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Life cycles, molecular phylogeny and historical biogeography of the ‘pygmaeus’ microphallids (Digenea: Microphallidae): widespread parasites of marine and coastal birds in the Holarctic

Published online by Cambridge University Press:  01 May 2012

KIRILL V. GALAKTIONOV ,
ISABEL BLASCO-COSTA  and
PETER D. OLSON
KIRILL V. GALAKTIONOV*
Affiliation:
Zoological Institute of the Russian Academy of Sciences, St Petersburg, Russia Department of Invertebrate Zoology, St Petersburg State University, St Petersburg, Russia
ISABEL BLASCO-COSTA
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
PETER D. OLSON
Affiliation:
Department of Zoology, The Natural History Museum, London SW7 5BD, UK
*
*Corresponding author: Zoological Institute of the Russian Academy of Sciences, St Petersburg, Russia. Fax: +78123282941. E-mail address: kirill.galaktionov@gmail.com
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Summary

The ‘pygmaeus’ microphallids (MPG) are a closely related group of 6 digenean (Platyhelminthes: Trematoda) Microphallus species that share a derived 2-host life cycle in which metacercariae develop inside daughter sporocysts in the intermediate host (intertidal and subtidal gastropods, mostly of the genus Littorina) and are infective to marine birds (ducks, gulls and waders). Here we investigate MPG transmission patterns in coastal ecosystems and their diversification with respect to historical events, host switching and host-parasite co-evolution. Species phylogenies and phylogeographical reconstructions are estimated on the basis of 28S, ITS1 and ITS2 rDNA data and we use a combination of analyses to test the robustness and stability of the results, and the likelihood of alternative biogeographical scenarios. Results demonstrate that speciation within the MPG was not associated with co-speciation with either the first intermediate or final hosts, but rather by host-switching events coincident with glacial cycles in the Northern Hemisphere during the late Pliocene/Pleistocene. These resulted in the expansion of Pacific biota into the Arctic-North Atlantic and periodic isolation of Atlantic and Pacific populations. Thus we hypothesize that contemporary species of MPG and their host associations resulted from fragmentation of populations in regional refugia during stadials, and their subsequent range expansion from refugial centres during interstadials.

Keywords

marine parasitestrematodeMicrophallusparasite speciationparasite transmissionhost-parasite co-evolutionhost switchinghost-parasite assemblages
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1346 - 1360
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Alerstam, T., Bäckman, J., Gudmundsson, G. A., Hedenström, A., Henningsson, S. S., Håkan, K., Rosén, M. and Strandberg, R. (2007). A polar system of intercontinental bird migration. Proceedings of the Royal Society of London, B 274, 2523–2530.Google ScholarPubMed
Anderson, G. R. and Barker, S. C. (1993). Species differentiation in the Didymozoidae (Digenea): Restriction fragment length differences in internal transcribed spacer and 5·8S ribosomal DNA. International Journal for Parasitology 23, 133–136.CrossRefGoogle ScholarPubMed
Bartoli, P., Jousson, O. and Russell-Pinto, F. (2000). The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. The Journal of Parasitology 86, 479–489.CrossRefGoogle ScholarPubMed
Belopolskaya, M. M. (1963). Family Microphallidae Travassos, 1920. In Trematodes of Animals and Man. Vol. 21 (ed. Skrjabin, K. I.), pp. 259–502. USSR Academy of Sciences Press, Moscow-Leningrad, USSR (in Russian).Google Scholar
Bianki, V. V., Boyko, N. S., Ninburg, E. A. and Shklyarevich, G. A. (1979). Feeding of the common eider of the White Sea. In Ecology and Morphology of Eiders in the USSR (ed. Kishchinskiy, A. A.), pp. 126–170. Nauka, Moscow, USSR (in Russian).Google Scholar
Blair, D., Davis, G. M. and Wu, B. (2001). Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123, S229–S243.CrossRefGoogle ScholarPubMed
Briggs, J. C. (2003). Marine centers of origin as evolutionary engines. Journal of Biogeography 30, 1–18.CrossRefGoogle Scholar
Bustnes, J. O., Mosbech, A., Sonne, Ch. and Systad, G. H. (2010). Migration patterns, breeding and moulting locations of king eiders wintering in north-eastern Norway. Polar Biology 33, 1379–1385.CrossRefGoogle Scholar
Ching, H. L. (1991). List of larval worms from marine invertebrates of the Pacific coast of North America. Journal of the Helminthological Society of Washington 58, 57–68.Google Scholar
Cribb, T. H., Bray, R. A., Olson, P. D. and Littlewood, D. T. J. (2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.CrossRefGoogle ScholarPubMed
Dau, C. P., Flint, P. L. and Petersen, M. R. (2000). Distribution of recoveries of Steller's eiders banded on the lower Alaska Peninsula, Alaska. Journal of Field Ornithology 71, 541–548.CrossRefGoogle Scholar
Deblock, S. (1971). Contribution à l’étude des Microphallidae Travassos, 1920. XXIV. Tentative de phylogénie et de taxonomie. Bulletin de Muséum National d'Histoire Naturelle 3e sér, 7, Zoologie 7, 353–469.Google Scholar
Galaktionov, K. V. (1983). Microphallids of the “pygmaeus” group. I. Description of species Microphallus pygmaeus (Levinsen, 1881) nec Odhner, 1905 and M. piriformes (Odhner, 1905) nom. nov. (Trematoda: Microphallidae). Vestnik Leningradskogo Universiteta (Bulletin of the Leningrad University) 15, 20–30 (in Russian).Google Scholar
Galaktionov, K. V. (1984). Microphallids of the “pygmaeus” group. II. Microphallus triangulatus sp. nov. (Trematoda: Microphallidae). Vestnik Leningradskogo Universiteta (Bulletin of the Leningrad University) 3, 5–11 (in Russian).Google Scholar
Galaktionov, K. V. (1993). Life Cycles of Trematodes as Components of Ecosystems. Kola Scientific Centre of the Russian Academy of Sciences Press, Apatity (in Russian).Google Scholar
Galaktionov, K. V. (2009). Description of the maritae and determination of the species status of Microphallus pseudopygmaeus sp. nov. (Trematoda: Microphallidae). Parazitologiya 43, 289–299 (in Russian).Google ScholarPubMed
Galaktionov, K. V., Bulat, S. A., Alekhina, I. A., Saville, D. H., Fitzpatrick, S. M. and Irwin, S. W. B. (2004). An investigation of evolutionary relationships within “pygmaeus” group microphallids (Trematoda: Microphallidae) using genetic analysis and scanning electron microscopy. Journal of Helminthology 78, 231–236.CrossRefGoogle Scholar
Galaktionov, K. V., Regel, K. V. and Atrashkevich, G. I. (2010). Microphallus kurilensis sp. nov., a new species of microphallids from the “pygmaeus” species group (Trematoda, Microphallidae) from the coastal areas of Okhotsk and Bering Seas. Parazitologiya 44, 496–507 (in Russian).Google Scholar
Gladenkov, Yu. B. (1978). Marine Upper Cenozoic of the Northern Regions. Nauka, Moscow, USSR (in Russian).Google Scholar
Golikov, A. N. and Scarlato, O. A. (1989). Evolution of the Arctic ecosystems during the Neogene period. In The Arctic Seas: Climatology, Oceanography, Geology, and Biology (ed. Herman, Y.), pp. 257–279. Van Nostrand Reinhold, New York, USA.CrossRefGoogle Scholar
Harris, A. J. and Xiang, Q.-Y. (2009). Estimating ancestral distributions of lineages with uncertain sister groups: a statistical approach to Dispersal-Vicariance Analysis and a case using Aesculus L. (Sapindaceae) including fossils. Journal of Systematics and Evolution 47, 349–368.CrossRefGoogle Scholar
Hoberg, E. P. (1992). Congruent and synchronic patterns in biogeography and speciation among seabirds, pinnipeds and cestodes. Journal of Parasitology 78, 601–615.CrossRefGoogle ScholarPubMed
Hoberg, E. P. (1995). Historical biogeography and modes of speciation across high-latitude seas of the Holarctic: concepts for host–parasite co-evolution among the Phocini (Phocidae) and Tetrabothriidae. Canadian Journal of Zoology 73, 45–57.CrossRefGoogle Scholar
Hoberg, E. P. and Adams, A. (1992). Phylogeny, historical biogeography, and ecology of Anophryocephalus spp. (Eucestoda: Tetrabothriidae) among pinnipeds of the Holarctic during the late Tertiary and Pleistocene. Canadian Journal of Zoology 70, 703–719.CrossRefGoogle Scholar
Hoberg, E. P. and Adams, A. (2000). Phylogeny, history and biodiversity: understanding faunal structure and biogeography in the marine realm. Bulletin of the Scandinavian Society of Parasitology 10, 19–37.Google Scholar
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 1533–1550.CrossRefGoogle Scholar
Hopkins, D. M. (1959). Cenozoic history of the Bering land bridge. Science 129, 1519–1528.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. and Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.CrossRefGoogle ScholarPubMed
Iwagami, M., Ho, L. Y., Su, K., Lai, P. F., Fukushima, M., Nakano, M., Blair, D., Kawashima, K. and Agatsuma, T. (2000). Molecular phylogeographic studies on Paragonimus westermani in Asia. Journal of Helminthology 74, 315–322.CrossRefGoogle ScholarPubMed
Jousson, O., Bartoli, P., Zaninetti, L. and Pawlowski, J. (1998). Use of the ITS rDNA for elucidation of some life-cycles of Mesometridae (Trematoda, Digenea). International Journal for Parasitology 28, 1403–1411.CrossRefGoogle ScholarPubMed
Krechmar, A. V. and Kondratyev, A. V. (2006). Waterfowl Birds of North-East Asia. NESC FEB RAS, Magadan, Russia (in Russian).Google Scholar
Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. and Littlewood, D. T. J. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma (Weinland, 1858). Parasitology 126, 203–224.CrossRefGoogle ScholarPubMed
Lotfy, W. M., Brant, S. V., DeJong, R. J., Le, T. H., Demiaszkiewicz, A., Rajapakse, J. R. P. V., Perera, V. B. V. P., Laursen, J. R. and Loker, E. S. (2008). Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). The American Journal of Tropical Medicine and Hygiene 79, 248–255.CrossRefGoogle ScholarPubMed
Maddison, D. R. and Maddison, W. P. (2005). MacClade 4: Analysis of Phylogeny and Character Evolution. Sinauer Associates, Inc. Sunderland, MA, USA.Google Scholar
Marincovich, L. (2000). Central American paleogeography controlled Pliocene Arctic Ocean molluscan migrations. Geology 28, 551–554.2.0.CO;2>CrossRefGoogle Scholar
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 102–163.Google ScholarPubMed
Nylander, J. A. A., Olsson, U., Alström, P. and Sanmartín, I. (2008). Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to Dispersal – Vicariance Analysis of the thrushes (Aves: Turdus). Systematic Biology 57, 257–268.CrossRefGoogle ScholarPubMed
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Petersen, M. R., Bustnes, J. O. and Systad, G. H. (2006). Breeding and moulting locations and migration patterns of the Atlantic population of Steller's eiders Polysticta stelleri as determined from satellite telemetry. Journal of Avian Biology 37, 58–68.CrossRefGoogle Scholar
Pina, S., Tajdari, J., Russell-Pinto, F. and Rodrigues, P. (2009). Morphological and molecular studies on life cycle stages of Diphtherostomum brusinae (Digenea: Zoogonidae) from northern Portugal. Journal of Helminthology 83, 321–331.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Reid, D. G. (1996). Systematics and Evolution of Littorina. The Ray Society, London, UK.Google ScholarPubMed
Reid, D. G., Rumbak, E. and Thomas, R. H. (1996). DNA, morphology and fossils: phylogeny and evolutionary rates of the gastropod genus Littorina . Philosophical Transactions of the Royal Society of London, B 351, 877–895.Google ScholarPubMed
Ronquist, F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195–203.CrossRefGoogle Scholar
Ronquist, F. (2001). DIVA Version 1.2. Computer Program for MacOS and Win32. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.Google Scholar
Ronquist, F. and Huelsenbeck, J. (2003). MRBAYES 3: Bayesian inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Saville, D. H., Galaktionov, K. V., Irwin, S. W. B. and Malkova, I. I. (1997). Morphological comparison and identification of metacercariae in the “pygmaeus” group of microphallids, parasites of seabirds in western palearctic regions. Journal of Helminthology 71, 167–174.CrossRefGoogle Scholar
Sher, A. (1999). Traffic lights at the Beringian crossroads. Nature, London 397, 103–104.CrossRefGoogle Scholar
Sonsthagen, S. A., Talbot, S. L., Scribner, K. T. and McCracken, K. G. (2011). Multilocus phylogeography and population structure of common eiders breeding in North America and Scandinavia. Journal of Biogeography, 38, 1368–1380. doi: 10.1111/j.1365-2699.2011.02492.x.CrossRefGoogle Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods). Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Thorley, J. L. and Wilkinson, M. (1999). Testing the phylogenetic stability of early tetrapods. Journal of Theoretical Biology 200, 343–344.CrossRefGoogle ScholarPubMed
Tkach, V. V., Littlewood, D. T. J., Olson, P. D., Kinsella, J. M. and Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.CrossRefGoogle ScholarPubMed
Vermeij, G. J. (1991). Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17, 281–307.CrossRefGoogle Scholar
Webster, M. S., Marra, P. P., Haig, S. M., Bensch, S. and Holmes, R. T. (2002). Links between worlds – unraveling migratory connectivity. Trends in Ecology and Evolution 17, 76–83.CrossRefGoogle Scholar
Yu, Y., Harris, A. J. and He, X. (2010). S-DIVA (Statistical Dispersal-Vicariance Analysis): A tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution 56, 848–850.CrossRefGoogle ScholarPubMed
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