Синдром аномалии P у зеленых лягушек: история открытия, морфологические особенности и возможные причины возникновения

А.О. Свинин, О.А. Ермаков, С.Н. Литвинчук и И.В. Башинский

Труды Зоологического института РАН, 2020, 324(1): 108–123   ·   https://doi.org/10.31610/trudyzin/2020.324.1.108

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Резюме

Аномалия P у зеленых лягушек была впервые найдена во Франции в 1952 г. французским писателем и ученым Жаном Ростаном. При легкой форме проявления она включает в себя полидактилию, тогда как сложные морфологические преобразования затрагивают передние и задние конечности и включают комплекс признаков: полидактилию, брахимелию, инверсию задних конечностей, небольшие дополнительные конечности, костные выросты, опухоли и отеки в области задних конечностей. Ростан экспериментально показал, что эта аномалия не наследуется и вызывается неким фактором, получаемым из окружающей среды. Она была отмечена только у западно-палерктических представителей зеленых лягушек рода Pelophylax и отсутствовала у других видов амфибий, несмотря на их синтопичное обитание. Тяжелые случаи аномалии P долго не встречались исследователям и были вновь обнаружены спустя полвека с момента их последней регистрации. Новая находка была сделана в 2016 г. в центральной части России, в заповеднике «Приволжская лесостепь». Морфологические особенности аномальных особей лягушек на исследуемой территории оказались схожими с таковыми, описанными Ростаном. Обнаружены симметричная полидактилия, брахимелия, инверсия задних конечностей, отеки бедренной области задних конечностей, небольшие дополнительные конечности в области бедер, костные выросты, а также сопутствующие аномалии – мандибулярная гипоплазия, негнущаяся задняя конечность, несрастание оперкулярной камеры. Частота встречаемости аномалии P в изученной популяции достигала 24.7% (n = 384). Причем «тяжелые формы» аномалии были отмечены в 4.7% случаев, а «легкие» (полидактилия) – у 20.0%. Позднее в разных регионах России было обнаружено еще три популяции с тяжелыми случаями аномалии Р. Выращивание головастиков совместно с пресноводными моллюсками позволило нам получить аномалию P в лаборатории. Выявлено, что промежуточным хозяином (вектором) для «инфекционного агента» этой аномалии служит роговая катушка Planorbarius corneus. В качестве наиболее вероятной причины возникновения аномалии рассматривается заражение определенным видом трематод.

Ключевые слова

амфибии, аномалия P, Жан Ростан, зеленые лягушки, морфологические аномалии, трематоды, Pelophylax

Поступила в редакцию 21 июля 2019 г.  ·  Принята в печать 17 февраля 2020 г.  ·  Опубликована 24 марта 2020 г.

Литература

Ben Hassine J., de Buffrenil V. and Nouira S. 2011. First record of morphological abnormalities in natural populations of two amphibian species in Tunisia. Journal of Herpetology, 45(4): 465–471. https://doi.org/10.1670/10-002.1

Bezman-Moseyko O.S., Borkin L.J., Rozanov Y.M. and Litvinchuk S.N. 2014. Mass hindlimb deformities of green frogs (Pelophylax esculentus complex) in Pridnestrovie: causes and bioindication. Anomalies and Pathologies of Amphibians and Reptiles: Methodology, Evolutionary Significance, the Ability to Assess the Health of the Environment. Ekaterinburg: Publishing House of the Ural University: 13–19. [In Russian].

Bonnet A. and Rey M. 1937. Sur quelques cas de polydactyly et de schistodactylie observes en série chez la grenouille. Bulletin de la Société zoologique de France, 62 : 21–25.

Borkin L.J. 2014. Morphological abnormalities in natural populations of amphibians: What do we study and how do we measure? Anomalies and Pathologies of Amphibians and Reptiles: Methodology, Evolutionary Significance, the Ability to Assess the Health of the Environment. Ekaterinburg: Publishing House of the Ural University: 25–36. [In Russian].

Borkin L.J. and Pikulik M.M. 1986. The occurrence of polymely and polydactyly in natural populations of anurans of the USSR. Amphibia–Reptilia, 7: 205–216. https://doi.org/10.1163/156853886X00019

Borkin L.J., Bezman-Moseyko O.S. and Litvinchuk S.N. 2012. Evaluation of the occurrence of morphological anomalies in natural populations (using amphibians as an example). Proceedings of the Zoological Institute RAS, 316(4): 324–343. [In Russian].

Burkhart J.G., Ankley G., Carpenter H., Fort D., Gardiner D., Gardner H., Hale R., Helgen J. C., Jepson P., Johnson D., Lannoo M., Lee D., Lary J., Levey R., Magner J., Meteyer C., Shelby M.D. and Lucier G. 2000. Strategies for assessing the implications of frog malformations for environmental and human health. Environmental Health Perspectives, 108(1): 83–90. https://doi.org/10.1289/ehp.0010883

Dubois A. 1979. Anomalies and mutations in natural populations of the Rana esculenta” complex (Amphibia, Anura). Mitteilungen aus dem zoologischen Museum in Berlin, 55(1): 59–87. https://doi.org/10.1002/mmnz.4830550108

Dubois A. 1984. L’anomalie P des Grenouilles vertes (complexe de Rana kl. esculenta Linné, 1758) et les anomalies voisines chez les Amphibiens. Comptes rendus du Premier Colloque international de Pathologie des Reptiles et des Amphibiens, Angers (Presses Universitaires d’Angers): 215–221.

Dubois A. 2014. The anomaly P in palaearctic green frogs of the genus Pelophylax (Ranidae). Anomalies and Pathologies of Amphibians and Reptiles: Methodology, Evolutionary Significance, the Ability to Assess the Health of the Environment. Ekaterinburg: Publishing House of the Ural University: 96–104.

Dubois A. 2017. Rostand’s anomaly P in Palaearctic green frogs (Pelophylax) and similar anomalies in amphibians. Studies on Anomalies in Natural Populations of Amphibians. Mertensiella, 25: 49–56.

Fayzulin A.I. 2012. Occurrence and morphological anomalies variety of populations of the marsh frog (Anura, Amphibia) of the Middle Volga. Proceedings of the Samara Scientific Center of the Russian Academy of Sciences, 14(5): 150–154. [In Russian].

Fayzulin A.I., Chikhlyaev I.V., Mineev A.K., Kuzovenko A.E., Mihaylov R.A., Zaripova F.F., Popov A.I. and Ermakov O.A. 2018. New data on the anomalies of tailless amphibians of the Volga Basin. Second International Conference on Amphibian and Reptiles Anomalies and Pathology: Methodology, Evolutionary Significance, Monitoring and Environmental Health. KnE Life Sciences: 29–35. https://doi.org/10.18502/kls.v4i3.2099

Guex G.-D., Hotz H., Uzzell Th., Semlitsch R.D., Beerli P. and Pascolini R. 2001. Developmental disturbances in Rana esculenta tadpoles and metamorphs. Zoosystematics and Evolution, 77(1): 79–86. https://doi.org/10.1002/mmnz.20010770113

Henle K., Dubois A. and Vershinin V. 2017a. A review of anomalies in natural populations of amphibians and their potential causes. Studies on Anomalies in Natural Populations of Amphibians. Mertensiella, 25: 57–164.

Henle K., Dubois A. and Vershinin V. 2017b. Commented glossary, terminology and synonymies of anomalies in natural populations of amphibians. Studies on Anomalies in Natural Populations of Amphibians. Mertensiella, 25: 9–48.

Henle K., Rimpp K., Margraf J. and Dubois A. 2017c. The Roβwag affair: history and controversy of the discovery of mass anomalies in the green toad (Bufotes viridis) in a German quarry. Studies on Anomalies in Natural Populations of Amphibians. Mertensiella, 25: 165–184.

Henle K., Dubois A., Rimpp K. and Vershinin V. 2017d. Mass anomalies in green toads (Bufotes viridis) at a quarry in Roβwag, Germany: inbred hybrids, radioactivity or an unresolved case? Studies on Anomalies in Natural Populations of Amphibians. Mertensiella, 25: 185–242.

Hillenius D. 1959. A second case of “Anomaly P” (Rostand) in Rana esculenta Linné. Med. Klinik. 54: 99–100.

Jayawardena U.A., Tkach V.V., Navaratne A.N., Amerasinghe P.H. and Rajakaruna R.S. 2013. Malformations and mortality in the Asian common toad induced by exposure to Pleurolophocercous cercariae (Trematoda: Cryptogonimidae). Parasitology International, 62(3): 246–252. https://doi.org/10.1016/j.parint.2013.01.003

Jayawardena U.A., Rohr J.R., Navaratne A.N., Amerasinghe P.H. and Rajakaruna R.S. 2016. Combined effects of pesticides and trematode infections on hourglass tree frog Polypedates cruciger. Ecohealth, 13(1): 111–122. https://doi.org/10.1007/s10393-016-1103-2

Johnson P.T.J., Lunde K.B., Ritchie E.G. and Launer A.E. 1999. The effect of trematode infection on amphibian limb development and survivorship. Science, 284(5415): 802–804. https://doi.org/10.1126/science.284.5415.802

Johnson P.T.J., Lunde K.B., Haight R.W., Bowerman J. and Blaustein A.R. 2001. Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology, 79(3): 370–379. https://doi.org/10.1139/z00-210

Johnson P.T.J., Lunde K.B., Thurman E.M., Rit­chie E.G., Wray S.W., Sutherland D.R., Kapfer J.M., Frest T.J., Bowerman J. and Blaustein A.R. 2002. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs, 72(2): 151–168. https://doi.org/10.2307/3100022

Johnson P.T. and Sutherland D.R. 2003. Amphibian deformities and Ribeiroia infection: an emerging helminthiasis. Trends in Parasitology, 19(8): 332–335. https://doi.org/10.1016/s1471-4922(03)00148-x

Kholodkovskiy N.A. 1897. Two examples of polydactyly. Proceedings of the Imperial Saint Petersburg Society of Naturalists, 27(2): 74–80. [In Russian].

Kozhevnikova V.N. and Lada G.A. 2016. On polydactyly in the marsh frog Pelophylax ridibundus (Pallas, 1771) in Tambov Province. Tambov University Bulletin. Series: Natural and Technical Sciences, 21(1): 265–268. [In Russian]. https://doi.org/10.20310/1810-0198-2016-21-1-265-268

Kovalenko E.E. 2000. Mass anomalies of extremities in Anura. Zhurnal Obshchei Biologii, 61(4): 412–427.

Kovalenko E.E. and Kovalenko Y.I. 2000. Hind limb anomalies in laboratory clawed frogs Xenopus laevis (Anura, Pipidae). 1. The phenomenon of mass anomalies. Vestnik of Saint Petersburg University, Ser. 3 (Biol.), 1(3): 3–22.

Lada G.A. 1999. Polydactyly in anurans in the Tambov Region (Russia). Russian Journal of Herpetology, 6(2): 104–106. https://doi.org/10.30906/1026-2296-1999-6-2-104-106

Machado C., Kwet A. and Schlüter A. 2010. Polydactyly and polymely in two populations of Rana temporaria and Pelophylax esculentus (Anura, Ranidae) in southern Germany. Salamandra, 46(4): 239–242.

Marushchak A.Y., Kuzmin Y.I., Oskirko A.S., Dmitrieva I.G. and Nekrasova O.D. 2017. Investigation of morphological anomalies and inflammation by helminths of marsh frogs, Pelophylax ridibundus (Pallas, 1771), in separate populations of the Kiev city. Proceedings of the Zoological Museum, Kiev, 48: 38–45. [In Russian].

Marushchak O.Y. and Muravynets O.A. 2018. Morphological abnormalities in tailless amphibians (Amphibia, Anura) in Ukraine. Geo & Bio, 16: 76–82. https://doi.org/10.15407/gb.2018.16.076

McKinnell R.G. 1973. The Lucké frog kidney tumor and its herpesvirus. American Zoologist, 13(1): 97–114. https://doi.org/10.1093/icb/13.1.97

Mizgireuv I.V., Flax N.L., Borkin L.J. and Khudoley V.V. 1984. Dysplastic lesions and abnormalities in amphibians associated with environmental conditions. Neoplasma, 31(2): 175–181.

Nekrasova O.D., Mezhzherin S.V., Morozov-Leonov S.Y. and Sytnik Y.M. 2007. A cases of mass polymelia in the lake frog (Rana ridibunda Pall., 1771) from Kyiv. The Science Bulletin of Uzhgorod University. Ser. Biol., 21: 92–95. [In Russian].

Rajakaruna R.S., Piyatissa P.M.J.R., Jayawardena U.A., Navaratne A.N. and Amerasinghe P.H. 2008. Trematode infection induced malformations in the common hourglass treefrogs. Journal of Zoology, 275: 89–95. https://doi.org/10.1111/j.1469-7998.2008.00416.x

Rostand J. 1947. De quelques anomalies digitales chez le crapaud ordinaire (Bufo bufo). La Revue Scientifique, 85: 1121–1125.

Rostand J. 1949. Polydactylie naturelle chez la grenouille verte (Rana esculenta). Comptes rendus de l’Académie des Sciences, 228: 1666–1667.

Rostand J. 1951. La génétique des Batraciens. Paris (Hermann et Cie): 1–80.

Rostand J. 1952. Sur la variété d’expression d’une certain anomalie (P) chez la grenouille verte (Rana esculenta L.). Comptes rendus de l’Académie des Sciences, 235: 583–585.

Rostand J. 1958. Les anomalies des Amphibiens Anoures. Paris, Sedes, 100 p.

Rostand J. 1971. Les étangs à monstres. Histoire d’une recherché (1947–1970). Paris, Stock, 91 p.

Rostand J. and Darré P. 1967. Sur les conditions d’apparition de l’anomalie P chez Rana esculenta. Comptes rendus de l’Académie des Sciences, 265: 761–762.

Rostand J. and Darré P. 1968. Conditions déterminantes de l’anomalie P chez Rana esculenta. Comptes rendus des séances de la Société de Biologie et sa Filiales, 162: 1682–1683.

Rostand J. and Darré P. 1969. Action tératogène des déjections de certains poissons sur les larves de Rana esculenta. Comptes rendus des séances de la Société de Biologie et sa Filiales, 163: 2033–2034.

Rostand J., Jacquot M. and Darré P. 1967. Nouvelles expériences sur les causes de l’anomalie P chez Rana esculenta. Comptes Rendus Hebdomadaires Séances de l’Académie des Sciences Paris, 264: 2395–2397.

Sas I. and Kovacs E.-H. 2006. Hexadactyly case at a Rana kl. esculenta sample from the north-western part of Romania. Analele Universit ăţii din Oradea. Fascicula Biologie, 13: 52–53.

Sessions S.K. and Ruth S.B. 1990. Explanation for naturally occurring supernumerary limbs in amphibians. Journal of Experimental Zoology, 254: 38–47. https://doi.org/10.1002/jez.1402540107

Sessions S.K., Franssen R.A. and Horner V.L. 1999. Morphological clues from multilegged frogs: are retinoids to blame? Science, 284: 800–802. https://doi.org/10.1126/science.284.5415.800

Silantiev A. 1898. Zoological studies on the sections of the Expedition of the Forest Department (1894–96). Proceedings of the Expedition of the Forest Department, 4(2): 1–230. [In Russian].

Surleve-Bazeille J.E. and Cambar R. 1969. New research on transmission modality of anomaly P in green frog (Rana esculenta L.). Comptes rendus des séances de la Société de Biologie et sa Filiales, 163: 2034–2037.

Surlève-Bazeille J.-E., Cambar R. and Mauget R. 1969. Essay on transmission of anomaly P to diverse species of amphibians. First results obtained on Rana temporaria. Actes de la Société Linnéenne de Bordeaux, Série A, 106(2): 1–7.

Svinin A.O. 2014. The occurrence of morphological anomalies in green frog population systems (Pelophylax Fitzinger, 1843) from the north-eastern part of the areas. Anomalies and Pathologies of Amphibians and Reptiles: Methodology, Evolutionary Significance, the Ability to Assess the Health of the Environment. Ekaterinburg: Publishing House of the Ural University: 156–161. [In Russian].

Svinin A.O., Bashinskiy I.V., Neymark L.A., Katsman E.A. and Osipov V.V. 2018. Morphological anomalies of anuran amphibians in the Khoper river valley of «Privolzhskaya Lesostep’» nature reserve and adjacent territories. Amphibian and Reptiles Anomalies and Pathology: Methodology, Evolutionary Significance, Monitoring and Environmental Health. KnE Life Sciences: 150–155. https://doi.org/10.18502/kls.v4i3.2117

Svinin A.O., Bashinskiy I.V., Litvinchuk S.N., Neymark L.A., Osipov V.V., Katsman E.A., Ermakov O.A., Ivanov A.Yu., Vedernikov A.A., Drobot G.P. and Dubois A. 2019a. First record of the Jean Rostand’s “anomaly P” in the marsh frog, Pelophylax ridibundus, in central Russia. Alytes, 37(1–2): 31–45.

Svinin A.O., Bashinskiy I.V., Osipov V.V., Neymark L.A., Ivanov A.Yu, Ermakov O.A. and Litvinchuk S.N. 2019b. New records of the anomaly P syndrome in two water frog species (Pelophylax ridibundus and P. lessonae) in Russia. Herpetozoa, 32: 277–281. https://doi.org/10.3897/herpetozoa.32.e47205

Svinin A. O., Bashinskiy I.V., Litvinchuk S.N., Ney­mark L.A., Ivanov A.Y., Ermakov O.A., Vedernikov A.A. and Dubois A. 2019c.Planorbarius corneus is an intermediate host of the infectious agent of Rostand’s “anomaly P” in green frogs. Russian Journal of Herpetology, 26(6): 349–353. https://doi.org/10.30906/1026-2296-2019-26-6-349-353

Svinin A.O., Vedernikov A.A., Neymark L.A., Ivanov A.Yu., Ermakov O.A. and Bashinsky I.V. 2019d. Three-year monitoring of Rostand’s anomaly in the marsh frog populations from “Ostrovtsovskaya Lesosteppe”. Modern Problems of Medicine and Natural Sciences, Vol. 8. Yoshkar-Ola: 157–159. [In Russian].

Szuroczki D., Vesprini N.D., Jones T.R.B., Spencer G.E. and Carlone R.L. 2012. Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels. Parasitology Research, 110(1): 49–59. https://doi.org/10.1007/s00436-011-2451-z

Vershinin V.L. 1989. Morphological anomalies of amphibians in the urban area. Russian Journal of Ecology, 3: 58–66. [In Russian].

Vershinin V.L. 2002. Ecological specifity and microevolution in amphibian populations in urbanized areas. Advances in Amphibian Research in the Former Soviet Union, 7: 1–161.

Vershinin V.L. and Neustroeva N.S. 2011. The role of trematode invasion in the specificity of skeletal of tailless amphibians on the example of Rana arvalis Nilsson, 1842. Doklady Biological Sciences, 440(2): 279–281. [In Russian]. https://doi.org/10.1134/S0012496611050073

Voitkevich A.A. 1948. Phenomenon of hereditary distortion of the realization of formative potency. Reports of the Academy of Sciences of the USSR, 60(2): 305–308. [In Russian].

Voitkevich A.A. 1958. The peculiar reduction of the tibia with doubling of a limb in a frog in nature. Reports of the Academy of Sciences of the USSR, 118(4): 841–844. [In Russian].

Voitkevich A.A. 1965. Mass formation of additional hind limbs in the marsh frog. Journal of General Biology, 26(1): 56–62. [In Russian].

Woitkewitch A.A. 1961. Le developpement des extremites surnumeraires chez les amphibiens. Bulletin Biologique de la France et de la Belgique, 95: 569–600.

Zaks M.M. 2008. On the morphological anomalies of green frogs (Rana ridibunda, R. lessonae) of the city of Penza. Izvestia of the Penza State University, 14(10): 63–65. [In Russian].

Zamaletdinov R.I. 2003. Morphological anomalies in urban populations of tailless amphibians (on the example of Kazan). Current Studies in Herpetology, 2: 148–153. [In Russian].

 

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