Behavioral differentiation and hybridization of the European and Asian forms of Harting’ vole <i>Microtus hartingi</i> (Rodentia, Arvicolinae)

Zorenko, T.A.; Atanasov, N.; Golenishchev, F.N.

Russian Journal of Theriology. Main page

Behavioral differentiation and hybridization of the European and Asian forms of Harting’ vole Microtus hartingi (Rodentia, Arvicolinae)
Zorenko T.A., Atanasov N., Golenishchev F.N.
P. 133-150
The final isolation of Europe from Asia took place comparatively not long ago — in the early Holocene – late Pleistocene which led to the division of Microtus hartingi area into two isolated parts (Asian–Central and West Anatolia and European–southern Balkans). The Northern Mediterranean was influenced by considerable climatic and habitat fluctuations that caused fragmentation of a potential area of Microtus hartingi and promoted microevolutionary processes. The purpose of the work was evaluation of the range disjunction influence on diversification of the species. We analyzed (1) copulatory behavior, (2) exploratory activity and ability to overcome the stress, (3) growth and development of pups, and also (4) hybridization success in the two nominal forms of M. hartingi — M. h. lydius and M. h. strandzensis. Considerable changes in behavior of individuals of two subspecies were obtained. As a result of the hybridization of the two forms, viable and prolific posterity of F1 was received, but the subsequent cross breeding including backcrossing sterility of males and high mortality of posterity began to be established. The testes and the epididymis of the hybrids were with smaller weight in comparison with parents’ subspecies, especially M. h. lydius, reduced quantity of spermatozoa and small percent mobile of them which confirmed the lower level of spermatogenesis. We assume that evolution of the phenotypic characteristics of the voles was supported by gene drift and probably by the selection, induced by the stress more strongly, than changes in the genotypic characteristics, e.g. distinctions on cytochrome b and the karyotype are not significant. This can be explained as an influence of specific ecological conditions and fragmentation of the habitats in the Northern Mediterranean Region. Until recently M. h. lydius and M. h. strandzensis were considered as subspecies. However, they reached considerable degree of a divergence and the question of their specific status has to be considered additionally.

DOI: 10.15298/rusjtheriol.15.2.06

Литература

Akhverdyan M.R., Vorontsov N.N. & Lyapunova E.A. 1991. [The shidlovsky’s vole Microtus schidlovskii (Rodentia, Cricetidae) — an independent species of fauna Armenia] // Biologichesky Zhurnal Armenii. Vol.4. No.44. P.266–271 [in Russian].

Atanasova I., Raykov I., Raykova V. & Vasilev V. 2010. Outlining the most northerly points of the habitat of Guenther“s vole Microtus guentheri (Danford & Alston, 1888) in Bulgaria and some ecological notes // Annual of Konstsntin Preslavski University, Bulgaria, Faculty of Natural Sciences, Vol.20. No6. P.148–168.

Avise J.C., Arnold J., Ball R. et al. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics // Annual Review of Ecology, Evolution and Systematics. Vol.18. P.489–522.

Badyaev A.V. 2008. Maternal effects as generators of evolutionary change. A reassessment //Annals of the New York Academy of Sciences. No.1133. P.151–161.

Bashenina N.V. 1977. [The Trends in Adaptation of Small Rodents]. Moskva: Izdatel’stvo Nauka. 355 p. [in Russian].

Bond J.E., Hedin M.C., Ramirez M.G. & Opell B.D. 2001. Deep molecular divergence in the absence of morphological and ecological change in the Californian coastal dune endemic trap-door spider Aptostichus simus // Molecular Ecology. Vol.10. No.4. P.899–910.

Borodin P.M., Barreiros-Gomez S.C., Zhelezova A.I., Bonvicino C.R. & D’Andrea P.S. 2006. Reproductive isolation due to the genetic incompatibilities between Thrichomys pachyurus and two subspecies of Thrichomys apereoides (Rodentia, Echimyidae) // Genome. Vol.49. No.2. P.159–167.

Castiglia R. & Capanna E. 2000. Contact zone between chromosomal races of Mus musculus domesticus. 2. Fertility and segregation in laboratory-reared and wild mice heterozygous for multiple robertsonian rearrangements // Heredity. Vol.85. P.147–156.

Chassovnikarova T.G., Markov G.G., Atanasov N.I. & Dimitrov H.A. 2008. Sex chromosome polymorphism in Bulgarian populations of Microtus guentheri (Danford & Alston, 1880) // Journal Natural History. Vol.42. No.5-8. P.261–267.

Crusio W.E., Schwegler H., van Abeelen J.H.F. 1989. Behavioral responses to novelty and structural variation of the hippocampus in mice. I. Quantitative–genetic analysis of behavior in the open-field. // Behavioral Brain Research. Vol.32. No1. P.75–80.

Crusio W.E. & van Abeelen J.H.F. 1986. The genetic architecture of behavioral responses to novelty in mice // Heredity. Vol.56. P.55–63.

Dewsbury D.A. 1972. Patterns of copulatory behaviour in male mammals // The Quarterly Review of Biology. Vol.47. No.1. P.1–33.

Erman A. & Parson P. 1984. [Genetics of Behavior and Evolution]. Translated from English. Moskva: Izdatel’stvo Mir. 566 p. [in Russian].

Esin N.V., Yanko-Hombach V. & Kukleva O.N. 2010. Mathematical model of the Late Pleistocene and Holocene transgressions of the Black Sea // Quaternary International. Vol.225. P.180–190.

Ferguson J.W.H. 2002. On the use of genetic divergence for identifying species // Biological Journal of Linnaean Society. Vol.75. P.509–516.

Frynta D. 1993 (1994). Exploratory behaviour in 12 Palaearctic mice species (Rodentia: Muridae): A comparative study using “free exploration” tests // Acta Societatis Zoologicae Bohemicae. Vol.57. P.173–182.

Golenishchev F.N. & Abramson N.I. 2011. [New data on phylogeography of voles’ subgenus Sumeriomys (Arvicolinae, Rodentia)] // Rozhnov V.V. et al. (eds.) Proceedings of International Conference “Mammals of Russia and Adjacent Territories”. IX Congress of Theriological Society, RAS. Moscow: KMK Scientific Press. P.117 [in Russian].

Golenishchev F.N. & Malikov V.G. 2011. [The systematics and distribution of the grey voles of the tribe Microtini (Rodentia, Arvicolinae) in the Caucasus and Asia Minor] // Movsesyan S.O. et al. (eds.) Proceeding of the International Conference “Biological diversity and conservation problems of the fauna of the Caucasus”. 26–29 September 2011. Yerevan: LLC Spika. P.101–105 [in Russian].

Golenishchev F.N., Gerasimov C. & Sablina O.V. 1991. [Reproduction, postnatal growth and development of the voles (subgenus Sumeriomys)] // Proceedings of Zoological Institute RAS. Vol.243. P.71–80 [in Russian with English summary].

Golenishchev F.N., Sablina O.V., Borodin P.M. & Gerasimov S. 2002. Taxonomy of voles of the subgenus Sumeriomys Argyropulo, 1993 (Rodentia, Arvicolinae, Microtus) // Russian Journal of Theriology. Vol.1. No.1. P.43–55.

Golenishchev F.N., Malikov V.G., Nazari F., Vaziri A. Sh., Sablina O.V. & Polyakov A.V. 2003. New species of vole of “guentheri” group (Rodentia, Arvicolinae, Microtus) from Iran // Russian Journal of Theriology. Vol.1. No.2. P.117–123.

Gromov I.M. & Erbayeva M.A. 1995. [The Mammals of Russia and Adjacent Territories. Lagomorpha and Rodents]. Saint Perersburg: Zoologicheskii Institut RAN. 520 p. [in Russian].

Kurilo L.F. 2001. [Handbook WHO for laboratory study of human semen and sperm interaction with cervical mucous]. Moscow: MedPress. 144 p. [in Russian].

Karnaukhov A.V. & Karnaukhov V.N. 1997. [Where the Siberian Rivers were flowing during the Ice Age?] // Priroda. No.1. P.46–55 [in Russian].

Krushinsky L.V. 1991. [Evolutionary-genetic Aspects of Behavior]. Moskva: Izdatel’stvo Nauka. 259 p. [in Russian].

Kryљtufek B. & Vohrбlik V. 2005. Mammals of Turkey and Cyprus. Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae. Ljubljana: Univerza na Primorskem, Znanstveno-raziskovalno srediљиe Koper, Založba Annales, Zgodovinsko druљtvo za južno Primorsko. 292 p.

Kryљtufek B., Vohrбlik V., Zareie R. & Цzkan B. 2009. Mithochondrial cytochrom b sequences into the speciation of social voles in southwest Asia // Biological Journal of Linnaean Society. Vol.98. P.121–128.

Makaryan C.R., Dadikyan K.M. & Papanyan C.B. 1991. [Morphological features of hybrids of voles (female Misrotus schidlovskii Argyropule 1933  male Microtus socialis binominatus Ellerm, 1941)] // Biologichesky Zhurnal Armenii. Vol.44, No.3-4. P.175–186 [in Russian].

Markov G. 1960. Microtus gьentheri strandzensis subsp. nov., eine neue wьhlmaus-unterart im Strandza–Gebirge, Ostbulgarien // Comptes Rendus de l‘Academia Bulgare des Sciences. Vol.13. P.615–617.

Markov G., Yiğit N., Зolak E., Kocheva M. & Gospodinova M. 2014. Epigenetic diversity and similarity of the voles of “guentheri” group (Mammalia: Rodentia) in Anatolian Peninsula and South–Eastern part of the Balkan Peninsula // Acta Zoologica Bulgarica. Vol. 66. No.2. P.159–164.

Meaney M.J. & Szyf M. 2005. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome // Dialogues Clinic Neuroscience. Vol.7. P.103–123.

Meshkova N.N. & Fedorovich E.F. 1996. [Exploratory Behavior, Imitation and Play as Psychological Mechanisms of Adaptation of Animals to the Urbanized Environment]. Moscow: Izdatel’stvo Argus. 224 p. [in Russian].

Minkova T. 2004. Small mammals (Insectivora and Rodentia) of the Eastern Rhodopes (Bulgaria) // Beron P., Popov A. (eds.). Biodiversity of Bulgaria. 2. Biodiversity of Eastern Rhodopes (Bulgaria and Greece). Sofia: Pensoft & Nat. Mus. Hist. P.895–906.

Musser G.G. & Carleton M.D. 2005. Superfamily Muroidea // Wilson D.E. & Reeder A.M. (eds.). Mammal Species of the World. Third edition. Baltimore: Johns Hopkins University Press. Vol.2. P.894–1531.

Ondrias J.C. 1965. Contribution to the knowledge of Microtus guentheri hartingi from Thebes, Greece // Mammalia. Vol.29. P.489–506.

Ondrias J.C. 1966. The taxonomy and geographical distribution of the rodents of Greece // Sдugetierkundliche Mittelungen. Vol.14. P.1–136.

Pavlinov I.Ya. 1992. [Whether there is a biological species or what is the harm of the systematics] // Zhurnal Obschei Biologii. Vol.53. No.5. P.757–767 [in Russian].

Perissoratis C. & Conispoliatis N. 2003. The impacts of sea–level changes during latest Pleistocene and Holocene times on the morphology of the Ionian and Aegean seas (SE Alpine Europe) // Marine Geology. Vol.164. No.3–4. P.145–156.

Polyakov I.Y. 1959. [Morphophysiological variability of populations of rodents under the influence of environmental conditions] // Soveshchanie po Ekologicheskoi Fiziologii. Part 1. Moskva–Leningrad: AN SSSR Publ. P.46–49 [in Russian].

Ryan W.B. & Pitman W.C. 1999. Noah’s Flood: The New Scientific Discoveries about the Event That Changed History. New York: Simon and Schuster. 319 p.

Schwartz S.S., Kopein K.I. & Pokrovsky A.V. 1960. [Comparative study of some biological features of voles Microtus gregalis gregalis Pall. and Microtus gregalis major Ogn. and their hybrids] // Zoologicheskii Zhurnal. Vol.39. No.6. P.912–926 [in Russian].

Shchipanov N.A. & Kasatkin M.V. 1996. [Microtus socialis in changes landscapes of south Dagestan: population aspect of survival] // Zoologicheskii Zhurnal. Vol.75. No.9. P.1412–1426 [in Russian with English summary].

Shepherd G. 1983. Neurobiology. New York, Oxford: Oxford University Press. 500 p.

Shilova S.A. & Kasatkin M.V. 2000. [A comparative analysis of the population structure of social vole (Microtus socialis Pall., 1773, Cricetidae, Rodentia) in different parts of the area] // Ekologiya. No.4. P.287–294 [in Russian with English summary].

Simakova A.N. 2008. Development of a vegetable cover of East European Plain and Western Europe in the late Neopleistocene — the middle Holocene (33–4.8 BP). Avtoreferat na soiskanie uchenoi stepeni kandidata geologicheskih i mineralogicheskih nauk. Moskva. 34 p. [in Russian].

Thanou E., Fraguedakis-Tsolis S.E., Chondropoulos B., Paragamian K. & Lymberakis P. 2011. Ancient DNA clarifies the systematic and phylogenetic status of the only vole species living in Africa // Borsch T., Giere P., Hoffmann J. et al. (eds.) BioSystematics Berlin. Berlin: Freie Universitдt Berlin. P.355–356.

Thanou E., Tryfonopoulos G., Chondropoulos B. & Fraguedakis-Tsolis S.E. 2012. Comparative phylogeography of the live Greek vole species infers the existence of multiple South Balkan subrefugia // Italian Journal of Zoology. Vol.79. No.3. P.363–376.

van Abeleen J.H.F. 1970. Genetics of rearing behavior in mice // Behavioural Genetics. Vol.1. P.71–76.

Velikanov A., Danov Ch., Marikov Ch. & Vladeev P. 1983. [Black sea]. Leningrad: Hidrometeoizdat. 408 p. [in Russian].

Vigorov J.L., Bolshakov V.N. & Pokrovsky A.V. 1977. [Experimental study of the exploratory and emotional behavior of four species of voles] // Povedenie Mlekopitayushchikh. Moskva: Izdatel’stvo Nauka. P.247–267 [in Russian].

Vigorov J.L. 1980. [Specific and ecological differences of an exploratory behavior of some small rodents’ species] // Ryabitsev V.K. (ed.) Ekologicheskie Aspekty Povedeniya Zhivotnikh. Sverdlovsk: Izdatel’stvo Uralskogo Nauchnogo Tsentra AN SSSR. P.61–81 [in Russian].

Weaver I.C. 2007. Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let’s call the whole thing off // Epigenetics. Vol.2. No.1. P.22–28.

Yiğit N. & Зolak E. 2002. On the distribution and taxonomic status of Mirotus guentheri Danford and Alston, 1880 and Microtus lydius Blackler, 1916 (Mammalia: Rodentia) in Turkey // Turkish Journal of Zoology. Vol.26. P.197–204.

Yiğit N., Markov G., Зolak E.., Kocheva M., Saygılı F., Yüce D. & Зam P. 2012. Phenotypic Features of the “Guentheri” Group Vole (Mammalia: Rodentia) in Turkey and Southeast Bulgaria: Evidence for Its Taxonomic Detachment // Acta Zoologica Bulgarica. Vol.64. No.1. P.23–32

Zakharyan C.A. 1958. [Systematics of Microtus guentheri schidlovskii Arg.] // Doklady AN Armyanskoy SSR. Vol.26. No.2. P.125–128 [in Russian].

Zhabin C.G, Artifeksov S.B., Nagaytsev V.M., Artifeksova M.S., Treshchenkov E.A. & Pavlenko I.I. 2010. [Modern ideas of maturation of spermatozoa in the epididymis of testis] // Problemi reproduktsii. Vol.2. P.66–73 [in Russian with English summary].

Zima J., Arslan A., Benda P., Macholаn M. & Kryљtufek B. 2013. Chromosomal variation in social voles: a Robertsonian fusion in Gыnter’s vole // Acta Theriologica. Vol.58. P.255–265.

Zorenko T.A. 1996. [Reproductive behavior of mammals] // Laboratornye Zhivotnye. Vol.6. No.2. P.95–109 [in Russian with English summary].

Zorenko T.A. 2000. [Morphology of genitals and sexual behavior of social voles of the subgenus Sumeriomys (Arvicolinae, Microtus)] // Zoologicheskii Zhurnal. Vol.79 No.8. P.990–999 [in Russian with English summary].

Zorenko T.A. 2012. [The taxonomical status of the social vole from Kopet Dagh] // Litvinov Yu.N. et al. (eds.). Aktual’nye Problemy Sovremennoi Teriologii. Novosibirsk: LLC Subregion Info. P.51 [in Russian].

Zorenko T. 2013. [Social Voles of the Subgenus Sumeriomys: Systematics, Biology and Behaviour]. Saarbrьcken: Palmariun Academic Publishing. 541 p. [in Russian].

Zorenko T.A. & Andersone Zh.E. 1996. [Play behaviour in voles (Rodentia, Arvicolinae)] // Zoologicheskii Zhurnal. Vol.75. No.10. P.1560–1572 [in Russian with English summary].

Zorenko T. & Golenishchev F. 2015. The spermatozoa structure peculiarities of the subgenus Sumeriomys Argyropulo, 1933 (Rodentia, Arvicolinae, Microtus) // Russian Journal of Theriology. Vol.14. No.1. P.105–111.

Zorenko T.A. & Malygin V.M. 1984. [The effect of the mechanisms of ethological reproductive isolation for the hybridization of three species of common voles group arvalis (Microtus, Cricetidae)] // Zoologicheskii Zhurnal. Vol.63. No.7. P.1072–1983 [in Russian with English summary].

Zorenko T.A., Zakharov K.V. & Berezina R.J. 1989. [Exploratory behavior of voles: microevolutional and taxonomical aspects] // Zorenko T.A. & Zakharov K.V. (eds.) Aktualnye Problemy Zoologii. Riga: University of Latvia. P.57–110 [in Russian with English summary].

Zorenko T.A., Golenishchev F.N. & Skinderskaya I.A. 1997. [Peculiarities of the behaviour in social voles of the subgenus Sumeriomys (Arvicolinae, Microtus) in hybridization] // Baltic Journal of Laboratory Animal Science. Vol.7. No.2. P.77–102 [in Russian with English summary].

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