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Tracing ancient evolutionary divergence in parasites

Published online by Cambridge University Press:  31 August 2016

RICHARD C. TINSLEY  and
MATTHEW C. TINSLEY
RICHARD C. TINSLEY*
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK
MATTHEW C. TINSLEY
Affiliation:
School of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK
*
*Corresponding author. School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol BS8 1TQ, UK. E-mail: r.c.tinsley@bristol.ac.uk
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Summary

For parasitic platyhelminths that generally lack a fossil record, there is little information on the pathways of morphological change during evolution. Polystomatid monogeneans are notable for their evolutionary diversification, having originated from ancestors on fish and radiated in parallel with tetrapod vertebrates over more than 425 million years (My). This study focuses on the genus Polystomoides that occurs almost worldwide on freshwater chelonian reptiles. Morphometric data show a major divergence in structural adaptations for attachment; this correlates with a dichotomy in micro-environmental conditions in habitats within the hosts. Species infecting the urinary tract have attachment organs with large hamuli and small suckers; species in the oro-nasal tract differ fundamentally, having small hamuli and large suckers. Zoogeographical and molecular evidence supports ancient separation of these site-specific clades: a new genus is proposed – Uropolystomoides – containing urinary tract species distinct from Polystomoides sensu stricto in oro-nasal sites. Aside from differences in attachment adaptations, body plans have probably changed little over perhaps 150 My. This case contrasts markedly with polystomatids in other vertebrate groups where major morphological changes have evolved over much shorter timescales; the chelonian parasites show highly stable morphology across their global distribution over a long period of evolution, exemplifying ‘living fossils’.

Keywords

MonogeneaPolystomatidaePolystomoidesUropolystomoidesliving fossilssite-specific attachment adaptations
Type
Research Article
Information
Parasitology , Volume 143 , Issue 14 , December 2016 , pp. 1902 - 1916
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Bychowsky, B. E. (1957). Monogenetic trematodes, their classification and phylogeny. Academy of Sciences, U.S.S.R. Moscow and Leningrad (in Russian). English Translation by Hargis, W.J. and Oustinoff, P.C. (1961). American Institute of Biological Sciences, Washington.Google Scholar
Chen, Q., Gorb, S. N., Gorb, E. and Pugno, N. (2013). Mechanics of plant fruit hooks. Journal of the Royal Society Interface 10, 20120913.CrossRefGoogle ScholarPubMed
Combes, C. (1976). [World biogeography of polystomatid monogeneans. In memoriam of B.E. Bykhovskiĭ.] (in Russian) Trudy Biologo – Pochvennogo Instituta (Issle dovaniya monogenehcheskikh sasal'shchikov) Novaya Senaya 34(137), 55–69.Google Scholar
Crawford, N. G., Parham, J. F., Sellas, A. B., Faircloth, B. C., Glenn, T. C., Papenfuss, T. J., Henderson, J. B., Hansen, M. H. and Simison, W. B. (2015). A phylogenomic analysis of turtles. Molecular Phylogenetics and Evolution 83, 250–257.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
De Baets, K., Dentzien-Dias, P., Upeniece, I., Verneau, O. and Donoghue, P. C. J. (2015). Constraining the deep origin of parasitic flatworms and host-interactions with fossil evidence. Advances in Parasitology 90, 93–135.CrossRefGoogle ScholarPubMed
Du Preez, L. H. and Van Rooyen, M. (2015). A new polystomatid (Monogenea, Polystomatidae) from the mouth of the North American freshwater turtle Pseudemys nelsoni . ZooKeys 539, 1–9.CrossRefGoogle Scholar
Euzet, L. and Combes, C. (1965). Polystomoides chabaudi n. sp (Monogenea) chez la tortue d'eau douce Pelomedusa subrufa Lacépede 1788. Annales de Parasitologie Humaine et Comparée 40, 455–450.CrossRefGoogle Scholar
Fairfax, R. A. (1990). A new species of Neopolystoma (Monogenea) and the occurrence of Polystomoides sp. in New Guinea, with notes on some polystomes from North-East Australia. Science in New Guinea 16, 109–114.Google Scholar
Fischthal, J. H. and Kuntz, R. E. (1964). A monogenetic and seven digenetic trematodes of amphibians and reptiles from Palawan Island, Philippines. Proceedings of the Helminthological Society of Washington 31, 230–240.Google Scholar
Fukui, T. and Ogata, T. (1936). Sur deux espèces nouvelles de trématode provenant de l‘Ocadia sinensis . Zoological Magazine, Tokyo 48, 765–770.Google Scholar
Fukui, T. and Ogata, T. (1939). On three species of trematodes from Ocadia sinensis (Gray). Volume Jubilare pro Prof. S. Yoshida 2, 187–202.Google Scholar
Gupta, N. K. and Randev, R. (1974). On the histomorphology of Polystomoides ludhianae n. sp. (Monogenea) recovered from the urinary bladder of Kachuga tectum and Kachuga smithi in North India. Parassitologia 16, 225–229.Google Scholar
Héritier, L., Badets, M., Du Preez, L. H., Aisien, M. S. O., Lixian, F., Combes, C. and Verneau, O. (2015). Evolutionary processes involved in the diversification of chelonian and mammal polystomatid parasites (Platyhelminthes, Monogenea, Polystomatidae) revealed by palaeoecology of their hosts. Molecular Phylogenetics and Evolution 92, 1–10.CrossRefGoogle ScholarPubMed
Hidalgo-Vila, J., Díaz-Paniagua, C., Ribas, A., Florencio, M., Pérez-Santigosa, N. and Casanova, J. C. (2009). Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: transmission from native turtles. Research in Veterinary Science 86, 463–465.CrossRefGoogle ScholarPubMed
Jackson, J. A., Tinsley, R. C. and Hinkel, H. (1998). Mutual exclusion of congeneric monogenean species in a space-limited habitat. Parasitology 117, 563–569.CrossRefGoogle Scholar
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogeneous interspecific interactions in a host–parasite system. International Journal for Parasitology 36, 1341–1349.CrossRefGoogle Scholar
Kearn, G. C. (1998). Parasitism and the Platyhelminths. Chapman and Hall, London, UK.Google Scholar
Kearn, G. C. (2004). Leeches, Lice and Lampreys. A natural history of skin and gill parasites of fishes. Springer, Dordrecht, Netherlands.Google Scholar
Knoepffler, L. -P. and Combes, C. (1977). Présence en Corse de Polystomoides ocellatum (Rudolphi, 1819) chez Emys orbicularis (L., 1758) (Chelonia, Emydidae). Considérations sur la répartition mondiale du genre Polystomoides . Vie Milieu 27, 221–230.Google Scholar
Lambert, A. and Kulo, S. D. (1982). Existence d'une dualité morphologique chez l'oncomiracidium de Polystomoides nabedei Kulo, 1980. Annales de Parasitologie Humaine et Comparée 57, 237–243.CrossRefGoogle ScholarPubMed
Lambert, A., Combes, C. and Ktari, M. H. (1978). Morphologie de l'oncomiracidium de Polystomoϊdes Ward, 1917 (Monogenea) et situation du genre parmi les Polystomatidae. Zeitschrift für Parasitenkunde 56, 175–181.CrossRefGoogle Scholar
Leidy, J. (1888). Entozoa of the terrapin. Proceedings of the Academy of Natural Sciences, Philadelphia 40, 127–128.Google Scholar
Lenis, C. and García-Prieto, L. (2009). Polystomoides magdalenensis n. sp. (Monogenoidea: Polystomatidae), a parasite of buccal cavity of Trachemys callirostris callirostris (Testudinata: Emydidae) from Colombia. Journal of Parasitology 95, 850–854.CrossRefGoogle Scholar
Leung, T. L. F. (2016). Fossils of parasites: what can the fossil record tell us about the evolution of parasitism? Biological Reviews (in press) [doi: 10.1111/brv.12238].Google Scholar
Littlewood, D. T. J., Rohde, K. and Clough, K. A. (1997). Parasite speciation within or between host species? – Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297.CrossRefGoogle ScholarPubMed
Mañé-Garzón, F. (1958). Sobre el hallazgo de Polystomoides coronatus (Leidy, 1888) en la boca de una tortuga de Sudamérica. Revista de Medicina Veterinaria y Parasitología, Maracay 18, 35–41.Google Scholar
Mañé-Garzón, F. and Gil, O. (1961). Trematodos de las tortugas del Uruguay, I. Una nueva especie del genero Polystomoides Ward 1917, de la cavidad bucal de Phrynops geoffroana hillarii (D. & B.). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 5, 1–4.Google Scholar
Mañé-Garzón, F. and Gil, O. (1962). Trematodos de las tortugas del Uruguay, V. Sobre un nuevo Polystomatidae de la faringe de Phrynops geoffroana hillarii (D. & B.). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 7, 1–6.Google Scholar
Mañé-Garzón, F. and Holcman-Spector, B. (1968). Trematodos de las tortugas del Uruguay, VII. Polystomoides rohdei n. sp. de la boca de Pseudemys dorbigni (Dum. & Bib.). Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 9, 1–3.Google Scholar
Meyer, L., Du Preez, L., Bonneau, E., Héritier, L., Quintana, M. F., Valdeón, A., Sadaoui, A., Kechemir-Issad, N., Palacios, C. and Verneau, O. (2015). Parasite host-switching from the invasive American red-eared slider, Trachemys scripta elegans, to the native Mediterranean pond turtle, Mauremys leprosa, in natural environments. Aquatic Invasions 10, 79–91.CrossRefGoogle Scholar
Morrison, C. and Du Preez, L. (2011). Turtle Polystomes of the World. Neopolystoma, Polystomoidella & Polystomoides. VDM Verlag Dr Muller, Saarbrücken, Germany.Google Scholar
Oi, M., Araki, J., Matsumoto, J. and Nogami, S. (2012). Helminth fauna of a turtle species introduced in Japan, the red-eared slider turtle (Trachemys scripta elegans). Research in Veterinary Science 93, 826–830.CrossRefGoogle ScholarPubMed
Olsen, P. D. and Littlewood, D. T. J. (2002). Phylogenetics of the Monogenea – evidence from a medley of molecules. International Journal for Parasitology 32, 233–244.CrossRefGoogle Scholar
Ozaki, Y. (1936). Two new trematodes from tortoise Geoemyda spengleri (Gmelin). Journal of Science of the Hiroshima University, Series B 4, 85–90.Google Scholar
Pandey, K. C. (1973). Studies on monogenetic trematodes of India, II. On a new species of the rare genus Polystomoides Ward, 1917. Indian Journal of Zootomy 14, 143–145.Google Scholar
Pandey, K. C. and Agarwal, N. (1978). A new monogenean, Polystomoides chauhani n.sp., from Hardella thurgi Gray. Indian Journal of Helminthology 30, 126–128.Google Scholar
Pichelin, S. (1995). The taxonomy and biology of the Polystomatidae (Monogenea) in Australian freshwater turtles (Chelidae, Pleurodira). Journal of Natural History 29, 1345–1381.CrossRefGoogle Scholar
Price, E. W. (1939). North American monogenetic trematodes. IV. The family Polystomatidae (Polystomatoidea). Proceedings of the Helminthological Society of Washington 6, 80–94.Google Scholar
Rao, S. L. (1975). On two monogenetic trematodes from the urinary bladder of Kachuga tectum tentora Gray (Family Polystomatidae Gamble, 1896). Rivista di Parassitologia 36, 261–266.Google Scholar
R Development Core Team (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rohde, K. (1963). Polystomoides malayi n. sp. (Monogenea, Polystomatidae) aus der harnblase von Cyclemys amboinensis in Malaya. Zeitschrift für Parasitenkunde 22, 278–282.CrossRefGoogle Scholar
Rohde, K. (1965). Studies on the genus Polystomoides Ward, 1917 (Monogenea). I. Description of 4 Malayan species, a key to the known species, and a comparison of the subcuticular layer in Polystomoides and some digenetic trematodes. Zoologische Jahrbücher Abteilung für Systematik, Ökologie und Geographie der Tiere 92, 345–368.Google Scholar
Rohde, K. (1984). Three new species of the genus Neopolystoma (Monogenea) from river tortoises in Australia. Systematic Parasitology 6, 99–105.CrossRefGoogle Scholar
Rohde, K. and Pearson, J. C. (1980). Two polystomes (Monogenea) from Australian river tortoises (Pleurodira, Chelidae), Polystomoides australiensis sp. nov. from Emydura krefftii, and Neopolystoma chelodinae (MacCallum, 1919) from Chelodina longicollis . Zoologischer Anzeiger 204, 191–208.Google Scholar
Sinnappah, N. D., Lim, L. H. S., Rohde, K., Tinsley, R., Combes, C. and Verneau, O. (2001). A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution 18, 189–201.CrossRefGoogle ScholarPubMed
Sproston, N. G. (1946). A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London 25, 185–600.CrossRefGoogle Scholar
Stewart, F. H. (1914). Studies in Indian Helminthology 11. The anatomy of Polystomum kachugae, sp. nov., with notes on the genus Polystomum . Records of the Indian Museum 10, 195–205.Google Scholar
Strankowski, M. (1937). Recherches anatomiques sur Polystoma ocellatum Rud. Zoologica Poloniae 2, 1–20.Google Scholar
Stunkard, H. (1917). Studies on North American Polystomidae, Aspidogastridae, and Paramphistomidae. Illinois Biological Monographs 3, 285–385.Google Scholar
Thatcher, V. E. (1963). Trematodes of turtles from Tabasco, Mexico with a description of a new species of Dadaytrema (Trematoda: Paramphistomidae). American Midland Naturalist 70, 347–355.CrossRefGoogle Scholar
Timmers, S. F. and Lewis, P. D. (1979). Helminths of Chrysemys picta belli in Manitoba including Polystomoides pauli sp. n. (Monogenea: Polystomatidae). Canadian Journal of Zoology 57, 1046–1051.CrossRefGoogle Scholar
Tinsley, R. C. (1981). The evidence from parasite relationships for the evolutionary status of Xenopus (Anura Pipidae). Monitore zoologico italiano N.S. Supplemento 15, 367–385.CrossRefGoogle Scholar
Tinsley, R. C. (1983). Ovoviviparity in platyhelminth life cycles. Parasitology 86, 161–196.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1990). Host behaviour and opportunism in parasite life cycles. In Parasitism and Host Behaviour (ed. Barnard, C. J. and Behnke, J.), pp. 158–192. Taylor and Francis, London, UK.Google Scholar
Tinsley, R. C. (1993). The population biology of polystomatid monogeneans. Bulletin Français de la Pêche et de la Pisciculture 328, 120–136.CrossRefGoogle Scholar
Tinsley, R. C. (1999). Parasite adaptations to extreme conditions in a desert environment. Parasitology 119, S31–S56.CrossRefGoogle Scholar
Tinsley, R. C. (2003). Polystomatid monogeneans and anuran amphibians: an evolutionary arms race leading to parasite extinctions? In Taxonomie, écologie et évolution des métazoaires parasites (ed. Combes, C. and Jourdane, J.), pp. 259–285. Presses Universitaires de Perpignan, Perpignan, France.Google Scholar
Tinsley, R. C. (2004). Platyhelminth parasite reproduction: some general principles derived from monogeneans. Canadian Journal of Zoology 82, 270–291.CrossRefGoogle Scholar
Tinsley, R. C. (2005). Parasitism and hostile environments. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J. -F.), pp. 85–112. Oxford University Press, Oxford.CrossRefGoogle Scholar
Tinsley, R. C. (2013). The oncomiracidium of Oculotrema hippopotami Stunkard, 1924 and relationships within the Polystomatidae (Monogenea). Systematic Parasitology 84, 123–135.CrossRefGoogle ScholarPubMed
Tinsley, R. C., York, J. E., Stott, L. C., Everard, A. L. E., Chapple, S. J., Tinsley, M. C. (2011). Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on development within the host. Parasitology 138, 1039–1052.CrossRefGoogle Scholar
Verneau, O., Bentz, S., Sinnappah, N. D., Du Preez, L., Whittington, I. and Combes, C. (2002). A view of early vertebrate evolution inferred from the phylogeny of polystome parasites (Monogenea: Polystomatidae). Proceedings of the Royal Society, London B 269, 535–543.CrossRefGoogle ScholarPubMed
Verneau, O., Palacios, C., Platt, T., Alday, M., Billard, E., Allienne, J.- F., Basso, C. and Du Preez, L. H. (2011). Invasive parasite threat: parasite phylogenetics reveals patterns and processes of host-switching between non-native and native captive freshwater turtles. Parasitology 138, 1778–1792.CrossRefGoogle ScholarPubMed
Vieira, F. M., Novelli, I. A., Sousa, B. M. and de SouzaLima, S. (2008). A new species of Polystomoides Ward, 1917 (Monogenea: Polystomatidae) from freshwater chelonians (Testudines: Chelidae) in Brazil. Journal of Parasitology 94, 626–630.CrossRefGoogle ScholarPubMed
Ward, H. B. (1917). On the structure and classification of North American parasitic worms. Journal of Parasitology 4, 1–13.CrossRefGoogle Scholar