Mating behavior of house mice of Trans-Caucasian hybrid zone: a comparative study with parent species Mus musculus

Mating behavior of house mice of Trans-Caucasian hybrid zone: a comparative study with parent species Mus musculus

Ambaryan A.V., Kotenkova E.V.

P. 149-160

The functional significance of the different types of social behavior in total as well as distinct elements of these behavior, are shaped by factors derived mainly from individual, gender and species specific characteristics. We analyzed which of these factors (or all of them) affect features of mating behavior in dyadic encounters of conand heterospecific partners in two closely related forms of house mice — Mus musculus and mice from hybrid zone of Trans-Caucasia. There are two sources of the polymorphism in the gene pool of Trans-Caucasian mice: the ancient (stemmed from relict origin of the genetic pool) and evolutionarily new (derived from gene flows from differentiated taxa: M. domesticus and M. musculus). We revealed that sex is the main factor determining the level of aggression during dyadic encounters of sexual partners. It has been shown that species-specific behavioral patterns are the only factor that determines some of the main quantitative parameters of the male’s sexual behavior. These include the frequency of ejaculation and the rate of mounts with intromission, which are definitive for the successful copulation. As we have shown earlier species-specific features in the patterns of sexual behavior, which appear during encounters of heterospecific males and females belonging to the closely related taxa of house mice, may provoke the incomplete or the unsuccessful copulation. This means that differences in the main quantitative parameters of male’s mating behavior may represent (on an evolutionary scale) one of the driving forces behind the reproductive isolation of Trans-Caucasian mice of hybrid origin from M. musculus.DOI: 10.15298/rusjtheriol.19.2.05

Литература
  • Albrechtová J., Albrecht T., Baird S.J.E., Macholán M., Rudolfsen G., Munclinger P., Tucker P.K. & Piálek J. 2012. Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse // Proceedings of the Royal Society B, Biological Sciences. Vol.279. No.1748. P.4803–4810.
  • Alekperov Kh.M. 1966. [Mammals of Southwestern Azerbaijan]. Baku: Akademiya Nauk Azerbaidzhanskoi SSR. 147 p. [in Russian].
  • Alieva Sh.B. 1965. [Materials on the fauna and ecology of rodents of Nakhichevan ASSR] // Turaev D.G. (ed.). [Fauna and Ecology of Terrestrial Vertebrates of Azerbaijan]. Baku: Akademiya Nauk Azerbaidzhanskoi SSR. P.133–164 [in Russian].
  • Ambaryan A.V. & Kotenkova E.V. 2008. [A comparative analysis of sexual behavior of Mus musculus and Mus spicilegus] // Uspechi Sovremennoi Biologii. Vol.128. No.2. P.199–214 [in Russian, with English summary].
  • Ambaryan A.V., Maltzev A.N. & Kotenkova E.V. 2015. [Relationship between characteristics of sexual behavior and male sperm competitive ability in taxa of superspecies complex Mus musculus sensu lato] // Zhurnal Obshchei Biologii. Vol.76. No.3. P.212–224 [in Russian, with English summary].
  • Ambaryan A.V., Voznessenskaya V.V. & Kotenkova E.V. 2019. Mating behavior differences in monogamous and polygamous sympatric closely related species Mus musculus and Mus spicilegus and their role in behavioral precopulatory isolation // Russian Journal of Theriology. Vol.18. No.2. P.67–79.
  • Arnold M.L. 1997. Natural Hybridization and Evolution. New York: Oxford University Press. 228 p.
  • Arnold M.L. & Martin N.H. 2010. Hybrid fitness across time and habitats // Trends in Ecology & Evolution. Vol.25. No.9. P.530–536.
  • Baack E.J. & Rieseberg L.H. 2007. A genomic view of introgression and hybrid speciation // Current Opinion in Genetics & Development. Vol.17. No.6. P.513–518.
  • Bank C., Hermisson J. & Kirkpatrick M. 2011. Can reinforcement complete speciation? // Evolution. Vol.66. No.1. P.229–239.
  • Barton N.Y. 2001. The role of hybridization in evolution // Molecular Ecology. Vol.10. No.3. P.551–568.
  • Batty J. 1978a. Acute changes in plasma testosterone levels and their relation to measures of sexual behaviour in the male house mouse (Mus musculus) // Animal Behaviour. Vol.26. No.2. P.349–357.
  • Batty J. 1978b. Plasma levels of testosterone and male sexual behaviour in strains of the house mouse (Mus musculus) // Animal Behaviour. Vol.26. No.2. P.339–348.
  • Beach F.A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals // Hormones and Behavior. Vol.7. No.7. P.105–138.
  • Bímová B., Macholán M., Baird S.J.E., Munclinger P., Dufková P., Laukaitis C.M., Karn R.C., Luzynski K., Tucker P.K. & Piálek J. 2011. Reinforcement selection acting on the European house mouse hybrid zone // Molecular Ecology. Vol.20. No.11. P.2403–2424.
  • Bonhomme F., Anand R., Darviche D., Din W. & Boursot P. 1994. The mouse as a ring species? // Moriwaki K., Shiroishi T. & Yonekawa H. (eds.). Genetics in Wild Mice. Its application to Biomedical Research. Tokyo: Japan Scientific Societies Press. P.13–23.
  • Borkin L.Ya. & Litvinchuk S.N. 2013. [Hybridization, Speciation, and Systematics of Animals]. Alimov A.F. & Stepan’yants S.D. (eds.). [Current Problems of Biological Taxonomy]. Trudy Zoologicheskogo Instituta AN SSSR. Suppl. No.2. Saint Petersburg: KMK Sci Press. P.83–139 [in Russian, with English summary].
  • Boursot P., Auffray J-C., Britton-Davidian J. & Bonhomme F. 1993. The evolution of house mice // Annual Review of Ecology, Evolution, and Systematics. Vol.24. P.119–152.
  • Britton-Davidian J., Fel-Clair F., Lopez J., Alibert P. & Boursot P. 2005. Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids // Biological Journal of the Linnean Society. Vol.84. No.3. P.379–393.
  • Canastar A. & Maxson S.C. 2003. Sexual aggression in mice: effects of male strain and of female estrous state // Behavior Genetics. Vol.33. No.5. P.521–528.
  • Comeault A.A. & Matute D.R. 2018. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation // Proceedings of the National Academy of Sciences of USA. Vol.115. No.39. P.9761–9766.
  • Crowcroft P. 1955. Social organization in wild mouse colonies // British Journal of Animal Behaviour. Vol.3. No.1. P.1–36.
  • Cucchi T., Kovács Z., Berthon R., Orth A., Bonhomme F., Evin A., Siahsarvie R., Darvish J., Bakhshaliyev V. & Marro C. 2013. On the trail of Neolithic mice and men towards Transcaucasia: zooarchaeological clues from Nakhchivan (Azerbaijan) // Biological Journal of the Linnean Society. Vol.108. No.4. P.917–928.
  • Dewsbury D.A., Oglesby J.M., Sandra L., Shea S.L., James L. & Connor J.L. 1979. Inbreeding and copulatory behavior in house mice: a further consideration // Behavior Genetics. Vol.9. No.3. P.151–163.
  • Dobson F.S. & Baudoin C. 2002. Experimental tests of spatial association and kinship in monogamous mice (Mus spicilegus) and polygamous mice (Mus musculus domesticus) // Canadian Journal of Zoology. Vol.80. No.6. P.980–986.
  • Eigelis Yu.K. 1980. [Rodents of Eastern Trans-Caucasia and the Problem of Rehabilitation of Local Foci of Plague]. Saratov: Saratov University Press. 262 p. [in Russian].
  • Estep D.Q., Lanier D.L. & Dewsbury D.A. 1975. Copulatory behavior and nest building behavior of wild house mice (Mus musculus) // Animal Learning & Behavior. Vol.3. No.4. P.329−336.
  • Feliner G.N., Alvarez I., Fuertes-Aguilar J., Heuertz M., Marques I., Moharrek F., Pineiro R., Riina R., Rossello J.A., Soltis P.S. & Villa-Machío I. 2017. Is homoploid hybrid speciation that rare? An empiricist’s view // Heredity. Vol.118. No.6. P.513–516.
  • Firman R.C. & Simmons L.W. 2009. Experimental evolution of sperm quality via postcopulatory sexual selection in house mice // Evolution. Vol.64. No.5. P.1245–1256.
  • Firman R.C., Garcia-Gonzalez F., Thyer E., Wheeler S., Yamin Z., Yuan M. & Simmons L.W. 2015. Evolutionary changes in testes tissue composition among experimental populations of house mice // Evolution. Vol.69. No.3. P.848–855.
  • Forejt J. & Ivanyi P. 1974. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.) // Genetics Research. Vol.24. No.2. P.189–206.
  • Frisman L.V., Korobitsina K.V., Yakimenko L.V., Bokshtein F.M. & Muntyanu A.I. 1990. Genetic differentiation of the U.S.S.R. house mice: electrophoretic study of proteins // Biological Journal of the Linnean Society. Vol.41. No.1–3. P.65–72.
  • Good J.M., Handel M.A. & Nachman M.W. 2008. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice // Evolution. Vol.62. No.1. P.50–65.
  • Hewitt G.M. 2001. Speciation, hybrid zones and phylogeography — or seeing genes in space and time // Molecular Ecology. Vol.10. No.3. P.537–549.
  • Jaenike J., Dyer K.A., Cornish C. & Minhas M.S. 2006. Asymmetrical reinforcement and Wolbachia infection in Drosophila // PLoS Biology. Vol.4. No.10. P.1852–1862.
  • Kotenkova E.V. & Munteanu A.I. 2006. [A comparative analysis of the spatial-ethological population structure of different species of house mice related to their mode of life] // Uspekhi Sovremennoi Biologii. Vol.126. No.5. P.513–528 [in Russian, with English summary].
  • Kotenkova E.V. & Naidenko S.V. 1999. Discrimination of conand heterospecific odors in different taxa of the Mus musculus species group: olfactory cues as precopulatory isolating mechanism // Johnston R.E., Muller-Schwarze D. & Sorensen P. (eds.). Advances in Chemical Communication in Vertebrates. New York: Plenum Press. P.299–308.
  • Kotenkova E.V., Mal’tsev A.N. & Ambaryan A.V. 2018. Experimental analysis of the reproductive potential of house mice (Mus musculus sensu lato, Rodentia, Muridae) in Transcaucasia and other regions // Biology Bulletin. Vol.45. No.8. P.884–897.
  • Kotenkova E.V., Osadchuck A.V. & Lyalyukhina S.I. 1989b. Precopulatory isolating mechanisms between the house and mound-building mouse // Acta Theriologica. Vol.34. No.22. P.315–324.
  • Kotenkova E.V., Osipova O.V. & Lyalyukhina S.I. 1989a. [Behavioral elements and seasonal changes of behavior in mound-building mice (Mus hortulanus Nordm.)] // Sokolov V.E., Kotenkova E.V., Krasnov B.R. & Meshkova N.N. (eds.). The House Mouse. Moscow: Institute of Evolutionary Animal Morphology and Ecology Press. P.256–272 [in Russian, with English summary].
  • Kotenkova E., Romachenko A., Ambaryan A. & Maltsev A. 2019. Effect of early experience on neuronal and behavioral responses to conand heterospecific odors in closely related Mus taxa: epigenetic contribution in formation of precopulatory isolation // BMC Evolutionary Biology. Vol.19. P.51.
  • Latour Y. & Ganem G. 2017. Does competitive interaction drive species recognition in a house mouse secondary contact zone? // Behavioral Ecology. Vol.28. No.1. P.212–221.
  • Latour Y., Perriat-Sanguinet M., Caminade P., Boursot P., Smadja C.M. & Ganem G. 2013. Sexual selection against natural hybrids may contribute to reinforcement in a house mouse hybrid zone // Proceedings of the Royal Society B, Biological Sciences. Vol.281. No.1776. e.20132733.
  • Levenets J.V., Panteleeva S.N., Reznikova Zh.I., Gureeva A.V., Feoktistova N.Y. & Surov A.V. 2019. Experimental comparative analysis of hunting behavior of four species of Cricetinae hamsters // Zoologicheskii Zhurnal. Vol.98. No.6. P.673–683 [in Russian, with English summary].
  • Mackintosh J.H. 1981. Behaviour of house mouse // Symposia of the Zoological Society of London. Vol.47. P.337–365. Mallet J. 2007. Hybrid speciation // Nature. Vol.446. No.7133. P.279–283.
  • Maltsev A.N., Ambaryan A.V., Bazhenov U.A. & Kotenkova E.V. 2016. Experimental hybridization and an evaluation of the fertility of some forms of the house mouse supraspecies complex Mus musculus (Rodentia, Muridae) // Biology Bulletin. Vol.43. No.7. P.747–757.
  • Maltsev A.N., Stakheev V.V., Bogdanov A.S., Fomina E.S. & Kotenkova E.V. 2015. Phylogenetic relationships of intraspecific forms of the house mouse Mus musculus: Analysis of variability of the control region (D-loop) of mitochondrial DNA// Doklady Biological Sciences. Vol.465. No.3. P.285–288.
  • Mavárez J. & Linares M. 2008. Homoploid hybrid speciation in animals // Molecular Ecology. Vol.17. No.19. P.4181–4185. McGill T.E. 1962. Sexual behavior in three inbred strains of mice // Behaviour. Vol.19. No.4. P.341–350.
  • Mezhzherin S.V. & Kotenkova E.V. 1989. [Genetic marking of the house mouse subspecies of the USSR fauna] // Doklady Akademii Nauk SSSR. Vol.304. No.5. P.1271–1275 [in Russian].
  • Mezhzherin S.V., Kotenkova E.V. & Mikhailenko A.G. 1998. The house mice, Mus musculus s. l., hybrid zone of Trans-Caucasus // Zeitschrift für Säugetierkunde. Bd.63. Hf.2. S.154–168.
  • Mihola O., Trachtulec Z., Vlcek C., Schimenti J.C. & Forejt J. 2009. A mouse speciation gene encodes a meiotic histone h3 methyltransferase // Science. Vol.323. No.5912. P.373–375.
  • Milishnikov A.N. 2004. Differentiation between the ancestral and evolutionarily new polymorphism in populations of the superspecies complex of house mice Mus musculus sensu lato // Doklady Biological Sciences. Vol.397. No.2. P.317–320.
  • Milishnikov A.N., Lavrenchenko L.A. & Lebedev V.S. 2004. Origin of the house mice (superspecies complex Mus musculus sensu lato) from the Transcaucasia region: a new look at dispersal routes and evolution // Russian Journal of Genetics. Vol.40. No.9. P.1011–1026.
  • Milishnikov A.N., Rafiev A.N., Lavrenchenko L.A. & Orlov V.N. 1990. High level of introgression of Mus domesticus genes in a Transcaucasian population of Mus musculus s. str. // Doklady Biological Sciences. Vol.311. No.3. P.279–282.
  • Mosig D.W. & Dewsbury D.A. 1976. Studies of the copulatory behavior of house mice (Mus musculus) // Behavioral Biology. Vol.16. No.4. P.463–473.
  • Nelson J.F., Felicio L.S., Randall P.K., Sims C. & Finch C.E. 1982. A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology // Biology of Reproduction. Vol.27. No.2. P.327–339.
  • Niel L. & Monks D.A. 2013. Mouse sex: sexual differentiation and sexual behavior in Mus musculus // Crusio W.E., Sluyter F., Gerlai R.T. & Pietropaolo S. (eds.). Behavioral Genetics of the Mouse. Vol.1. Genetics of Behavioral Phenotypes. Cambridge: Cambridge University Press. P.218–229.
  • Nosil P., Crespi B.J., Gries R. & Gries G. 2007. Natural selection and divergence in mate preference during speciation // Genetica. Vol.128. No.3. P.309–327.
  • Orth A., Lyapunova E., Kandaurov A., Boissinot S., Boursot P., Vorontsov N. & Bonhomme F. 1996. L’espèce polytypique Mus musculus en Transcaucasie // Comptes Rendus de l’Académie des Sciences. Series III. Sciences de la Vie. Vol.319. No.5. P.435–441.
  • Panteleeva S.N., Levenets J.V., Novikovskaya A.A., Reznikova Zh.I., Lopatina N.V. & Litvinov Yu.N. 2020. Experimental investigation of the hunting behavior in mountain voles Alticola strelzowi and Alticola tuvinicus (Rodentia, Cricetidae) // Zoologicheskii Zhurnal. Vol.99. No.1. P.113–120 [in Russian, with English summary].
  • Park J.H. 2011. Assessment of male sexual behavior in mice // Todd D.G. (ed.). Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests. Vol.2. New York: Humana Press. P.357–373.
  • Patris B., Gouat P., Jacquot C., Christophe N. & Baudoin C. 2002. Agonistic and sociable behaviors in the mound-building mouse, Mus spicilegus, a comparative study with Mus musculus domesticus // Aggressive Behavior. Vol.28. No.1. P.75–84.
  • Poteaux C., Busquet N., Gouat P., Katona K. & Baudoin C. 2008. Socio-genetic structure of mound-building mice, Mus spicilegus, in autumn and early spring // Biological Journal of the Linnean Society. Vol.93. No.4. P.689–699.
  • Rieseberg L.H. 1997. Hybrid origins of plant species // Annual Review of Ecology, Evolution, and Systematics. Vol.28. P.359–389.
  • Sage R.D., Atchley W.R. & Capanna E. 1993. House mice as models in systematic biology // Systematic Biology. Vol.42. No.4. P.523–561.
  • Schulte U., Veith M. & Hochkirch A. 2012. Rapid genetic assimilation of native wall lizard populations (Podarcis muralis) through extensive hybridization with introduced lineages // Molecular Ecology. Vol.21. No.17. P.4313–4326.
  • Schumer M., Rosenthal G.G. & Andolfatto P. 2014. How common is homoploid hybrid speciation? // Evolution. Vol.68. No.6. P.1553–1560.
  • Schumer M., Rosenthal G.G. & Andolfatto P. 2018. What do we mean when we talk about hybrid speciation? // Heredity. Vol.120. No.4. P.379–382.
  • Smadja C. & Ganem G. 2005. Asymmetrical reproductive character displacement in the house mouse // Journal of Evolutionary Biology. Vol.18. No.6. P.1485–1493.
  • Stopka P. & Macdonald D.W. 1998. Signal interchange during mating in the wood mouse Apodemus sylvaticus: The concept of active and passive signaling // Behaviour. Vol.135. No.2. P.231–249.
  • Stopka P. & Macdonald D.W. 1999. The market effect in the wood mouse Apodemus slvaticus: Selling information on reproductive status // Ethology. Vol.105. No.11. P.969–982.
  • Suzuki T.A. & Nachman M.W. 2015. Speciation and reduced hybrid female fertility in house mice // Evolution. Vol.69. No.9. 2468–2481.
  • Tembotov A.K. & Shkhashamiev Kh.K. 1984. [The Fauna of Kabardino-Balkaria]. Nalchik: Elbrus. 192 p. [in Russian]. Turner L.M., Schwahn D.J. & Harr B. 2012. Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone // Evolution. Vol.66. No.2. P.443–458.
  • Uy J.A.C., Irwin D.E. & Webster M.S. 2018. Behavioral isolation and incipient speciation in birds // Annual Review of Ecology, Evolution, and Systematics. Vol.49. P.1–24.
  • Walkowa W., Kotenkova E., Adamczyk K. & Barkowska M. 1998. Behavior of house mice in semi-natural conditions: influence of spatial separation and population size // Acta Theriologica. Vol.43. No.3. P.241–254.
  • White M.A., Steffy B., Wiltshire T. & Payseur B.A. 2011. Genetic dissection of a key reproductive barrier between nascent species of house mice, Mus musculus domesticus and Mus musculus musculus // Genetics. Vol.189. No.1. P.289–304.
  • Wolf R.J. 1985. Mating behaviour and female choice: their relation to social structure in wild caught house mice (Mus musculus) housed in semi-natural environment // Journal of Zoology. Vol.207. No.1. P.43–51.
  • Zorenko T. 2013. [Social Voles of the Subgenus Sumeriomys: Systematics, Biology and Behaviour] Saarbrücken: Palmariun Academic Publishing. 548 p. [in Russian].