Hostname: page-component-5d84bcc8dc-hb6bn Total loading time: 0 Render date: 2026-08-18T13:57:04.153Z Has data issue: false hasContentIssue false
  • English
  • Français

DNA barcoding of ancient parasites

Published online by Cambridge University Press:  20 March 2018

JAMIE R. WOOD
JAMIE R. WOOD*
Affiliation:
Manaaki Whenua Landcare Research, PO Box 69040, Lincoln, Canterbury 7640, New Zealand
*
Corresponding author: Manaaki Whenua Landcare Research, PO Box 69040, Lincoln, Canterbury 7640, New Zealand. E-mail: woodj@landcareresearch.co.nz
Get access Rights & Permissions [Opens in a new window]

Summary

Ancient samples present a number of technical challenges for DNA barcoding, including damaged DNA with low endogenous copy number and short fragment lengths. Nevertheless, techniques are available to overcome these issues, and DNA barcoding has now been used to successfully recover parasite DNA from a wide variety of ancient substrates, including coprolites, cesspit sediment, mummified tissues, burial sediments and permafrost soils. The study of parasite DNA from ancient samples can provide a number of unique scientific insights, for example: (1) into the parasite communities and health of prehistoric human populations; (2) the ability to reconstruct the natural parasite faunas of rare or extinct host species, which has implications for conservation management and de-extinction; and (3) the ability to view in ‘real-time’ processes that may operate over century- or millenial-timescales, such as how parasites responded to past climate change events or how they co-evolved alongside their hosts. The application of DNA metabarcoding and high-throughput sequencing to ancient specimens has so far been limited, but in future promises great potential for gaining empirical data on poorly understood processes such as parasite co-extinction.

Keywords

ancient DNAarchaeologyco-extinctionextinct speciesfossilsHolocenePleistocene

Information

Type
Special Issue Review
Information
Parasitology , Volume 145 , Special Issue 5: Advances and challenges in barcoding of microbes, parasites, and their vectors and reservoirs , April 2018 , pp. 646 - 655
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Alaeddini, R., Walsh, S. J. and Abbas, A. (2010). Forensic implications of genetic analyses from degraded DNA – a review. Forensic Science International: Genetics 4, 148–157.Google Scholar
Allentoft, M. E., Collins, M., Harker, D., Haile, J., Oskam, C. L., Hale, M. L., Campos, P. F., Samaniego, J. A., Gilbert, M. T., Willerslev, E., Zhang, G., Scofield, R. P., Holdaway, R. N. and Bunce, M. (2012). The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proceedings of the Royal Society B 279, 4724–4733.Google Scholar
Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W. and Huse, S. M. (2009). A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small subunit ribosomal RNA genes. PLoS ONE 4, e6372.CrossRefGoogle ScholarPubMed
Anastasiou, E. and Mitchell, P. D. (2013). Palaeopathology and genes: investigating the genetics of infectious diseases in excavated human skeletal remains and mummies from past populations. Gene 528, 33–40.CrossRefGoogle Scholar
Anderson-Carpenter, L. L., McLachlan, J. S., Jackson, S. T., Kuch, M., Lumibao, C. Y. and Poinar, H. N. (2011). Ancient DNA from lake sediments: bridging the gap between paleoecology and genetics. BMC Evolutionary Biology 11, 30.Google Scholar
Araújo, A. and Ferreira, L. F. (2000). Paleoparasitology and the antiquity of human host-parasite relationships. Memórias do Instituto Oswaldo Cruz 95(Suppl I), 89–93.Google Scholar
Araújo, A., Reinhard, K., Bastos, O. M., Costa, L. C., Pirmez, C., Iñiguez, A., Vicente, A. C., Morel, C. M. and Ferreira, L. F. (1998). Paleoparasitology: perspectives and new techniques. Revista do Instituto de Medicina Tropical de São Paulo 40, 371–376.Google Scholar
Araújo, A., Reinhard, K., Ferreira, L. F. and Gardner, S. L. (2008). Parasites as probes for prehistoric human migrations? Trends in Parasitology 24, 112–115.Google Scholar
Aufderheide, A. C., Salo, W., Madden, M., Streitz, J., Buikstra, J., Guhl, F., Arriaza, B., Renier, C., Wittmers, L. E. Jr., Fornaciari, G. and Allison, M. (2004). A 9,000-year record of Chagas’ disease. Proceedings of the National Academy of Sciences of the United States of America 101, 2034–2039.Google Scholar
Aufderheide, A. C., Salo, W., Madden, M., Streitz, J., Dittmar de la Cruz, K., Buikstra, J., Arriaza, B. and Wittmers, L. E. Jr. (2005). Aspects of ingestion transmission of Chagas disease identified in mummies and their coprolites. Chungara, Revista de Antropología Chilena 37, 85–90.Google Scholar
Bascompte, J. and Jordano, P. (2007). Plant-animal mutualistic networks: the architecture of biodiversity. Annual Reviews in Ecology, Evolution and Systematics 38, 567–593.Google Scholar
Boast, A. P., Weyrich, L. S., Wood, J. R., Metcalf, J. L., Knight, R. and Cooper, A. (2018). Coprolites reveal ecological interactions lost with the extinction of New Zealand birds. Proceedings of the National Academy of Sciences USA 115, 1546–1551.Google Scholar
Boessenkool, S., Austin, J. J., Worthy, T. H., Scofield, R. P., Cooper, A., Seddon, P. J. and Waters, J. M. (2009). Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proceedings of the Royal Society of London B 276, 815–821.Google Scholar
Bos, K. I., Schuenemann, V. J., Golding, G. B., Burbano, H. A., Waglechner, N., Coombes, B. K., McPhee, J. B., DeWitte, S. N., Meyer, M., Schmedes, S., Wood, J., Earn, D. J., Herring, D. A., Bauer, P., Poinar, H. N. and Krause, J. (2011). A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506–510.Google Scholar
Botella, H. G., Vargas, J. A. A., de la Rosa, M. A., Leles, D., Reimers, E. G., Vicente, A. C. P. and Iñiguez, A. M. (2010). Paleoparasitologic, paleogenetic and paleobotanic analysis of XVIII century coprolites from the church La Concepción in Santa Cruz de Tenerife, Canary Islands, Spain. Memórias do Instituto Oswaldo Cruz 105, 1054–1056.CrossRefGoogle Scholar
Brodie, J. F., Aslan, C. E., Rogers, H. S., Redford, K. H., Maron, J. L., Bronstein, J. L. and Groves, C. R. (2014). Secondary extinctions of biodiversity. Trends in Ecology & Evolution 29, 664–672.CrossRefGoogle ScholarPubMed
Brooks, T. M., Pimm, S. L. and Oyugi, J. O. (1999). Time lag between deforestation and bird extinction in tropical forest fragments. Conservation Biology 13, 1140–1150.Google Scholar
Brotherton, P., Endicott, P., Sanchez, J. J., Beaumont, M., Barnett, R., Austin, J. and Cooper, A. (2007). Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Research 35, 5717–5728.Google Scholar
Bush, A. O. and Kennedy, C. R. (1994). Host fragmentation and helminth parasites: hedging your bets against extinction. International Journal for Parasitology 24, 1333–1343.Google Scholar
Cizauskas, C. A., Carlson, C. J., Burgio, K. R., Clements, C. F., Dougherty, E. R., Harris, N. C. and Phillips, A. J. (2017). Parasite vulnerability to climate change: an evidence-based functional trait approach. Royal Society Open Science 4, 160535.Google Scholar
Cleeland, L. M., Reichard, M. V., Tito, R. Y., Reinhard, K. J. and Jewis, C. M. Jr. (2013) Clarifying prehistoric parasitism from a complementary morphological and molecular approach. Journal of Archaeological Science 40, 3060–3066.Google Scholar
Cole, T. L. and Wood, J. R. (In press). The ancient DNA revolution: the latest era in unearthing New Zealand's faunal history. New Zealand Journal of Zoology.Google Scholar
Colwell, R. K., Dunn, R. R. and Harris, N. C. (2012). Coextinction and persistence of dependent species in a changing world. Annual Review of Ecology, Evolution and Systematics 43, 183–203.Google Scholar
Cooper, A. and Poinar, H. N. (2000). Ancient DNA: do it right or not at all. Science 289, 1139.Google Scholar
Costa, M. A., Matheson, C., Lachetta, L., Llagostera, A. and Appenzeller, O. (2009). Ancient Leishmaniasis in a highland desert of northern Chile. PLoS ONE 4, e6983.Google Scholar
Côté, N. M., Daligault, J., Pruvost, M., Bennett, E. A., Gorgé, O., Guimaraes, S., Capelli, N., Le Bailly, M., Geigl, E. M. and Grange, T. (2016). A new high-throughput approach to genotype ancient human gastrointestinal parasites. PLoS ONE 11, e0146230.Google Scholar
Côté, N. M. L. and Le Bailly, M. (In press). Palaeoparasitology and palaeogenetics: review and perspectives for the study of ancient human parasites. Parasitology.Google Scholar
Darwin, C. (1862). The Various Contrivances by Which Orchids are Fertilised by Orchids. London, John Murray.Google Scholar
Der Sarkissian, C., Allentoft, M. E., Ávila-Arcos, M. C., Barnett, R., Campos, P. F., Cappellini, E., Ermini, L., Fernández, R., da Fonseca, R., Ginolhac, A., Hansen, A. J., Jónsson, H., Korneliussen, T., Margaryan, A., Martin, M. D., Moreno-Mayar, J. V., Raghavan, M., Rasmussen, M., Velasco, M. S., Schroeder, H., Schubert, M., Seguin-Orlando, A., Wales, N., Gilbert, M. T., Willerslev, E. and Orlando, L. (2015). Ancient genomics. Philosophical Transactions of the Royal Society B 370, 20130387.Google Scholar
Dittmar, K., Mamat, U., Whiting, M., Goldmann, T., Reinhard, K. and Guillen, S. (2003), Techniques of DNA-studies on prehispanic ectoparasites (Pulex sp., Pulicidae, Siphonaptera) from animal mummies of the Chiribaya culture, southern Peru. Memórias do Instituto Oswaldo Cruz 98(Suppl. I), 53–58.Google Scholar
Dunn, R. R. (2009). Coextinction: anecdotes, models, and speculation. In Holocene Extinctions (ed. Turvey, ST), pp. 167–180. Oxford University Press, Oxford, UK.Google Scholar
Dunn, R. R., Harris, N. C., Colwell, R. K., Koh, L. P. and Sodhi, N. S. (2009). The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Biological Society of London B 276, 3037–3045.Google Scholar
Fernandes, A., Iñiguez, A. M., Lima, V. S., Mendoça de Souza, S. M. F., Ferreira, L. F., Vicente, A. C. P. and Jansen, A. M. (2008). Pre-Columbian Chagas disease in Brazil: Trypanosoma cruzi I in the archaeological remains of a human in Peruaçu Valley, Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 103, 514–516.Google Scholar
Ferreira, L. F., Britto, C., Cardoso, M. A., Fernandes, O., Reinhard, K. and Araújo, A. (2000). Paleoparasitology of Chagas disease revealed by infected tissues from Chilean mummies. Acta Tropica 75, 79–84.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gilbert, M. T. P., Bandelt, H.-J., Hofreiter, M. and Barnes, I. (2005). Assessing ancient DNA studies. Trends in Ecology & Evolution 20, 541–544.Google Scholar
Gonçalves, M. L. C., Araújo, A. and Ferreira, L. F. (2003). Human intestinal parasites in the past: new findings and a review. Memórias do Instituto Oswaldo Cruz 98, 103–118.Google Scholar
Grealy, A. C., McDowell, M. C., Scofield, P., Murray, D. C., Fusco, D. A., Haile, J., Prideaux, G. J. and Bunce, M. (2015). A critical evaluation of how ancient DNA bulk bone metabarcoding complements traditional morphological analysis of fossil assemblages. Quaternary Science Reviews 128, 37–47.Google Scholar
Green, E. J. and Speller, C. F. (2017). Novel substrates as sources of ancient DNA: prospects and hurdles. Genes 8, 180.Google Scholar
Guhl, F., Jaramillo, C., Yockteng, R., Vallejo, G. A. and Arroyo, F. C. (1997). Trypanosoma cruzi DNA in human mummies. Lancet 349, 1370.CrossRefGoogle Scholar
Guhl, F., Jaramillo, C., Vallejo, G. A., Yockteng, R., Cárdenas-Arroyo, F., Fornaciari, G., Arriaza, B. and Aufderheide, A. C. (1999). Isolation of Trypanosoma cruzi DNA in 4000-year-old mummified human tissue from northern Chile. American Journal of Physical Anthropology 108, 401–407.Google Scholar
Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., et al. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398.Google Scholar
Hawass, Z., Gad, Y. Z., Ismail, S., Khairat, R., Fathalla, D., Hasan, N., Ahmed, A., Elleithy, H., Ball, M., Gaballah, F., Wasef, S., Fateen, M., Amer, H., Gostner, P., Selim, A., Zink, A. and Pusch, C. M. (2010). Ancestry and pathology in King Tuthankhamun's family. Journal of the American Medical Association 303, 638–647.CrossRefGoogle ScholarPubMed
Hebert, P. D., Cywinska, A., Ball, S. L. and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270, 313–321.Google Scholar
Hedges, R. E. M. and Sykes, B. C. (1992). Biomolecular archaeology: past, present and future. Proceedings of the British Academy 77, 267–283.Google Scholar
Higuchi, R., Bowman, B., Freiberger, M., Ryder, O. A. and Wilson, A. C. (1984). DNA sequences from the quagga, an extinct member of the horse family. Nature 312, 282–284.Google Scholar
Hofreiter, M., Serre, D., Poinar, H. N., Kuch, M. and Pääbo, S. (2001). Ancient DNA. Nature Reviews Genetics 2, 353–359.Google Scholar
Iñiguez, A. M., Reinhard, K. J., Araújo, A., Ferreira, L. F. and Vicente, A. C. P. (2003) Enterobius vermicularis: ancient DNA from North and South American human coprolites. Memórias do Instituto Oswaldo Cruz 98(Suppl. I), 67–69.Google Scholar
Iñiguez, A. M., Reinhard, K., Goncalves, M. L. C., Ferreira, L. F., Araújo, A. and Vicente, A. C. P. (2006). SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites. International Journal for Parasitology 36, 1419–1425.Google Scholar
Jaeger, L. H. and Iñiguez, A. M. (2014). Molecular paleoparasitological hybridization approach as effective tool for diagnosing human intestinal parasites from scarce archaeological remains. PLoS ONE 9, e105910.Google Scholar
Jaeger, L. H., Gijón-Botella, H., Del Carmen Del Arco-Aguilar, M., Martín-Oval, M., Rodríguez-Maffiotte, C., Del Arco-Aguilar, M., Araújo, A. and Iñiguez, A. M. (2016). Evidence of helminth infection in Guanche mummies: integrating paleoparasitological and paleogenetic investigations. Journal of Parasitology 102, 222–228.Google Scholar
Khairat, R., Ball, M., Chang, C.-C. H., Bianucci, R., Nerlich, A. G., Trautmann, M., Ismail, S., Shanab, G. M. L., Karim, A. M., Gad, Y. Z. and Pusch, C. M. (2013). First insights into the metagenome of Egyptian mummies using next-generation sequencing. Journal of Applied Genetics 54, 309–325.Google Scholar
Koh, L. P., Dunn, R. R., Sodhi, N. S., Colwell, R. K., Proctor, H. C. and Smith, V. S. (2004). Species coextinctions and the biodiversity crisis. Science 305, 1632–1634.Google Scholar
Krause, J. and Pääbo, S. (2016). Genetic time travel. Genetics 203, 9–12.Google Scholar
Lafferty, K. D. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society of London B: Biological Sciences 367, 2814–2827.Google Scholar
Lafferty, K. D. and Hopkins, S. R. (2018). Unique parasite aDNA in moa coprolites from New Zealand suggests mass parasite extinctions followed human-induced megafauna extinctions. PNAS 115, 1411–1413.Google Scholar
Lalremruata, A., Ball, M., Bianucci, R., Welte, B., Nerlich, A. G., Kun, J. F. J. and Pusch, C. M. (2013). Molecular identification of Falciparum malaria and human tuberculosis co-infections in mummies from the Fayum depression (lower Egypt). PLoS ONE 8, e60307.Google Scholar
Leles, D., Araújo, A., Ferreira, L. F., Vicente, A. C. P. and Iñiguez, A. M. (2008). Molecular paleoparasitological diagnosis of Ascaris sp. from coprolites: new scenery of ascariasis in pre-Colombian South America times. Memórias do Instituto Oswaldo Cruz 103, 106–108.Google Scholar
Leonardi, M., Librado, P., Der Sarkissian, C., Schubert, M., Alfarhan, A. H., Alquraishi, S. A., Al-Rasheid, K. A., Gamba, C., Willerslev, E. and Orlando, L. (2017). Evolutionary patterns and processes: lessons from ancient DNA. Systematic Biology 66, e1–e29.Google ScholarPubMed
Lindahl, T. (1993). Recovery of antediluvian DNA. Nature 365, 700.Google Scholar
Loreille, O., Roumat, E., Verneau, O., Bouchet, F. and Hänni, C. (2001). Ancient DNA from Ascaris: extraction amplification and sequences from eggs collected in coprolites. International Journal for Parasitology 31, 1101–1106.Google Scholar
Lydolph, M. C., Jacobsen, J., Arctander, P., Gilbert, M. T. P., Gilichinsky, D. A., Hansen, A. J., Willerslev, E. and Lange, L. (2005). Beringian paleoecology inferred from permafrost-preserved fungal DNA. Applied and Environmental Microbiology 71, 1012–1017.Google Scholar
Maizels, R. M. and McSorley, H. J. (2016). Regulation of the host immune system by helminth parasites. Journal of Allergy and Clinical Immunology 138, 666–675.Google Scholar
Marshall, W. F. III, Telford, S. R. III, Rys, P. N., Rutledge, B. J., Mathiesen, D., Malawista, S. E., Spielman, A. and Persing, D. H. (1994). Detection of Borrelia burgorferi DNA in museum specimens of Peromyscus leucopus. Journal of Infectious Diseases 170, 1027–1032.Google Scholar
Matheson, C. D., David, R., Spigelman, M. and Donoghue, H. D. (2014). Molecular confirmation of Schistosoma and familial relationship in two ancient Egyptian mummies. Yearbook of Mummy Studies 2, 39–47.Google Scholar
Moir, M. L., Vesk, P. A., Brennan, K. E., Keith, D. A., Hughes, L. and McCarthy, M. A. (2010). Current constraints and future directions in estimating coextinction. Conservation Biology 24, 682–290.Google Scholar
Myšková, E., Ditrich, O., Sak, B., Kváč, M. and Cymbalak, T. (2014). Detection of ancient DNA of Encephalitozoon intestinalis (Microsporidia) in archaeological material. Journal of Parasitology 100, 356–359.Google Scholar
Nerlich, A. G., Schraut, B., Dittrich, S., Jelinek, T. and Zink, A. R. (2008). Plasmodium falciparum in Ancient Egypt. Emerging Infectious Diseases 14, 1317–1319.Google Scholar
Oh, C. S., Seo, M., Chai, J. Y., Lee, S. J., Kim, M. J., Park, J. B. and Shin, D. H. (2010a). Amplification and sequencing of Trichuris trichiura ancient DNA extracted from archaeological sediments. Journal of Archaeological Science 37, 1269–1273.Google Scholar
Oh, C. S., Seo, M., Lim, N. J., Lee, S. J., Lee, E. J., Lee, S. D. and Shin, D. H. (2010b). Paleoparasitological report on Ascaris aDNA from an ancient East Asian sample. Memórias do Instituto Oswaldo Cruz 105, 225–228.Google Scholar
Orlando, L. and Cooper, A. (2014). Using ancient DNA to understand evolutionary and ecological processes. Annual Review of Ecology, Evolution, and Systematics 45, 573–598.Google Scholar
Orlando, L., Ginolhac, A., Zhang, G., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., Cappellini, E., Petersen, B., Moltke, I., Johnson, P. L., Fumagalli, M., Vilstrup, J. T., Raghavan, M., Korneliussen, T., Malaspinas, A. S., Vogt, J., Szklarczyk, D., Kelstrup, C. D., Vinther, J., Dolocan, A., Stenderup, J., Velazquez, A. M., Cahill, J., Rasmussen, M., Wang, X., Min, J., Zazula, G. D., Seguin-Orlando, A., Mortensen, C., et al. (2013). Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78.Google Scholar
Pääbo, S., Gifford, J. A. and Wilson, A. C. (1988). Mitochondrial DNA sequences from a 7000-year old brain. Nucleic Acids Research 16, 9775–9787.Google Scholar
Pääbo, S., Higuchi, R. G. and Wilson, A. C. (1989). Ancient DNA and the polymerase chain reaction. Journal of Biological Chemistry 254, 9709–9712.Google Scholar
Pääbo, S., Poinar, H., Serre, D., Jaenicke-Despres, V., Hebler, J., Rohland, N., Kuch, M., Krause, J., Vigilant, L. and Hofreiter, M. (2004). Genetic analyses from ancient DNA. Annual Review of Genetics 38, 645–679.CrossRefGoogle Scholar
Parducci, L., Bennett, K. D., Ficetola, G. F., Greve, I. A., Suyama, Y., Wood, J. R. and Pedersen, M. W. (2017). Ancient plant DNA from lake sediments. New Phytologist 214, 924–942.Google Scholar
Persing, D. H., Telford, S. R., Rys, P. N., Dodge, D. E., White, S. E. and Spielman, A. (1990). Detection of Borrelia burgdoferi DNA in museum specimens of Ixodes dammini ticks. Science 249, 1420–1423.Google Scholar
Pimm, S. L. and Raven, P. (2000). Biodiversity: extinction by numbers. Nature 403, 843–845.Google Scholar
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution Press, Washington DC, USA.Google Scholar
Powell, F. A. (2011). Can early loss of affiliates explain the coextinction paradox? An example from Acacia-inhabiting psyllids (Hemiptera: Psylloidea). Biodiversity and Conservation 20, 1533–1544.Google Scholar
Rawlence, N. J., Metcalf, J., Wood, J. R., Worthy, T. H., Austin, J. J. and Cooper, A. (2012). The effect of climate and environmental change on the megafaunal moa of New Zealand in the absence of humans. Quaternary Science Reviews 50, 141–153.Google Scholar
Rivera-Perez, J. I., Cano, R. J., Narganes-Storde, Y., Chanlatte-Baik, L. and Toranzos, G. A. (2015). Retroviral DNA sequences as a means for determining ancient diets. PLoS ONE 10, e0144951.CrossRefGoogle ScholarPubMed
Rizzi, E., Lari, M., Gigli, E., De Bellis, G. and Caramelli, D. (2012). Ancient DNA studies: new perspectives on old samples. Genetics Selection Evolution 44, 21.Google Scholar
Sallares, R. and Gomzi, S. (1999). Biomolecular archaeology of malaria. Ancient Biomolecules 3, 195–213.Google Scholar
Sawyer, S., Krause, J., Guschanski, K., Savolainen, V. and Pääbo, S. (2012). Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 7, e34131.Google Scholar
Selbach, C., Seddon, P. J. and Poulin, R. (2018) Parasites lost: neglecting a crucial element in de-extinction. Trends in Parasitology 34, 9–11.Google Scholar
Shapiro, B., Drummond, A. J., Rambaut, A., Wilson, M. C., Matheus, P. E., Sher, A. V., Pybus, O. G., Gilbert, M. T., Barnes, I., Binladen, J., Willerslev, E., Hansen, A. J., Baryshnikov, G. F., Burns, J. A., Davydov, S., Driver, J. C., Froese, D. G., Harington, C. R., Keddie, G., Kosintsev, P., Kunz, M. L., Martin, L. D., Stephenson, R. O., Storer, J., Tedford, R., Zimov, S. and Cooper, A. (2004). Rise and fall of the Beringian Steppe Bison. Science 306, 1561–1565.Google Scholar
Shin, D. H., Oh, C. S., Lee, S. J., Lee, E., Yim, S. G., Kim, M. J., Lee, S. D., Lee, Y. S., Lee, H. J. and Seo, M. (2012). Ectopic paragonimiasis from 400-year-old female mummy of Korea. Journal of Archaeological Science 39, 1103–1110.Google Scholar
Shin, D. H., Oh, C. S., Lee, H. J., Chai, J. Y., Lee, S. J., Hong, D.-W., Lee, S. D. and Seo, M. (2013). Ancient DNA analysis on Clonorchis sinensis eggs remained in samples from medieval Korean mummy. Journal of Archaeological Science 40, 211–216.Google Scholar
Skoglund, P., Northoff, B. H., Shunkov, M. V., Derevianko, A. P., Pääbo, S., Krause, J. and Jakobsson, M. (2014). Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proceedings of the National Academy of Sciences of the United States of America 111, 2229–2234.Google Scholar
Soubrier, J., Gower, G., Chen, K., Richards, S. M., Llamas, B., Mitchell, K. J., Ho, S. Y., Kosintsev, P., Lee, M. S., Baryshnikov, G., Bollongino, R., Bover, P., Burger, J., Chivall, D., Crégut-Bonnoure, E., Decker, J. E., Doronichev, V. B., Douka, K., Fordham, D. A., Fontana, F., Fritz, C., Glimmerveen, J., Golovanova, L. V., Groves, C., Guerreschi, A., Haak, W., Higham, T., Hofman-Kamińska, E., Immel, A., Julien, M. A., et al. (2016). Early cave art and ancient DNA record the origin of European bison. Nature Communications 7, 13158.Google Scholar
Spencer, H. G. and Zuk, M. (2016). For host's sake: the pluses of parasite preservation. Trends in Ecology & Evolution 31, 341–343.Google Scholar
Stork, N. E. and Lyal, C. H. C. (1993). Extinction or ‘co-extinction’ rates? Nature 366, 307.Google Scholar
Strona, G. and Fattorini, S. (2014). Parasitic worms: how many really? International Journal for Parasitology 44, 269–272.Google Scholar
Strona, G., Galli, P. and Fattorini, S. (2013). Fish parasites resolve the paradox of missing coextinctions. Nature Communications 4, 1718.Google Scholar
Sulaiman, I. M., Fayer, R., Bern, C., Gilman, R. H., Trout, J. M., Schantz, P. M., Das, P., Lal, A. A. and Xiao, L. (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerging Infectious Diseases 9, 1444–1452.Google Scholar
Thomsen, P. F., Elias, S., Gilbert, M. T., Haile, J., Munch, K., Kuzmina, S., Froese, D. G., Sher, A., Holdaway, R. N. and Willerslev, E. (2009). Non-destructive sampling of ancient insect DNA. PLoS ONE 4, e5048.Google Scholar
Vieira, M. C. and Almeida-Neto, M. (2015). A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecology Letters 18, 144–152.Google Scholar
Vieira, M. C., Cianciaruso, M. V. and Almeida-Neto, M. (2013). Plant-pollinator coextinctions and the loss of plant functional and phylogenetic diversity. PLoS ONE 8, e81242.Google Scholar
Weyrich, L. S., Duchene, S., Soubrier, J., Arriola, L., Llamas, B., Breen, J., Morris, A. G., Alt, K. W., Caramelli, D., Dresely, V., Farrell, M., Farrer, A. G., Francken, M., Gully, N., Haak, W., Hardy, K., Harvati, K., Held, P., Holmes, E. C., Kaidonis, J., Lalueza-Fox, C., de la Rasilla, M., Rosas, A., Semal, P., Soltysiak, A., Townsend, G., Usai, D., Wahl, J., Huson, D. H., Dobney, K. and Cooper, A. (2017). Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus. Nature 544, 357–361.Google Scholar
Willerslev, E., Cappellini, E., Boomsma, W., Nielsen, R., Hebsgaard, M. B., Brand, T. B., Hofreiter, M., Bunce, M., Poinar, H. N., Dahl-Jensen, D., Johnsen, S., Steffensen, J. P., Bennike, O., Schwenninger, J. L., Nathan, R., Armitage, S., de Hoog, C. J., Alfimov, V., Christl, M., Beer, J., Muscheler, R., Barker, J., Sharp, M., Penkman, K. E., Haile, J., Taberlet, P., Gilbert, M. T., Casoli, A., Campani, E. and Collins, M. J. (2007). Ancient biomolecules from deep ice cores reveal a forested southern Greenland. Science 317, 111–114.Google Scholar
Wood, J. R., Wilmshurst, J. M., Richardson, S. J., Rawlence, N. J., Wagstaff, S. J., Worthy, T. H. and Cooper, A. (2013a). Resolving lost herbivore community structure using coprolites of four sympatric moa species (Aves: Dinornithiformes). Proceedings of the National Academy of Sciences of the United States of America 110, 16910–16915.Google Scholar
Wood, J. R., Wilmshurst, J. M., Rawlence, N. J., Bonner, K. I., Worthy, T. H., Kinsella, J. M. and Cooper, A. (2013b). A megafauna's microfauna: gastrointestinal parasites of New Zealand's extinct moa (Aves: Dinornithiformes). PLoS ONE 8, e57315.Google Scholar
Wood, J. R., Perry, G. L. W. and Wilmshurst, J. M. (2017). Using palaeoecology to determine baseline ecological requirements and interaction networks for de-extinction candidate species. Functional Ecology 31, 1012–1020.Google Scholar
Xiao, L., Escalante, L., Yang, C., Sulaiman, I., Escalante, A. A., Montali, R. J., Fayer, R. and Lal, A. A. (1999). Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Applied and Environmental Microbiology 65, 1578–1583.Google Scholar
Yang, D. Y. and Watt, K. (2005). Contamination controls when preparing archaeological remains for ancient DNA analysis. Journal of Archaeological Science 32, 331–336.Google Scholar
Zink, A. R., Spigelman, M., Schraut, B., Greenblatt, C. L., Nerlich, A. G. and Donoghue, H. D. (2006). Leishmaniasis in ancient Egypt and upper Nubia. Emerging Infectious Diseases 12, 1616–1616.Google Scholar