Infectious disease, especially virulent infectious disease, is commonly regarded as a cause of fluctuation or decline in biological populations. However, it is not generally considered as a primary factor in causing the actual endangerment or extinction of species. We review here the known historical examples in which disease has, or has been assumed to have had, a major deleterious impact on animal species, including extinction, and highlight some recent cases in which disease is the chief suspect in causing the outright endangerment of particular species. We conclude that the role of disease in historical extinctions at the population or species level may have been underestimated. Recent methodological breakthroughs may lead to a better understanding of the past and present roles of infectious disease in influencing population fitness and other parameters. 1. Background Although lethal epi- or panzootics are obvious risk factors that can lead to population fluctuation or decline in particular circumstances, infectious diseases are seldom considered as potential drivers of extirpation or extinction—that is, of the complete loss of all populations or subunits comprising a given biological species. For example, in conservation biology, infectious disease is usually regarded as having only a marginal or contributory influence on extinction, except perhaps in unusual circumstances (e.g., [1–4]). In their examination of 223 instances of critically endangered species listed by the IUCN (International Union for Conservation of Nature) as allegedly threatened by infectious disease, Smith et al. [4] found that in the overwhelming majority of cases there was no conclusive evidence to support infectious disease as a contributing threat. Although this record should improve with increasing awareness of the effects of infectious diseases on wildlife, as this paper illustrates progress has so far been slow. Both of the authors of this paper are primarily concerned with mammals, which is the group that will receive the bulk of attention here. However, at the pragmatic, data-gathering level, the issues concerned with properly accounting for and evaluating the effects of infectious diseases on natural populations differ little from one phylogenetic grouping to another. First, narrowing down extinction events or even catastrophic population declines to single causes is almost always problematic. In most real cases, extinction is multicausational, even if one cause can be identified as being predominantly responsible [5]. Habitat fragmentation and climate change are
References
[1]
F. de Castro and B. Bolker, “Mechanisms of disease-induced extinction,” Ecology Letters, vol. 8, no. 1, pp. 117–126, 2005.
[2]
S. K. Lyons, F. A. Smith, P. J. Wagner, E. P. White, and J. H. Brown, “Was a ‘hyperdisease’ responsible for the late Pleistocene megafaunal extinction?” Ecology Letters, vol. 7, no. 9, pp. 859–868, 2004.
[3]
A. B. Pedersen, K. E. Jones, C. L. Nunn, and S. Altizer, “Infectious diseases and extinction risk in wild mammals,” Conservation Biology, vol. 21, no. 5, pp. 1269–1279, 2007.
[4]
K. F. Smith, D. F. Sax, and K. D. Lafferty, “Evidence for the role of infectious disease in species extinction and endangerment,” Conservation Biology, vol. 20, no. 5, pp. 1349–1357, 2006.
[5]
“IUCN Redlist of Threatened Species,” 2012, http://www.iucnredlist.org/.
[6]
N. S. B. Sodhi, N. S. B. B. W, and C. A. J. Bradshaw, Causes and Consequences of Species Extinctions, Princeton University Press, Princeton, NJ, USA, 2009.
[7]
A. M. Q. King, E. Lefkowitz, M. J. Adams, and E. B. Carstens, Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, Academic Press/Elsevier, New York, NY, USA, 2012.
[8]
J. F. Drexler, V. M. Corman, M. A. Müller et al., “Bats host major mammalian paramyxoviruses,” Nature Communications, vol. 3, p. 796, 2012.
[9]
Z. Wu, X. Ren, L. Yang et al., “Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces,” Journal of Virology, vol. 86, no. 20, pp. 10999–11012, 2012.
[10]
K. B. Wyatt, P. F. Campos, M. T. P. Gilbert et al., “Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease,” PLoS ONE, vol. 3, no. 11, Article ID e3602, 2008.
[11]
J. K. Taubenberger, D. Baltimore, P. C. Doherty et al., “Reconstruction of the 1918 influenza virus: unexpected rewards from the past,” MBio, vol. 3, no. 5, Article ID e00201-12.
[12]
I. Barnes and M. G. Thomas, “Evaluating bacterial pathogen DNA preservation in museum osteological collections,” Proceedings of the Royal Society B, vol. 273, no. 1587, pp. 645–653, 2006.
[13]
E. Willerslev and A. Cooper, “Ancient DNA,” Proceedings of the Royal Society B, vol. 272, no. 1558, pp. 3–16, 2005.
[14]
M. C. ávila-Arcos, S. Y. Ho, Y. Ishida et al., “One hundred twenty years of koala retrovirus 6 evolution determined from museum skins,” Molecular Biology and Evolution. In press.
[15]
S. Calvignac, J. M. Terme, S. M. Hensley, P. Jalinot, A. D. Greenwood, and C. H？nni, “Ancient DNA identification of early 20th century simian T-cell leukemia virus type 1,” Molecular Biology and Evolution, vol. 25, no. 6, pp. 1093–1098, 2008.
[16]
V. J. Schuenemann, K. Bos, S. DeWitte et al., “Targeted enrichment of ancient pathogens yielding the pPCP1 plasmid of Yersinia pestis from victims of the Black Death,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 38, pp. E746–E752, 2011.
[17]
J. K. Taubenberger, A. H. Reid, A. E. Krafft, K. E. Bijwaard, and T. G. Fanning, “Initial genetic characterization of the 1918 'Spanish' influenza virus,” Science, vol. 275, no. 5307, pp. 1793–1796, 1997.
[18]
M. Worobey, M. Gemmel, D. E. Teuwen et al., “Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960,” Nature, vol. 455, no. 7213, pp. 661–664, 2008.
[19]
R. D. E. MacPhee and P. A. Marx, The 40,000-Year Plague: Humans, Hyperdisease, and First-Contact Extinctions, Smithsonian Institution Press, Washington, DC, USA, 1997.
[20]
A. C. Breed, R. K. Plowright, D. T. S. Hayman et al., Disease Management in Endangered Mammals, Springer, Tokyo, Japan, 2009.
[21]
P. Daszak, A. A. Cunningham, and A. D. Hyatt, “Emerging infectious diseases of wildlife—threats to biodiversity and human health,” Science, vol. 287, no. 5452, pp. 443–449, 2000.
[22]
O. R. Bininda-Emonds, R. Beck, and R. D. E. MacPhee, Rocking Clocks and Clocking Rocks: A Critical Look at Divergence Time Estimation in Mammals, Cambridge University Press, 2012.
[23]
IUCN Red List, http://www.iucnredlist.org/.
[24]
S. Turvey, Holocene Extinctions, Oxford University Press, 2009.
[25]
R. R. Dunn, N. C. Harris, R. K. Colwell, L. P. Koh, and N. S. Sodhi, “The sixth mass coextinction: are most endangered species parasites and mutualists?” Proceedings of the Royal Society B, vol. 276, no. 1670, pp. 3037–3045, 2009.
[26]
N. W. Lerche, P. A. Marx, K. G. Osborn et al., “Natural history of endemic type D retrovirus infection and acquired immune deficiency syndrome in group-housed rhesus monkeys,” Journal of the National Cancer Institute, vol. 79, no. 4, pp. 847–854, 1987.
[27]
M. Guiserix, N. Bahi-Jaber, D. Fouchet, F. Sauvage, and D. Pontier, “The canine distemper epidemic in Serengeti: are lions victims of a new highly virulent canine distemper virus strain, or is pathogen circulation stochasticity to blame?” Journal of the Royal Society Interface, vol. 4, no. 17, pp. 1127–1134, 2007.
[28]
H. M. Weingartl, C. Embury-Hyatt, C. Nfon, A. Leung, G. Smith, and G. Kobinger, “Transmission of Ebola virus from pigs to non-human primates,” Scientific Reports, vol. 2, p. 811, 2012.
[29]
G. R. Scott, Wiildlife Rinderpest, Plenum Press, New York, NY, USA, 1976.
[30]
L. A. Freed, R. L. Cann, M. L. Goff, W. A. Kuntz, and G. R. Bodner, “Increase in avian malaria at upper elevation in Hawai‘i,” Condor, vol. 107, no. 4, pp. 753–764, 2005.
[31]
A. A. Cunningham and P. Daszak, “Extinction of a species of land snail due to infection with a microsporidian parasite,” Conservation Biology, vol. 12, no. 5, pp. 1139–1141, 1998.
[32]
“Synopsis of infectious diseases and parasites of commercially exploited shellfish: steinhausia mytilovum (mussel egg disease),” http://www.pac.dfo-mpo.gc.ca/science/species-especes/shellfish-coquillages/diseases-maladies/pages/medmu-eng.htm.
[33]
J. Murray, E. Murray, M. S. Johnson, and B. Clarke, “The extinction of Partula on Moorea,” Pacific Science, vol. 42, no. 3-4, pp. 150–153, 1988.
[34]
R. J. Orth, T. J. B. Carruthers, W. C. Dennison et al., “A global crisis for seagrass ecosystems,” BioScience, vol. 56, no. 12, pp. 987–996, 2006.
[35]
J. T. Carlton, G. J. Vermeij, D. R. Lindberg, D. A. Carlton, and E. C. Dudley, “The first historical extinction of a marine invertebrate in an ocean basin: the demise of the eelgrass limpet Lottia alveus,” Biological Bulletin, vol. 180, no. 1, pp. 72–80, 1991.
[36]
P. Daszak, L. Berger, A. A. Cunningham, A. D. Hyatt, D. Earl Green, and R. Speare, “Emerging infectious diseases and amphibian population declines,” Emerging Infectious Diseases, vol. 5, no. 6, pp. 735–748, 1999.
[37]
L. F. Skerratt, L. Berger, R. Speare et al., “Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs,” EcoHealth, vol. 4, no. 2, pp. 125–134, 2007.
[38]
L. M. Schloegel, A. M. Picco, A. M. Kilpatrick, A. J. Davies, A. D. Hyatt, and P. Daszak, “Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana),” Biological Conservation, vol. 142, no. 7, pp. 1420–1426, 2009.
[39]
L. M. Schloegel, J. M. Hero, L. Berger, R. Speare, K. McDonald, and P. Daszak, “The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case extinction by infection in a free-ranging wildlife species?” EcoHealth, vol. 3, no. 1, pp. 35–40, 2006.
[40]
R. E. Warner, “The role of introduced diseases in the extinction of the endemic Hawaiian avifauna,” The Condor, vol. 70, no. 2, pp. 101–120, 1968.
[41]
E. VanderWerf, “Distribution and potential impacts of avian pox-like lesions in 'Elepaio at Hakalau Forest National Wildlife Refuge,” Studies in Avian Biology, vol. 22, pp. 247–253, 2001.
[42]
C. van Riper and J. M. Scott, “Limiting factors affecting Hawaiian native birds,” Studies in Avian Biology, vol. 22, pp. 221–233, 2001.
[43]
M. E. Roelke-Parker, L. Munson, C. Packer et al., “A canine distemper virus epidemic in Serengeti lions (Panthera leo),” Nature, vol. 379, no. 6564, pp. 441–445, 1996.
[44]
E. S. Williams, E. T. Thorne, M. J. Appel, and D. W. Belitsky, “Canine distemper in black-footed ferrets (Mustela nigripes) from Wyoming,” Journal of Wildlife Diseases, vol. 24, no. 3, pp. 385–398, 1988.
[45]
E. M. Leroy, P. Telfer, B. Kumulungui et al., “A serological survey of ebola virus infection in central African nonhuman primates,” Journal of Infectious Diseases, vol. 190, no. 11, pp. 1895–1899, 2004.
[46]
A. M. Pearse and K. Swift, “Allograft theory: transmission of devil facial-tumour disease,” Nature, vol. 439, no. 7076, p. 549, 2006.
[47]
C. W. Andrews, A Monograph of Christmas Island (Indian Ocean), British Museum (Natural History), London, UK, 1900.
[48]
H. E. Durham, “Notes on Nagana and on some Haematozoa observed during my travels,” Parasitology, vol. 1, pp. 227–235, 1908.
[49]
R. D. E. MacPhee, Insulae Infortunatae: Establishing the Chronology of Late Quaternary Mammal Extinctions in the West Indies, Springer, Dordrecht, The Netherlands, 2008.
[50]
“National Recovery Plan for the Christmas Island Shrew Crocidura attenuata trichura,” Canberra, Australia, http://www.environment.gov.au/biodiversity/threatened/publications/recovery/c-attenuata-trichura/index.html.
[51]
T. G. Martin, S. Nally, A. A. Burbidge et al., “Acting fast helps avoid extinction,” Conservation Letters, vol. 5, no. 4, pp. 274–280, 2012.
[52]
J. Pickering and C. Norris, “New evidence on the extinction of the endemic murid Rattus macleari from Christmas Island, Indian Ocean,” Australian Mammalogy, vol. 19, pp. 35–41, 1996.
[53]
R. D. E. MacPhee and C. Flemming, Requiem Aeternum: The Last Five Hundred Years of Mammalian Species Extinctions, Kluwer Academic/Plenum Publishers, New York, NY, USA, 1999.
[54]
J. J. Hanger, L. D. Bromham, J. J. Mckee, T. M. O'Brien, and W. F. Robinson, “The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus,” Journal of Virology, vol. 74, no. 9, pp. 4264–4272, 2000.
[55]
R. E. Tarlinton, J. Meers, and P. R. Young, “Retroviral invasion of the koala genome,” Nature, vol. 442, no. 7098, pp. 79–81, 2006.
[56]
M. Jackson, N. White, P. Giffard, and P. Timms, “Epizootiology of Chlamydia infections in two free-range koala populations,” Veterinary Microbiology, vol. 65, no. 4, pp. 255–264, 1999.
[57]
R. Tarlinton, J. Meers, J. Hanger, and P. Young, “Real-time reverse transcriptase PCR for the endogenous koala retrovirus reveals an association between plasma viral load and neoplastic disease in koalas,” Journal of General Virology, vol. 86, no. 3, pp. 783–787, 2005.
[58]
K. Tsangaras, M. C. ávila-Arcos, Y. Ishida, K. M. Helgen, A. L. Roca, and A. D. Greenwood, “Historically low mitochondrial DNA diversity in koalas (Phascolarctos cinereus),” BMC Genetics, vol. 13, 92 pages, 2012.
[59]
Foundation WW.
[60]
L. Warnecke, J. M. Turner, T. K. Bollinger et al., “Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 18, pp. 6999–7003, 2012.
[61]
S. J. Puechmaille, W. F. Frick, T. H. Kunz et al., “White-nose syndrome: is this emerging disease a threat to European bats?” Trends in Ecology and Evolution, vol. 26, no. 11, pp. 570–576, 2011.
[62]
S. J. Puechmaille, G. Wibbelt, V. Korn et al., “Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality,” PLoS ONE, vol. 6, no. 4, Article ID e19167, 2011.
[63]
G. Wibbelt, A. Kurth, D. Hellmann et al., “White-nose syndrome fungus (Geomyces destructans) in bats, Europe,” Emerging Infectious Diseases, vol. 16, no. 8, pp. 1237–1243, 2010.
[64]
W. F. Frick, J. F. Pollock, A. C. Hicks et al., “An emerging disease causes regional population collapse of a common North American bat species,” Science, vol. 329, no. 5992, pp. 679–682, 2010.
[65]
E. P. Murchison, O. B. Schulz-Trieglaff, Z. Ning et al., “Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer,” Cell, vol. 148, no. 4, pp. 780–791, 2012.
[66]
C. E. Hawkins, C. Baars, H. Hesterman et al., “Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii,” Biological Conservation, vol. 131, no. 2, pp. 307–324, 2006.
[67]
H. McCallum, M. Jones, C. Hawkins et al., “Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction,” Ecology, vol. 90, no. 12, pp. 3379–3392, 2009.
[68]
I. Cho and M. J. Blaser, “The human microbiome: at the interface of health and disease,” Nature Reviews Genetics, vol. 13, no. 4, pp. 260–270, 2012.
[69]
J. F. Drexler, A. Seelen, V. M. Corman et al., “Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae,” Journal of Virology, vol. 86, no. 17, pp. 9134–9147, 2012.
[70]
C. Kohl, R. Lesnik, A. Brinkmann et al., “Isolation and characterization of three mammalian orthoreoviruses from European bats,” PLoS ONE, vol. 7, no. 8, Article ID e43106, 2012.
[71]
C. Kohl, M. Z. Vidovszky, K. Muhldorfer et al., “Genome analysis of bat adenovirus 2: indications of interspecies transmission,” Journal of Virology, vol. 86, no. 3, pp. 1888–1892, 2012.
[72]
A. Kurth, C. Kohl, A. Brinkmann et al., “Novel paramyxoviruses in free-ranging European bats,” PLoS ONE, vol. 7, no. 6, Article ID e38688, 2012.
[73]
M. Rasmussen, X. Guo, Y. Wang et al., “An Aboriginal Australian genome reveals separate human dispersals into Asia,” Science, vol. 333, no. 6052, pp. 94–98, 2011.
[74]
T. Maricic, M. Whitten, and S. P？？bo, “Multiplexed DNA sequence capture of mitochondrial genomes using PCR products,” PLoS ONE, vol. 5, no. 11, Article ID e14004, 2010.
[75]
H. A. Burbano, E. Hodges, R. E. Green et al., “Targeted investigation of the neandertal genome by array-based sequence capture,” Science, vol. 328, no. 5979, pp. 723–725, 2010.
[76]
M. C. ávila-Arcos, E. Cappellini, J. A. Romero-Navarro et al., “Application and comparison of large-scale solution-based DNA capture-enrichment methods on ancient DNA,” Scientific Reports, vol. 1, p. 74, 2011.
[77]
E. Cappellini, L. J. Jensen, D. Szklarczyk et al., “Proteomic analysis of a pleistocene mammoth femur reveals more than one hundred ancient bone proteins,” Journal of Proteome Research, vol. 11, no. 2, pp. 917–926, 2012.
