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Pathogen invasion history elucidates contemporary host pathogen dynamics


Autoři: Vance T. Vredenburg aff001;  Samuel V. G. McNally aff001;  Hasan Sulaeman aff001;  Helen M. Butler aff001;  Tiffany Yap aff001;  Michelle S. Koo aff002;  Dirk S. Schmeller aff004;  Celeste Dodge aff001;  Tina Cheng aff001;  Gordon Lau aff001;  Cheryl J. Briggs aff005
Působiště autorů: Department of Biology, San Francisco State University, San Francisco, California, United States of America aff001;  Museum of Vertebrate Zoology, University of California Berkeley, Berkeley, California, United States of America aff002;  Center for Biological Diversity, Oakland, California, United States of America aff003;  EcoLab, Université de Toulouse, Toulouse, France aff004;  Department of Ecology Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0219981

Souhrn

Amphibians, the most threatened group of vertebrates, are seen as indicators of the sixth mass extinction on earth. Thousands of species are threatened with extinction and many have been affected by an emerging infectious disease, chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis (Bd). However, amphibians exhibit different responses to the pathogen, such as survival and population persistence with infection, or mortality of individuals and complete population collapse after pathogen invasion. Multiple factors can affect host pathogen dynamics, yet few studies have provided a temporal view that encompasses both the epizootic phase (i.e. pathogen invasion and host collapse), and the transition to a more stable co-existence (i.e. recovery of infected host populations). In the Sierra Nevada mountains of California, USA, conspecific populations of frogs currently exhibit dramatically different host/ Bd-pathogen dynamics. To provide a temporal context by which present day dynamics may be better understood, we use a Bd qPCR assay to test 1165 amphibian specimens collected between 1900 and 2005. Our historical analyses reveal a pattern of pathogen invasion and eventual spread across the Sierra Nevada over the last century. Although we found a small number of Bd-infections prior to 1970, these showed no sign of spread or increase in infection prevalence over multiple decades. After the late 1970s, when mass die offs were first noted, our data show Bd as much more prevalent and more spatially spread out, suggesting epizootic spread. However, across the ~400km2 area, we found no evidence of a wave-like pattern, but instead discovered multiple, nearly-simultaneous invasions within regions. We found that Bd invaded and spread in the central Sierra Nevada (Yosemite National Park area) about four decades before it invaded and spread in the southern Sierra Nevada (Sequoia and Kings Canyon National Parks area), and suggest that the temporal pattern of pathogen invasion may help explain divergent contemporary host pathogen dynamics.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amphibians – Frogs – Zoology – Animal diseases – Epizootics – Conservation biology – Species extinction – Evolutionary biology – Evolutionary processes – Population biology – Population dynamics – Research and analysis methods – Research facilities – Museum collections – Ecology and environmental sciences – Conservation science – Species colonization – Invasive species – Medicine and health sciences – Pathology and laboratory medicine – Pathogens


Zdroje

1. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, et al. Status and trends of amphibian declines and extinctions worldwide. Science. 2004 Dec 3;306(5702):1783–6. doi: 10.1126/science.1103538 15486254

2. Wake DB, Vredenburg VT. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences. 2008 Aug 8.

3. Daszak P, Scott DE, Kilpatrick AM, Faggioni C, Gibbons JW, Porter D. Amphibian population declines at Savannah River site are linked to climate, not chytridiomycosis. Ecology. 2005 Dec 1; 86(12):3232–7.

4. Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid patho- genic to amphibians. Mycologia. 1999 Mar 1:219–27.

5. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the national academy of sci- ences of the United States of America. 2006 Feb 28; 103(9):3165–70. doi: 10.1073/pnas.0506889103 16481617

6. Rachowicz LJ, Knapp RA, Morgan JA, Stice MJ, Vredenburg VT, Parker JM, et al. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology. 2006 Jul 1; 87(7):1671–83. doi: 10.1890/0012-9658(2006)87[1671:eidaap]2.0.co;2 16922318

7. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences. 2010 May 25; 107 (21):9689–94.

8. Catenazzi A, Lehr E, Rodriguez LO, Vredenburg VT. Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the upper Manu National Park, southeastern Peru. Conservation Biology. 2011 Apr;25(2):382–91. doi: 10.1111/j.1523-1739.2010.01604.x 21054530

9. Berger L, Hyatt AD, Speare R, Longcore JE. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of aquatic organisms. 2005 Dec 30; 68(1):51–63. doi: 10.3354/dao068051 16465834

10. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, et al. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science. 2009 Oct 23; 326(5952):582–5. doi: 10.1126/science.1176765 19900897

11. Voyles J, Vredenburg VT, Tunstall TS, Parker JM, Briggs CJ, Rosenblum EB. Pathophysiology in mountain yellow-legged frogs (Rana muscosa) during a chytridiomycosis outbreak. PLoS One. 2012 Apr 25; 7(4):e35374. doi: 10.1371/journal.pone.0035374 22558145

12. Farrer RA, Weinert LA, Bielby J, Garner TW, Balloux F, Clare F, et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences. 2011 Nov 15;108(46):18732–6.

13. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, et al. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology. 2012 Nov;21(21):5162–77. doi: 10.1111/j.1365-294X.2012.05710.x 22857789

14. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, et al. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences. 2013 Jun 4;110(23):9385–90.

15. Bataille A, Fong JJ, Cha M, Wogan GO, Baek HJ, Lee H, et al. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Molecular ecology. 2013 Aug;22(16):4196–209. doi: 10.1111/mec.12385 23802586

16. O’hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018 May 11;360(6389):621–7. doi: 10.1126/science.aar1965 29748278

17. Lips KR, Diffendorfer J, Mendelson JR III, Sears MW. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS biology. 2008 Mar 25;6(3):e72. doi: 10.1371/journal.pbio.0060072 18366257

18. Collins JP, Storfer A. Global amphibian declines: sorting the hypotheses. Diversity and distributions. 2003 Mar;9(2):89–98.

19. Briggs CJ, Knapp RA, Vredenburg VT. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences. 2010 May 3:200912886.

20. Huss M, Huntley L, Vredenburg V, Johns J, Green S. Prevalence of Batrachochytrium dendrobatidis in 120 archived specimens of Lithobates catesbeianus (American bullfrog) collected in California, 1924–2007. EcoHealth. 2013 Dec 1;10(4):339–43. doi: 10.1007/s10393-013-0895-6 24419668

21. Yap TA, Koo MS, Ambrose RF, Vredenburg VT. Introduced bullfrog facilitates pathogen invasion in the western United States. PloS one. 2018 Apr 16;13(4):e0188384. doi: 10.1371/journal.pone.0188384 29659568

22. Sette CM, Vredenburg VT, Zink AG. Reconstructing historical and contemporary disease dynamics: A case study using the California slender salamander. Biological Conservation. 2015 Dec 31; 192:20–9.

23. Yap TA, Gillespie L, Ellison S, Flechas SV, Koo MS, Martinez AE, et al. Invasion of the fungal pathogen Batrachochytrium dendrobatidis on California islands. EcoHealth. 2016 Mar 1;13(1):145–50. doi: 10.1007/s10393-015-1071-y 26493624

24. Chaukulkar S, Sulaeman H, Zink AG, Vredenburg VT. Pathogen invasion and non-epizootic dynamics in Pacific newts in California over the last century. PloS one. 2018 Jul 2;13(7):e0197710. doi: 10.1371/journal.pone.0197710 29965970

25. Bradford DF. Mass mortality and extinction in a high-elevation population of Rana muscosa. Journal of Herpetology. 1991 Jun 1:174–7.

26. Drost CA, Fellers GM. Collapse of a regional frog fauna in the Yosemite area of the California Sierra Nevada, USA. Conservation biology. 1996 Apr 1;10(2):414–25.

27. Vredenburg VT, Koo MS, Wake DB. Declines of amphibians in California. Threatened Amphibians of the World. 2008:126.

28. Vredenburg VT. Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proceedings of the National Academy of Sciences. 2004 May 18;101(20):7646–50.

29. Sherman CK, Morton ML. Population declines of Yosemite toads in the eastern Sierra Nevada of California. Journal of Herpetology. 1993 Jun 1:186–98.

30. Green DE, Sherman CK. Diagnostic histological findings in Yosemite toads (Bufo canorus) from a die-off in the 1970s. Journal of Herpetology. 2001 Mar 1:92–103.

31. Vredenburg VT, Bingham R, Knapp R, Morgan JA, Moritz C, Wake D. Concordant molecular and phenotypic data delineate new taxonomy and conservation priorities for the endangered mountain yellow‐legged frog. Journal of Zoology. 2007 Apr;271(4):361–74.

32. Cheng TL, Rovito SM, Wake DB, Vredenburg VT. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences. 2011 Jun 7; 108(23):9502–7.

33. Butler H. 2017 "Sierra Nevada Retrospective Analysis" AmphibiaWeb: Amphibian Disease Portal. <https://n2t.net/ark:/21547/Ars2>.

34. Becker RA, Chambers JM, Wilks AR. The New S Language Pacific Grove CA: Wadsworth & Brooks/Cole. BeckerThe New S Language1988. 1988.

35. Venter O, Sanderson EW, Magrach A, Allan JR, Beher J, Jones KR, et al. Global terrestrial Human Footprint maps for 1993 and 2009. Scientific data. 2016 Aug 23; 3:sdata201667.

36. De Leon ME, Vredenburg VT, Piovia-Scott J. Recent emergence of a chytrid fungal pathogen in California Cascades frogs (Rana Cascadae). EcoHealth. 2017 Mar 1; 14(1):155–61. doi: 10.1007/s10393-016-1201-1 27957606

37. Phillips BL, Puschendorf R. Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America. Proceedings of the Royal Society of London B: Biological Sciences. 2013 Sep 7; 280(1766):20131290.

38. Talley BL, Muletz CR, Vredenburg VT, Fleischer RC, Lips KR. A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biological Conservation. 2015 Feb 28; 182:254–61.

39. Knapp RA, Fellers GM, Kleeman PM, Miller DA, Vredenburg VT, Rosenblum EB, et al. Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proceedings of the National Academy of Sciences. 2016 Oct 18;113(42):11889–94.

40. Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. Journal of evolutionary biology. 2009 Feb;22(2):245–59. doi: 10.1111/j.1420-9101.2008.01658.x 19196383

41. May RM, Anderson RM. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. Lond. B. 1983 Oct 22;219(1216):281–313. doi: 10.1098/rspb.1983.0075 6139816

42. Savage AE, Zamudio KR. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences. 2011 Sep 19:201106893.

43. Bataille A, Cashins SD, Grogan L, Skerratt LF, Hunter D, McFadden M, et al. Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proceedings of the Royal Society B: Biological Sciences. 2015 Apr 22;282(1805):20143127. doi: 10.1098/rspb.2014.3127 25808889

44. Piotrowski JS, Annis SL, Longcore JE. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia. 2004 Jan 1;96(1):9–15. 21148822

45. Becker CG, Greenspan SE, Tracy KE, Dash JA, Lambertini C, Jenkinson TS, et al. Variation in phenotype and virulence among enzootic and panzootic amphibian chytrid lineages. Fungal Ecology. 2017 Apr 30;26:45–50.

46. Rodriguez D, Becker CG, Pupin NC, Haddad CF, Zamudio KR. Long‐term endemism of two highly divergent lineages of the amphibian‐killing fungus in the Atlantic Forest of Brazil. Molecular Ecology. 2014 Feb;23(4):774–87. doi: 10.1111/mec.12615 24471406


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