Paleoparasitology

Paleoparasitology (or "palaeoparasitology") is the study of parasites from the past,[1] and their interactions with hosts and vectors; it is a subfield of Paleontology, the study of living organisms from the past. Some authors define this term more narrowly, as "Paleoparasitology is the study of parasites in archaeological material." (p. 103)[2] K.J. Reinhard suggests that the term "archaeoparasitology" be applied to "... all parasitological remains excavated from archaeological contexts ... derived from human activity" and that "the term 'paleoparasitology' be applied to studies of nonhuman, paleontological material." (p. 233)[3] This article follows Reinhard's suggestion and discusses the protozoan and animal parasites of non-human animals and plants from the past, while those from humans and our hominid ancestors are covered in archaeoparasitology.

Sources of material

Cysts found in a corpse in a late Roman grave in France, interpreted [4] as signs of probable hydatidosis and capillariasis

The primary sources of paleoparasitological material include mummified tissues,[4][5] coprolites (fossilised dung) from mammals[6] or dinosaurs,[7] fossils,[8] and amber inclusions.[9] Hair,[10] skins,[11] and feathers[12] also yield ectoparasite remains. Some archaeological artifacts document the presence of animal parasites. One example is the depiction of what appear to be mites in the ear of a "hyaena-like" animal in a tomb painting from ancient Thebes.[13]

Some parasites leave marks or traces (ichnofossils) on host remains, which persist in the fossil record in the absence of structural remains of the parasite. Parasitic ichnofossils include plant remains which exhibit characteristic signs of parasitic insect infestation, such as galls or leaf mines[14][15][16][17] and certain anomalies seen in invertebrate endoskeletal remains.[18][19][20][21][22][23]

Plant and animal parasites have been found in samples from a broad spectrum of geological periods, including the Holocene (samples over 10,000 years old),[24] Pleistocene (over 550,000 years old),[25] Eocene (over 44 million years old),[26] Cretaceous (over 100 million years)[27] and even Lower Cambrian (over 500 million years).[28]

Evidence of parasitism

One of the most daunting tasks involved in studying parasitic relationships from the past is supporting the assertion that the relationship between two organisms is indeed parasitic.[29] Organisms living in "close association" with each other may exhibit one of several different types of trophic relationships, such as parasitism, mutualism, and commensalism. Demonstration of true parasitism between existing species typically involves observing the harmful effects of parasites on a presumed host. Experimental infection of the presumed host, followed by recovery of viable parasites from that host also supports any claim of true parasitism. Obviously such experiments are not possible with specimens of extinct organisms found in paleontological contexts.

Assumptions of true parasitism in paleontological settings which are based on analogy to known present-day parasitic relationships may not be valid, due to host-specificity. For example, Trypanosoma brucei gambiense and Trypanosoma brucei rhodesiense are both devastating human parasites, but the related subspecies Trypanosoma brucei brucei will infect a number of animal hosts, but cannot even survive in the human blood stream, much less reproduce and infect a human host.[30] So a related (or unidentifiable) species of Trypanosoma found in a paleontological or archaeological context may not be a true human parasite, even though it appears identical (or very similar) to the modern parasitic forms.

The most convincing evidence of paleoparasitism is obtained when a presumed parasite is found in direct association with its presumed host, in a context that is consistent with known host-parasite associations. Some examples include helminths caught in amber in the process of escaping from the body of an insect,[31] lice found in the fur of guinea pig mummies,[32] protozoans in the alimentary canal of flies in amber,[33][34] nematode larvae found embedded in animal coprolites,[35][36] and a mite caught in amber in the process of apparently feeding on a spider.[37]

Fossil organisms which are related to present-day parasites often possess the morphological features associated with a parasitic lifestyle, such as blood-feeding mouthparts.[38] So fossil ticks[39][40] and hematophagous insects[41][42] are generally assumed to be ectoparasites, even when their remains are found in the absence of a host.

The presence of structures resembling leaf miner trails in leaf fossils provide indirect evidence of parasitism, even if remains of the parasite are not recovered.[43] The dramatic tissue aberrations seen in present-day plant galls and gall-like structures in some invertebrates are direct physiological reactions to the presence of either metazoan parasites or microbial pathogens. Similar structures seen in fossil plant[44] and invertebrate[45] remains are often interpreted as evidence of paleoparasitism.

Host-parasite interactions today are often exploited by other species, and similar examples have been found in the fossil record of plant galls and leaf mines. For example, there are species of wasps, called inquilines, which are unable to induce their own plant galls, so they simply take up residence in the galls that are made by other wasps.[17] Another example is the predation of plant galls or leaf mines, to eat the trapped insect larva inside the gall or mine.[46]

Knowledge gained from ancient animal and plant parasites

Studies of parasite remains and traces from the past have yielded a vast catalog of ancient host-parasite associations.[8][47][48][49] Genetic sequence data obtained directly from ancient animal parasites,[50] and inferences of past relationships based on genetic sequences of existing parasite groups are also being applied to paleoparasitological questions.[51][52] Data obtained by all of these methods are constantly improving our understanding of the origin and evolution of the parasites themselves[53] and their vectors,[54] and of the host-parasite and vector-parasite associations.[55][56][57][58][59]

In some cases, presumed host-parasite relationships of the past seem quite different from those known in the present, such as a fly which appears to be a parasite of a mite[60]

Paleoparasitological studies have also provided insight into questions outside the realm of parasitology. Examples include the migration and phylogeography of marine mammal hosts,[61] the identity of domestic animal bones based on the known hosts of parasite remains found at the site,[62] and the possible role of climatic changes on animal host genetic diversity.[63]

References

  1. ↑ Araújo, A., K. Reinhard and L. F. Ferreira (2015) Palaeoparasitology - Human Parasites in Ancient Material. Advances in Parasitology 90:349-387.
  2. ↑ Gonçalves, M.L.C., A. Araújo, and L.F. Ferreira (2003) Human intestinal parasites in the past: New findings and a review. Memórias do Instituto Oswaldo Cruz 98(Suppl 1):103-118.
  3. ↑ Reinhard, K.J. (1992) Parasitology as an interpretive tool in archaeology. American Antiquity 57(2):231-245.
  4. 1 2 Mowlavi, G.; Kacki, S.; Dupouy-Camet, J.; Mobedi, I.; Makki, M.; Harandi, MF.; Naddaf, SR. (2014). "Probable hepatic capillariosis and hydatidosis in an adolescent from the late Roman period buried in Amiens (France).". Parasite. 21: 9. doi:10.1051/parasite/2014010. PMC 3936287Freely accessible. PMID 24572211.
  5. ↑ Dittmar de la Cruz, K., R. Ribbeck, and A. Daugschies (2003) Paläoparasitologische Analyse von Meerschweinchenmumien der Chiribaya-Kultur (900-1100 AD). Berliner und Münchener Tierärztliche Wochenschrift 116(1-2):45-49.
  6. ↑ Schmidt, G.D., D.W. Duszynski, and P.S. Martin (1992) Parasites of the extinct Shasta ground sloth, Nothrotheriops shastensis, in Rampart Cave, Arizona. Journal of Parasitology 78(5):811-816.
  7. ↑ Poinar, G., Jr. and A.J. Boucot (2006) Evidence of intestinal parasites in dinosaurs. Parasitology 133(2):245-249.
  8. 1 2 Conway Morris, S. (1981) Parasites and the fossil record. Parasitology 82(3):489-509.
  9. ↑ Poinar, G.O., Jr. and R. Poinar (1999) The Amber Forest: A Reconstruction of a Vanished World. Princeton University Press, xviii, 239 pp.
  10. ↑ Penalver, E. and D. Grimaldi (2005) Assemblages of mammalian hair and blood-feeding midges (Insecta: Diptera: Psychodidae: Phlebotominae) in Miocene amber. Transactions of the Royal Society of Edinburgh: Earth Sciences 96:177-195.
  11. ↑ Mey E. (2005) Psittacobrosus bechsteini: A new extinct chewing louse (Insecta, Phthiraptera, Amblycera) off the Cuban macaw Ara tricolor (Psittaciiformes), with an annotated review of fossil and recently extinct animal lice. Anzeiger des Vereins Thueringer Ornithologen 5(2):201-217.
  12. ↑ Martill, D.M. and P.G. Davis (2001) A feather with possible ectoparasite eggs from the Crato Formation (Lower Cretaceous, Aptian) of Brazil. Neues Jahrbuch für Geologie und Palaeontologie Abhandlungen 219(3):241-259.
  13. ↑ Arthur, D.R. (1965) Ticks in Egypt in 1500 B.C.? Nature 206(4988):1060-1061.
  14. ↑ Scott, A.C., J. Stephenson, and M.E. Collinson (1994) The fossil record of leaves with galls. In: M.A.J. Williams (ed) Plant Gall - Organisms, Interactions, and Populations. Systematics Association Special Volume Series, Vol. 49. Clarendon Press: Oxford, pp. 447-470.
  15. ↑ Woodcock, D.W. and S. Maekawa (2006) Fossil leaf galls preserved in Honolulu volcanic series rocks. Bishop Museum Occasional Papers 88:20-22.
  16. ↑ Erwin, D.M. and K.N. Schick (2007) New Miocene oak galls (Cynipini) and their bearing on the history of cynipid wasps in western North America. Journal of Paleontology 81(3):568-580.
  17. 1 2 Stone, G.N., R.W.J.M. van der Ham, and J.G. Brewer (2008) Fossil oak galls preserve ancient multitrophic interactions. Proceedings of the Royal Society, Series B. Biological Sciences 275(1648):2213-2219.
  18. ↑ Ruiz, G.M. and D.R. Lindberg (1989) A fossil record for trematodes: Extent and potential uses. Lethaia 22:431-438.
  19. ↑ Radwanska, U. and A. Radwanski (2005) Myzostomid and copepod infestation of Jurassic echinoderms: A general approach, some new occurrences, and/or re-interpretation of previous reports. Acta Geologica Polonica 55(2):109-130.
  20. ↑ Huntley, J. W. and K. De Baets (2015) Trace Fossil Evidence of Trematode—Bivalve Parasite—Host Interactions in Deep Time. Advances in Parasitology 90:201-231. doi: 10.1016/bs.apar.2015.05.004
  21. ↑ Donovan, S. K. (2015) A Prejudiced Review of Ancient Parasites and Their Host Echinoderms: CSI Fossil Record or Just an Excuse for Speculation?. Advances in Parasitology 90:291-328.
  22. ↑ Klompmaker, A.A. and G. A. Boxshall G.A. (2015) Fossil Crustaceans as Parasites and Hosts.. Advances in Parasitology 90:233-289.
  23. ↑ Taylor, P. D. (2015) Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms. Advances in Parasitology 90:329-347.
  24. ↑ Larew, H.G. (1987) Two cynipid wasp acorn galls preserved in the La Brea Tar Pits (early Holocene). Proceedings of the Entomological Society of Washington 89(4):831-833.
  25. ↑ Jouy-Avantin, F., C. Combes, H. Lumley, J.-C. Miskovsky, and H. Moné (1999) Helminth eggs in animal coprolites from a Middle Pleistocene site in Europe. Journal of Parasitology 85(2):376-379
  26. ↑ Wappler, T., V.S. Smith, and R.C. Dalgleish (2004) Scratching an ancient itch: An Eocene bird louse fossil. Proceedings of the Royal Society of London, Series B. Biological Sciences 271(Suppl 5):s255-s258.
  27. ↑ Poinar, G., Jr. and S.R. Telford, Jr. (2005) Paleohaemoproteus burmacis gen.n., sp.n. (Haemosporidia: Plasmodidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae). Parasitology 131(1):79-84.
  28. ↑ Bassett, M.G., L.E. Popov and L.E. Holmer (2004) The oldest-known metazoan parasite? Journal of Paleontology 78(6):1214-1216.
  29. ↑ Littlewood, D.T.J. and S.K. Donovan (2003) Fossil parasites: A case of identity. Geology Today 19(4):136-142.
  30. ↑ Pays, E. and B. Vanhollebeke (2008) Mutual self-defence: The trypanolytic factor story. Microbes and Infection 10(9):985-989.
  31. ↑ Poinar, G., Jr. and R. Buckley (2006) Nematode (Nematoda: Mermithidae) and hairworm (Nematomorpha: Chordodidae) parasites in Early Cretaceous amber. Journal of Invertebrate Pathology 93(1):36-41.
  32. ↑ Dittmar, K. (2000) Evaluation of ectoparasites on the guinea pig mummies of El Yaral and Moquegua Valley, in southern Peru. Chungara — Revista de Antropología Chilena 32(1):123-125.
  33. ↑ Poinar, G., Jr. and S.R. Telford, Jr. (2005) Paleohaemoproteus burmacis gen.n., sp.n. (Haemospororidia: Plasmodiidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae). Parasitology 131(1):79-84.
  34. ↑ Poinar, G., Jr. (2008) Lutzomyia adiketis sp.n. (Diptera: Phlebotomidae), a vector of Paleoleishmania neotropicum sp.n. (Kinetoplastida: Trypanosomatidae) in Dominican amber. Parasites & Vectors 1:22 (8 pp.).
  35. ↑ Ferreira, L.F., A. Araújo, and A.N. Duarte (1993) Nematode larvae in fossilized animal coprolites from Lower and Middle Pleistocene sites, central Italy. Journal of Parasitology 79(3):440-442.
  36. ↑ Toker, N.Y., V. Onar, O Belli, S. Ak, H. Alpak, and E. Konyar (2005) Preliminary results of the analysis of coprolite material of a dog unearthed from the Van-Yoncatepe necropolis in eastern Anatolia. Turkish Journal of Veterinary and Animal Science 29(6):759-765.
  37. ↑ Wunderlich, J. (2004) Fossil spiders (Araneae) of the superfamily Dysderoidea in Baltic and Dominican amber, with revised family diagnoses. Beiträge zur Araneologie 3A:633-746
  38. ↑ Nagler, C. and J. T. Haug (2015) From Fossil Parasitoids to Vectors: Insects as Parasites and Hosts. Advances in Parasitology 90:137-200.
  39. ↑ De la Fuente, J. (2003) The fossil record and the origin of ticks (Acari: Parasitiformes: Ixodida). Experimental and Applied Acarology 29 (3-4): 331-344.
  40. ↑ Poinar, G., Jr. and R. Buckley (2008) Compluriscutula vetulum (Acari: Ixodida: Ixodidae), a new genus and species of hard tick from Lower Cretaceous Burmese amber. Proceedings of the Entomological Society of Washington 110 (2): 445-450.
  41. ↑ Lukashevich, E.D. and M.B. Mostovski (2003) Hematophagous insects in the fossil record. Paleontologicheskii Zhurnal 2003(2):48-56 (Russian) / Paleontological Journal 37(2):153-161 (English).
  42. ↑ Ponomarenko, A.G. (1976) A new insect from the Cretaceous of Transbaikalia, a possible parasite of pterosaurians. Paleontological Journal 10(3):339-343 (English) / Paleontologicheskii Zhurnal 1976(3):102-106 (Russian)
  43. ↑ Labandeira, C.C., D.L. Dilcher, D.R. Davis, and D.L. Wagner (1994) Ninety-seven million years of angiosperm-insect association: Paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Sciences of the United States of America 91(25):12278-12282.
  44. ↑ Srivastava, A.K. (2007) Fossil evidences of gall-inducing arthropod-plant interactions in the Indian subcontinent. Oriental Insects 41:213-222.
  45. ↑ Neumann, C. and M. Wisshak (2006) A foraminiferal parasite on the sea urchin Echinocorys: Ichnological evidence from the Late Cretaceous (Lower Maastrichtian, northern Germany). Ichnos 13(3):185-190.
  46. ↑ Krassilov, V. (2008) Mine and gall predation as top-down regulation in the plant-insect systems from the Cretaceous of Negev, Israel. Palaeogeography Palaeoclimatology Palaeoecology 261(3-4):261-269.
  47. ↑ Baumiller, T.K. and F.J. Gahn (2002) Fossil record of parasitism on marine invertebrates with special emphasis on the platyceratid-crinoid interaction. Paleontological Society Papers 8:195-209.
  48. ↑ De Baets, K. and Littlewood, D. T. J. (2015) The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors. Advances in Parasitology 90:1-51. doi: 10.1016/bs.apar.2015.07.001
  49. ↑ Leung, T. L. F. (2016) Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?. Biological Reviews doi: 10.1111/brv.12238
  50. ↑ Dittmar, K., U. Mamat, M. Whiting, T. Goldmann, K. Reinhard and S. Guillen (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 1):53-58
  51. ↑ Kerr, S.F. (2006) Molecular trees of trypanosomes incongruent with fossil records of hosts. Memórias do Instituto Oswaldo Cruz 101(1):25-30.
  52. ↑ Stevens, J.R. and J.F. Wallman (2006) The evolution of myiasis in humans and other animals in the Old and New Worlds. Part I. Phylogenetic analyses. Trends in Parasitology 22(3):129-136.
  53. ↑ Mu, J., J. Duan, K.D. Makova, D.A. Joy, C.Q. Huynh, O.H. Branch, W.-H. Li, and X.-Z. Su (2002) Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 418(6895):323-326.
  54. ↑ Black, W.C, IV (2003) Evolution of arthropod disease vectors. In: C.L. Greenblatt and M. Spigelman (eds) Emerging Pathogens: The Archaeology, Ecology, and Evolution of Infectious Disease. Oxford University Press, pp. 49-63.
  55. ↑ Opler, P.A. (1973) Fossil lepidopterous leaf mines demonstrate the age of some insect-plant relationships. Science 179(4080):1321-1323.
  56. ↑ Labandeira, C.C. (2006) Four phases of plant-arthropod associations in deep time. Geologica Acta 4(4):409-438.
  57. ↑ Nel, A. and D. Azar (2005) The oldest parasitic Scelionidae: Teleasinae (Hymenoptera: Platygastroidea). Polskie Pismo Entomologiczne 74(3):333-338.
  58. ↑ Sha, Z-L., C.-D. Zhu, R.W. Murphy, J. La Salle, and D.-W. Huang (2006) Mitochondrial phylogeography of a leafminer parasitoid, Diglyphus isaea (Hymenoptera: Eulophidae) in China. Biological Control 38(3):380-389.
  59. ↑ Poinar, G.O, Jr. (2007) The origins, acquisition and transmission of Leishmania in the distant past. Science and Culture 73:116-119.
  60. ↑ Kerr, P.H. and S.L. Winterton (2008) Do parasitic flies attack mites? Evidence in Baltic amber. Biological Journal of the Linnean Society 93(1):9-13.
  61. ↑ Bianucci, G., W. Landini and J. Buckeridge (2006) Whale barnacles and Neogene cetacean migration routes. New Zealand Journal of Geology and Geophysics 49(1):115-120.
  62. ↑ Schelvis, J. and C. Koot (1995) Sheep or goat? Damalinia deals with the dilemma. Proceedings of Experimental and Applied Entomology of the Netherlands Entomological Society 6:161-162
  63. ↑ Baker, B.W. (2007) Parasitism as a potential factor in reduced genetic variability in Late-Quaternary musk ox (Ovibos moschatus). Current Research in the Pleistocene 24:159-162.
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