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Mating behavior differences in monogamous and polygamous sympatric closely related species Mus musculus and Mus spicilegus and their role in behavioral precopulatory isolation
Ambaryan A.V., Voznessenskaya V.V., Kotenkova E.V.
P. 67–79
Closely related species with different mating system may be the most suitable model taxa for studies aimed to highlight the cause formation of species-specific peculiarities of sexual behavior and behavioral mechanisms of precopulatory isolation. The current study aimed to clarify the role of the mating system and lifestyle, including ecology features, in patterning of behavioral activities during mating, as well as the role of behavioral patterns in the precopulatory isolation of closely related Mus taxa. Test subjects were closely related sympatric species: polygynous/promiscuous M. musculus and presumably monogamous M. spicilegus, reproductively isolated in nature. Dyadic encounters of male and receptive female were conducted in clear chambers and the behavior was recorded by means of video camera. Sexual behavior, culminating in ejaculation, was observed in conspecific dyadic encounters only; it occurred more frequently and with longer duration in males of M. spicilegus, than in males of M. musculus. In conspecific encounters, males of M. spicilegus exhibited a higher level of affiliative behavior than females. In both species total frequency and duration of aggressive behavior was higher in females compared to males. In heterospecific dyadic encounters the behavioral pattern of males and females was strictly different from those in conspecific encounters, and the elements of aggressive behavior prevailed. We demonstrated that not only the pattern of sexual behavior is important for reproductive isolation, but also all types of behavioral interactions preceded copulation. In Mus species different stereotypes of mating behavior during the encounter of potential sexual partners can prevent successful copulation and may be associated with mating system.

DOI: 10.15298/rusjtheriol.18.2.01

References

  • Abeelen J.H., van. 1966. Effects of genotype on mouse behavior // Animal Behaviour. Vol.14. No.2. P.218−225.
  • Ambaryan A.B., 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].
  • Bardet J., Essen D.K., Feron C. & Gouat P.2007. Evaluation of the social bond: a new method tested in Mus spicilegus // Comptes Rendus Biologies. Vol.330. No.11. P.837–844.
  • Baudoin C., Busquet N., Dobson F.S., Cheusi G., Feron Ch., Durand J-L., Heth G., Patris B. & Todrank J. 2005. Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus // Biological Journal of the Linnean Society. Vol.84. No.3. P.323−334.
  • Beach F.A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals // Hormones and Behavior. Vol.7. No.1. P.105–138.
  • Bronson F.H. 1979. The reproductive ecology of the house mouse // The Quarterly Review of Biology. Vol.54. No.3. P.265–299.
  • Brotherton P.N.M. & Komers P.E. 2003. Mate guarding and the evolution of social monogamy in mammals // Reichard U.H. & Boesch C. (eds.). Monogamy: Mating Strategies and Partnerships in Birds, Humans and Other Mammals. Cambridge: Cambridge University Press. P.42–58.
  • Bulatova N.Sh., Kotenkova E.V. & Lyalyukhina S.I. 1986. [Fertility of hybrids and cytogenetic effect of hybrid dysgenesis in crossing in the mound-building mouse and laboratory mice] // Doklady Academii Nauk SSSR. Vol.288. No.4. P.1018–1020 [in Russian, with English summary].
  • Carlsen M. 1993. Migrations of Mus musculus musculus in Danish farmland // Zeitschrift fur Saugetierkunde. Vol.58. No.3. P.172–180.
  • Carter S., Vries C. & Getz L. 1995. Physiological substrates of mammalian monogamy: the prairie vole model // Neuroscience & Biobehavioral Reviews. Vol.19. No.2. P.303–314.
  • Carter C.S., Whitt M.D., Thompson G. & Carlstead K. 1988. Effects of hormonal, sexual, and social history on mating and pair bonding in prairie voles // Physiology and Behavior. Vol.44. No.6. P.691−697.
  • Chatterjee S. & Singh B.N. 1989. Sexual isolation in Drosophila // Indian Review of Life Science. Vol.9. P.101–135.
  • Chevret P., Veyrunes F. & Britton-Davidian J. 2005. Molecular phylogeny of the genus Mus (Rodentia: Murinae) based on mitochondrial and nuclear data // Biological Journal of the Linnean Society. Vol.84. No.3. P.417–427.
  • Clutton-Brock T.H., Guinness F.E. & Albon S.D. 1982. Red Deer: Behavior and Ecology of Two Sexes. Edinburgh: Edinburgh University Press. 378 p.
  • Clutton-Brock T.H. & Isvaran K. 2006. Paternity loss in contrasting mammalian societies // Biological Letters. Vol.2. No.4. P.513–516.
  • Crowcroft P.1954. Mouse research in Suffolk // Transactions of the Suffolk Natural Society. Vol.8. P.185–187.
  • Crowcroft P.1955. Social organization in wild mouse colonies // The British Journal of Animal Behaviour. Vol.3. No.1. P.1−36.
  • Crowcroft P.& Rowe F.P. 1963. Social organization and territorial behavior in the wild house mouse (Mus musculus L.) // Proceedings of the Zoological Society of London. Vol.140. No.3. P.517–531.
  • Davis D.E. 1958. The role of density in aggressive behaviour in house mice // Animal Behaviour. Vol.6. No.3–4. P.207–210.
  • Dewsbury D.A. 1981. On the function of the multiple-intromission, multiple-ejaculation copulatory patterns of rodents // Bulletin of the Psychonomic Society. Vol.18. No.4. P.221–223.
  • Dewsbury D.A. 1987. The comparative psychology of monogamy // Leger D.W. (ed.). Comparative Perspectives in Modern Psychology. Nebraska Symposium on Motivation. Vol.35. Nebraska: Nebraska University Press. P.1–50.
  • 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.
  • Dixon A.F. 2012. Primate Sexuality. Comparative Studies of the Prosimians, Monkeys, Apes and Humans. New York: Oxford Academic Press. 742 p.
  • Dobson F.S. & Baudoin C. 2002. Experimental tests of spatial association and kinship in monogamous mice (Mus spicilegus) and polygynous mice (Mus musculus domesticus) // Canadian Journal of Zoology. Vol.80. No.6. P.980–986.
  • Dobson F.S., Way B.M. & Baudoin C. 2010. Spatial dynamics and the evolution of social monogamy in mammals // Behavioral Ecology. Vol.21. No.4. P.747–752.
  • Emlen S.T. & Oring L.W. 1977. Ecology, sexual selection, and the evolution of mating systems // Science. Vol.197. No.4300. P.215–223.
  • Estep D.Q., Lanier D.L. & Dewsbury D.A. 1975. Copulatory behavior and nest building behavior of wild house mice (Mus musculus) // Animal Learning and Behavior. Vol.3. No.4. P.329–336.
  • Feron C. & Gouat P.2007. Paternal care in the mound-building mouse reduces inter-litter intervals // Reproduction, Fertility and Development. Vol.19. No.3. P.425–429.
  • Fitzgerald R.W. & Madison D.M. 1983. Social organization of a free-ranging population of pine voles, Microtus pinetorum // Behavioral Ecology and Sociobiology. Vol.13. No.3. P.183–187.
  • Frynta D., Slábová M. & Vohralík V. 2009. Why do male house mice have such small testes? // Zoological Science. Vol.26. No.1. P.17–23.
  • Frynta D., Volfová R., Franková-Nováková M. & Stejskal 2010. Oestrous females investigate the unfamiliar male more than the familiar male in both commensal and non-commensal populations of house mice // Behavioural Processes. Vol.83. No.1. P.54–60.
  • Getz L.L., Hofmann J.E. & Carter C.S. 1987. Mating system and population fluctuations of the prairie vole, Microtus ochrogaster // American Zoologist. Vol.27. No.3. P.909–920.
  • Gouat P.& Feron C. 2005. Deficit in reproduction in polygynously mated females of the monogamous mound-building mouse Mus spicilegus // Reproduction, Fertility and Development. Vol.17. No.6. P.617–623.
  • Gouat P., Katona K. & Poteaux C. 2003. Is the socio-spatial distribution of mound-building mice, Mus spicilegus, compatible with a monogamous mating system? // Mammalia. Vol.67. No.1. P.15–24.
  • Grant E.C. & Mackintosh I.H. 1963. A comparison of social posture of some common laboratory rodents // Behavior. Vol.21. No.3–4. P.246−259.
  • Hamar M. & Sutova-Hamar M. 1969. Estimation of rodent home ranges in different agrosystems // Energy Flow Through Small Mammal Population. Proceedings of IBP Meeting on Secondary Productivity in Small Mammal Populations. Oxford. P.99–109.
  • Harcourt A.H., Harvey P.H., Larson S.G. & Short R.V. 1981. Testis weight, body weight and breeding system in primates // Nature. Vol.293. No.5827. P.55–57.
  • Harvey P.H. & Harcourt A.H. 1984. Sperm competition, testes size, and breeding systems in primates // Smith R.L. (ed.). Sperm Competition and the Evolution of Animal Mating Systems. New York: Academic Press. P.589–600.
  • Heske E.J. & Ostfeld R.S. 1990. Sexual dimorphism in size, relative size of testes, and mating systems in North American voles // Journal of Mammalogy. Vol.71. No.4. P.510–519. Hurst J.L. 1986. Mating in free-living wild house mice (Mus domesticus) // Journal of Zoology. Vol.210. No.4. P.623–628.
  • Johnson Z. & Young L.J. 2015. Neurobiological mechanisms of social attachment and pair bonding // Current Opinion in Behavioral Sciences. Vol.3. P.38–44.
  • Iossa G., Soulsbury C.D., Baker P.J. & Harris S. 2008. Sperm competition and the evolution of testes size in terrestrial mammalian carnivores // Functional Ecology. Vol.22. No.4. P.655–662.
  • Isvaran K. & Clutton-Brock T. 2007. Ecological correlates of extra-group paternity in mammals // Proceedings of the Royal Society of London, B. Vol.274. No.1607. P.219–224. Kenagy G.J. & Trombulak S.C. 1986. Size and function of mammalian testes in relation to body size // Journal of Mammalogy. Vol.67. No.1. P.1–22.
  • Kotenkova E.V. 2014. A comparative analysis of ethological and physiological mechanisms of precopulatory isolation // Biology Bulletin Reviews. Vol.134. No.5. P.488–518.
  • 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., 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. P.256−272 [in Russian, with English summary]
  • 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.
  • Krasnov B.R. & Chochlova J.S. 1994. [Spatial ethological structure of groups] // Kotenkova E.V. & Bulatova N.Sh. (eds.). [The House Mouse: Origin, Distribution, Systematics, Behaviour]. Moscow: Nauka. P.188–214 [in Russian].
  • Laconi M.R. & Castro-Vázquez A. 1998. Aggressive interactions during mating encounters in the corn mouse, Calomys musculinus (Muridae, Sigmodontinae) // Mastozoología Neotropical. Vol.5. No.1. P.21–28.
  • Levine L., Barsel G.E. & Diakow G.A. 1966. Mating behavior of two inbred strains of mice // Animal Behaviour. Vol.14. No.1. P.1–6.
  • Lidicker W.L. 1976. Social behavior and density regulation in house mice living in large enclosure // Journal of Animal Ecology. Vol.45. No.3. P.677–697.
  • Lieberwirth C. & Wang Z. 2016. The neurobiology of pair bond formation, bond disruption, and social buffering // Current Opinion in Neurobiology. Vol.40. P.8–13.
  • Lloyd I.A. 1975. Social structure and reproduction in two free-growing populations in house mice (Mus musculus) // Animal Behaviour. Vol.23. No.2. P.413–424.
  • Mackintosh J.H. 1981. Behaviour of house mouse // Symposia of the Zoological Society of London. Vol.47. P.337–365.
  • Mangels R., Tsung K., Kwan K. & Dean M.D. 2016. Copulatory plugs inhibit the reproductive success of rival males // Journal of Evolutionary Biology. Vol.29. No.11. P.2289–2296.
  • Manno T.G. & Dobson F.S. 2008. Why are male Columbian ground squirrel’s territorial? // Ethology. Vol.114. No.11. P.1049–1060.
  • Manno T.G., Nesterova A.P., Debarbieri L.M., Kennedy S.E., Wright K.S. & Dobson F.S. 2007. Why do male Columbian ground squirrels give a mating call? // Animal Behaviour. Vol.74. No.5. P.1319–1327.
  • McGill Т.Е. 1962. Sexual behavior in three inbred strains of mice // Behaviour. Vol.19. No.4. P.341–350.
  • McGill Т.Е. & Ranson T.W. 1968. Genotypic change affecting conclusions regarding the mode of inheritance of elements of behavior // Animal Behaviour. Vol.16. No.1. P.88–91.
  • Mezhzherin S.V. 1994. [Taxonomy and modern views on the system of Palaearctic house mice] // Kotenkova E.V. & Bulatova N.Sh. (eds.). [The House Mouse: Origin, Distribution, Systematics, Behaviour]. Moscow: Nauka. P.15–36 [in Russian].
  • Montoto L.G., Magana C., Tourmente M., Martin-Coello J., Crespo C., Luque-Larena J.J., Gomendio M. & Roldan E.R.S. 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents // PLoS ONE. Vol.6. No.3. e18173.
  • 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.
  • Naumov N.P. 1940. [Ecology of mound-building mouse Mus musculus hortulanus Nordm.] // Trudy Instituta Evolutsionnoi Morfologii Akademii Nauk SSSR. Vol.3. P.33–76 [in Russian, with English summary].
  • 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.327–39.
  • Noordwijk M.A., van & Schaik C.P., van. 2004. Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions // Kappeler P.M. & Schaik C.M., van. (eds.). Sexual Selection in Primates: New and Comparative Perspectives. Cambridge: Cambridge University Press. P.208–221.
  • Patris B. & Baudoin C. 1998. Female sexual preferences in Mus spicilegus and Mus musculus domesticus: the role of familiarization and sexual experience // Animal Behaviour. Vol.56. No.6. P.1465–1470.
  • Patris B. & Baudoin C. 2000. A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus // Behavioural Processes. Vol.51. No.1–3. P.35–43.
  • 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.
  • Pelikán J. 1981. Patterns of reproduction in the house mouse // Symposia of the Zoological Society of London. Vol.47. P.205–229.
  • Pisareva M.E. 1948. [Ecology and systematic of mound-building mouse] // Sbornik Rabot Biologicheskogo Fakulteta Dnepropetrovskogo Gosudarstvennogo Universiteta: Uchenye Zapiski. Vol.32. P.68–71 [in Russian].
  • Pitcher T.E., Dunn P.O. & Whittingham L.A. 2005. Sperm competition and the evolution of testes size in birds // Journal of Evolutionary Biology. Vol.18. No.3. P.557–567.
  • Kenagy G.J. & Trombulak S.C. 1986. Size and function of mammalian testes in relation to body size // Journal of Mammalogy. Vol.67. No.1. P.1–22.

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