, Forwood JK, Raidal SR (2016) Evolution of circoviruses in lorikeets lags behind its hosts. Mol Phylogenet Evol 100:281–291PubMedGoogle Scholar
  21. 21.
    Varsani A, Regnard GL, Bragg R, Hitzeroth II, Rybicki EP (2011) Global genetic diversity and geographical and host-species distribution of beak and feather disease virus isolates. J Gen Virol 92:752–767PubMedGoogle Scholar
  22. 22.
    Bonne N, Clark P, Shearer P, Raidal SR (2008) Elimination of false-positive polymerase chain reaction results resulting from hole punch carryover contamination. J Vet Diagn Investig 20:60–63Google Scholar
  23. 23.
    Ypelaar I, Bassami MR, Wilcox GE, Raidal SR (1999) A universal polymerase chain reaction for the detection of psittacine beak and feather disease virus. Vet Microbiol 68:141–148PubMedGoogle Scholar
  24. 24.
    Das S, Subir S, Adriaanse K, Forwood JK, Ghorashi SA, Raidal SR (2016) Characterization of beak and feather disease virus genomes from wild musk lorikeets (Glossopsitta concinna). Genome Announc 4:e01107–e01116PubMedPubMedCentralGoogle Scholar
  25. 25.
    Das S, Sarker S, Ghorashi SA, Forwood JK, Raidal SR (2016) A comparison of PCR assays for beak and feather disease virus and high resolution melt (HRM) curve analysis of replicase associated protein and capsid genes. J Virol Methods 237:47–57PubMedGoogle Scholar
  26. 26.
    Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066PubMedPubMedCentralGoogle Scholar
  27. 27.
    Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772PubMedPubMedCentralGoogle Scholar
  28. 28.
    Guindon S, Gascuel O (2003) A Simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedGoogle Scholar
  29. 29.
    Prost S, Anderson CNK (2011) TempNet: a method to display statistical parsimony networks for heterochronous DNA sequence data. Methods Ecol Evol 2:663–667Google Scholar
  30. 30.
    Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  31. 31.
    Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361Google Scholar
  32. 32.
    Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191PubMedPubMedCentralGoogle Scholar
  33. 33.
    Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolut Bioinform Online 1:47–50Google Scholar
  34. 34.
    Balbuena JA, Míguez-Lozano R, Blasco-Costa I (2013) PACo: a novel procrustes application to cophylogenetic analysis. PLoS ONE 8:e61048PubMedPubMedCentralGoogle Scholar
  35. 35.
    Meier-Kolthoff JP, Auch AF, Huson DH, Göker M (2007) CopyCat: cophylogenetic analysis tool. Bioinformatics 23:898–900PubMedGoogle Scholar
  36. 36.
    Maldonado E, Sunagar K, Almeida D, Vasconcelos V, Antunes A (2014) IMPACT_S: integrated multiprogram platform to analyze and combine tests of selection. PLoS ONE 9:e96243PubMedPubMedCentralGoogle Scholar
  37. 37.
    Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49PubMedPubMedCentralGoogle Scholar
  38. 38.
    Hanson-Smith V, Johnson A (2016) PhyloBot: a web portal for automated phylogenetics, ancestral sequence reconstruction, and exploration of mutational trajectories. PLoS Comput Biol 12:e1004976PubMedPubMedCentralGoogle Scholar
  39. 39.
    Bienert S, Waterhouse A, de Beer Tjaart A P, Tauriello G, Studer G, Bordoli L, Schwede T (2017) The SWISS-MODEL repository—new features and functionality. Nucleic Acids Res 45:D313–D319PubMedGoogle Scholar
  40. 40.
    Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291Google Scholar
  41. 41.
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612Google Scholar
  42. 42.
    Sievers F, Higgins DG (2014) Clustal Omega, accurate alignment of very large numbers of sequences. Methods Mol Biol 1079:105–116PubMedGoogle Scholar
  43. 43.
    Messinger SM, Ostling A (2009) The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. Am Nat 174:441–454PubMedGoogle Scholar
  44. 44.
    Harkins GW, Martin DP, Christoffels A, Varsani A (2014) Towards inferring the global movement of beak and feather disease virus. Virology 450:24–33PubMedGoogle Scholar
  45. 45.
    Aiewsakun P, Katzourakis A (2016) Time-dependent rate phenomenon in viruses. J Virol 90:7184–7195PubMedPubMedCentralGoogle Scholar
  46. 46.
    Raidal SR, Sarker S, Peters A (2015) Review of psittacine beak and feather disease and its effect on Australian endangered species. Aust Vet J 93:466–470PubMedGoogle Scholar
  47. 47.
    Raidal SR (2016) In: Speer BL (ed) Current therapy in avian medicine and surgery. Elsevier, St. Louis, pp 51–58Google Scholar
  48. 48.
    Bahadur RP, Janin J (2008) Residue conservation in viral capsid assembly. Proteins Struct Funct Bioinform 71:407–414Google Scholar
  49. 49.
    Mintseris J, Weng Z (2005) Structure, function, and evolution of transient and obligate protein–protein interactions. Proc Natl Acad Sci USA 102:10930–10935PubMedGoogle Scholar
  50. 50.
    Amery-Gale J, Marenda MS, Owens J, Eden PA, Browning GF, Devlin JM (2017) A high prevalence of beak and feather disease virus in non-psittacine Australian birds. J Med Microbiol 66:1005–1013PubMedGoogle Scholar
  51. 51.
    Bonne N, Shearer P, Sharp M, Clark P, Raidal SR (2009) Assessment of recombinant beak and feather disease virus capsid protein as a vaccine for psittacine beak and feather disease. J Gen Virol 90:640–647PubMedGoogle Scholar
  52. 52.
    Raidal SR, McElnea CL, Cross GM (1993) Seroprevalence of psittacine beak and feather disease in wild psittacine birds in New South Wales. Aust Vet J 70:137–139PubMedGoogle Scholar
  53. 53.
    Lekcharoensuk P, Morozov I, Paul PS, Thangthumniyom N, Wajjawalku W, Meng XJ (2004) Epitope mapping of the major capsid protein of type 2 porcine circovirus (PCV2) by using chimeric PCV1 and PCV2. J Virol 78:8135–8145PubMedPubMedCentralGoogle Scholar
  54. 54.
    Smith-Tsurkan SD, Wilke CO, Novella IS (2010) Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types. J Gen Virol 91:1484–1493PubMedPubMedCentralGoogle Scholar
  55. 55.
    Clarke DK, Duarte EA, Elena SF, Moya A, Domingo E, Holland J (1994) The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci USA 91:4821–4824PubMedGoogle Scholar
  56. 56.
    Kassen R, Rainey PB (2004) The ecology and genetics of microbial diversity. Annu Rev Microbiol 58:207–231PubMedGoogle Scholar
  57. 57.
    Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190Google Scholar
  58. 58.
    Whitlock MC (1992) Temporal fluctuation in demographic parameters and the genetic variance among populations. Evolution 46:608–615PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Animal and Veterinary SciencesCharles Sturt UniversityWagga WaggaAustralia
  2. 2.School of Biomedical SciencesCharles Sturt UniversityWagga WaggaAustralia
  3. 3.Department of Physiology, Anatomy and Microbiology, School of Life SciencesLa Trobe UniversityMelbourneAustralia
  4. 4.Healesville SanctuaryHealesvilleAustralia

Personalised recommendations