No asymmetry in the level of incest avoidance between mother–son and father–daughter pairs in the mandarin vole (Lasiopodomys mandarinus) (Rodentia: Arvicolinae)

Naumova A.E., Smorkatcheva A.V., Sablina S.A.

P. 120-125

Animals of most species avoid close inbreeding, but the levels of incest avoidance (IA) vary both between and within species. Evolutionary reasons for this diversity are generally unclear. Comparison of IA between closely-related species and between within species categories (sexes, age classes or categories of kin pairs) could provide important tools to test hypotheses on the evolution of IA strategies. In this laboratory study we compared the likelihood of reproduction between mother–son and father–daughter pairs in a monogamous subterranean vole, Lasiopodomys mandarinus. The subterranean lifestyle is associated with impeded mates’ encounters, costly dispersal, and relatively low value of each breeding attempt, which factors are expected to restrain the IA evolution. In polygynous uniparental animals, the predominance of father–daughter inbreeding over mother–son inbreeding is predicted. We aimed to test whether L. mandarinus, which exhibits a partial reversal of sex roles, displays an opposite pattern of asymmetry with a weakened IA between a mother and a son. Against the expectation, reproductive performance was dramatically reduced in both kin combinations. Mandarin vole’s IA strategies follow the pattern typical for non-subterranean species with strong pair bonding, supporting the importance of mating system for IA evolution.DOI: 10.15298/rusjtheriol.22.2.04

• Batzli G.O., Getz L.L. & Hurley S.S. 1977. Suppression of growth and reproduction of Microtine rodents by social factors // Journal of Mammalogy. Vol.58. No.4. P.583–591.
• Berger P.J., Negus N.C. & Day M. 1997. Recognition of kin and avoidance of inbreeding in the Montane Vole, Microtus montanus // Journal of Mammalogy. Vol.78. No.4. P.1182–1186.
• Bixler A. & Tang-Martinez Z. 2006. Reproductive performance as a function of inbreeding in prairie voles (Microtus ochrogaster) // Journal of Mammalogy. Vol.87. No.5. P.944–949.
• Bollinger E.K., Harper S.J., Kramer J.M. & Barrett G.W. 1991. Avoidance of inbreeding in the meadow vole (Microtus pennsylvanicus) // Journal of Mammalogy. Vol.72. No.2. P. 419–421.
• Bondareva O., Genelt-Yanovskiy E., Petrova T., Bodrov S., Smorkatcheva A. & Abramson N. 2021. Signatures of adaptation in mitochondrial genomes of Palearctic subterranean voles (Arvicolinae, Rodentia) // Genes. Vol.12. No.12. P.e1945.
• Boyd S. K. & Blaustein A. R. 1985. Familiarity and inbreeding avoidance in the gray-tailed vole (Microtus canicaudus)// Journal of Mammalogy. Vol.66. No.2. P.348–352.
• Burda H. 1995. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents // Experientia. Vol.51. P.411–413.
• Burda H. 1999. Syndrome of eusociality in African subterranean mole-rats (Bathyergidae, Rodentia), its diagnosis and aetiology // Wasser S.P. (ed.). Evolutionary Theory and Processes: Modern Perspectives. NL-Dordrecht: Kluwer Academic Publ. P.385–418.
• Burda H. 2007. From natural histories to life histories // Begall S.H., Burda H. & Schleich C.E. (eds.). Subterranean Rodents: News from Underground. Berlin, Heidelberg: Springer. P.197–203.
• Davydov G.S. 1988. [Fauna of Tadzhikskaya SSR. Mammals (Rodents)]. Dushanbe: Donish. 313 p. [in Russian].
• de Boer R.A., Vega-Trejo R., Kotrschal A. & Fitzpatrick J.L. 2021. Meta-analytic evidence that animals rarely avoid inbreeding // Nature Ecology and Evolution. Vol.5. No.7. P.949–964.
• Dmitriev P.P. 1980. [The ecology of the Chinese vole (Microtus mandarinus) and its role in the pasture biocenoses of northern Mongolia] // Zoologicheskii Zhurnal. Vol.59. No.18. P.1852–1861 [in Russian].
• Dos Santos E.M., Andreassen H.P. & Ims R.A. 1995. Differential inbreeding tolerance in two geographically distinct strains of root voles Microtus oeconomus // Ecography. Vol.18. No.3. P.238–247.
• Duthie A.B. & Reid J.M. 2015. What happens after inbreeding avoidance? Inbreeding by rejected relatives and the inclusive fitness benefit of inbreeding avoidance // PLoS ONE. Vol.10. No.4. P.e0125140.
• Dymskaya M.M., Volodin I.A., Smorkatcheva A.V., Vasilieva N.A. & Volodina E.V. 2022. Audible, but not ultrasonic, calls reflect surface-dwelling or subterranean specialization in pup and adult Brandt’s and mandarin voles // Behavioral Ecology and Sociobiology. Vol.76. No.7. DOI:10.1007/s00265-022-03213-6.
• Evdokimov N.G. 2001. [Population ecology of the Northern mole vole]. Yekaterinburg: Institute of Ecology of Plants and Animals, Ural Branch, RAS. 144 p. [in Russian].
• Facemire C.F. & Batzli G.O. 1983. Suppression of growth and reproduction by social factors in microtine rodents: tests of two hypotheses // Journal of Mammalogy. Vol.64. No.1. P.152–156.
• Galezo A.A., Nolas M.A., Fogel A.S., Mututua R.S., Warutere J.K., Long’ida Siodi I., Altmann J., Archie E.A., Tung J. & Alberts S.C. 2022. Mechanisms of inbreeding avoidance in a wild primate // Current Biology. Vol.32. P.1607–1615.
• Gavish L., Hofmann J.E. & Getz L.L. 1984. Siblings recognition in the prairie vole, Microtus ochrogaster // Animal Behaviour. Vol.32. P.362–366.
• Getz L.L. & Carter C.S. 1998. Inbreeding avoidance in the prairie vole, Microtus ochrogaster // Ethology Ecology & Evolution. Vol.10. P.115–120.
• Greenwood P.J., Harvey P.H. & Perrins C.M. 1978. Inbreeding and dispersal in the great tit // Nature. Vol.271. P.52–54.
• Haig D. 1999. Asymmetric relations: internal conflicts and the horror of incest // Evolution and Human Behavior. Vol.20. P.83–98.
• Hatchwell B.J. 2010. Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation // Ethology. Vol.116. P.203–216.
• Ialongo C. 2016. Understanding the effect size and its measures // Biochemia Medica. Vol.26. No.2. P.150–163.
• Kokko H. & Ots I. 2006. When not to avoid inbreeding // Evolution. Vol.60. No.3. P.467–475.
• Kruczek M. 2007. Recognition of kin in bank voles (Clethrionomys glareolus) // Physiology & Behavior. Vol.90. P.483–489.
• Lemaître J.F., Ramm S.A., Hurst J.L. & Stockley P. 2012. Inbreeding avoidance behaviour of male bank voles in relation to social status // Animal Behaviour. Vol.83. No.2. P.453–457.
• Liu X.H., Yue L.F., Wang D.W., Li N. & Cong L. 2013. Inbreeding avoidance drives consistent variation of fine-scale genetic structure caused by dispersal in the seasonal mating system of Brandt’s voles // PLoS ONE. Vol.8. No.3. P.e58101.
• Lucia K. E. & Keane B. 2012. A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles // Behavioral Ecology and Sociobiology. Vol.66. P.13–27.
• Mcguire M.R. & Getz L.L. 1981. Incest taboo between sibling Microtus ochrogaster // Journal of Mammalogy. Vol.62. No.1. P.213–215.
• Nevo E. 1979. Adaptive convergence and divergence of subterranean mammals // Annual Review of Ecology and Systematics. Vol.10. P.269–308.
• Parker G.A. 2006. Sexual conflict over mating and fertilization: an overview // Philosophical Transactions of the Royal Society B: Biological Sciences. Vol.361. No.1466. P.235–259.
• Pillay N. & Rymer T.L. 2017. Preference for outbreeding in inbred Littledale’s whistling rats, Parotomys littledalei // Evolutionary Biology. Vol.44. No.1. P.21–30.
• Pusey A.E. 1987. Sex-biased dispersal and inbreeding avoidance in birds and mammals // Trends in Ecology & Evolution. Vol.2. No.10. P.295–299.
• Schadler M.H. 1983. Male siblings inhibit reproductive activity in female pine voles, Microtus pinetorum // Biology of Reproduction. Vol.28. P.1137–1139.
• Smorkatcheva A.V. 1998. [The biology of the mandarin vole, Lasiopodomys mandarinus vinogradovi] // PhD in Biology Thesis. Saint Petersburg: Saint Petersburg State University. 18 p. [in Russian].
• Smorkatcheva A.V. 1999. The social organization of the mandarine vole, Lasiopodomys mandarinus, during the reproductive period // Zeitschrift für Säugetierkunde. Vol.64. P.344–355.
• Smorkatcheva A.V. 2001. [On the distribution and ecology of the mandarin vole, Lasiopodomys mandarinus in Buryatia] // Proceedings of the Zoological Institute RAS. Vol. 288. P.188–204 [in Russian, with English summary].
• Smorkatcheva A.V. 2003a. Parental care in the captive mandarin vole, Lasiopodomys mandarinus // Canadian Journal of Zoology. Vol.81. No.8. P.1339–1345.
• Smorkatcheva A.V. 2003b. [Sexual maturation and reproduction of young females of the mandarin vole Lasiopodomys mandarinus under keeping them in groups of different composition] // Zoologicheskii Zhurnal. Vol.81. P.991–998 [in Russian, with English summary].
• Smorkatcheva A.V., Aksenova T.G. & Zorenko T.A. 1990. [The ecology of Lasiopodomys mandarinus (Rodentia, Cricetidae) in the Transbaikal area] // Zoologicheskii Zhurnal. Vol.69. P.115–124 [in Russian, with English summary].
• Smorkatcheva A.V. 2021. Weakened inbreeding avoidance in a monogamous subterranean vole, Ellobius tancrei // Mammalian Biology. Vol.101. No.5. P.601–607.
• Smorkatcheva A.V., Bychenkova T.N. & Zavjalov E.L. 2010. Parental responsiveness negatively correlates with fecal testosterone concentration in male mandarin voles (Microtus mandarinus) // Journal of Ethology. Vol.28. No.1. P.53–60.
• Stein B.R. 2000. Morphology of subterranean rodents // Lacey E.A., Patton J.I. & Cameron G.N. (eds.). Life Underground: the Biology of Subterranean Rodents. Chicago: University of Chicago Press. P.19–61.
• Streltsov V.V. & Smorkatcheva A.V. 2021. Social regulation of female reproduction in the steppe lemming, Lagurus lagurus // Mammal Research. Vol.66. P.457–465.
• Sullivan G.M. & Feinn R. 2012. Using effect size — or why the p value is not enough // Journal of Graduate Medical Education. Vol.4. No.3. P.279–282.
• Sun H., Zhang Y., Shi Y., Li Y., Li W. & Wang Z. 2018. Evolution of the CLOCK and BMAL1 genes in a subterranean rodent species (Lasiopodomys mandarinus) // International Journal of Biological Macromolecules. Vol.109. P.932–940.
• Szulkin M., Stopher K.V., Pemberton J.M. & Reid J.M. 2013. Inbreeding avoidance, tolerance, or preference in animals? // Trends in Ecology & Evolution. Vol.28. No.4. P.205–211.
• Tai F., Wang T. & Zhao Y. 2000. Inbreeding avoidance and mate choice in the mandarin vole (Microtus mandarinus) // Canadian Journal of Zoology. Vol.78. P.2119–2125.
• Tai F., Ruyong S. & Tingzheng W. 2002. Does low fecundity reflect kin recognition and inbreeding avoidance in the mandarin vole (Microtus mandarinus)? // Canadian Journal of Zoology. Vol. 80. No.12. P.2150–2155.
• Waser P.M., Austad S.N. & Keane B. 1986. When should animals tolerate inbreeeding? // The American Naturalist. Vol.128. P.529–537.
• Wheelwright N.T., Freeman-Gallant C.R. & Mauck R.A. 2006. Asymmetrical incest avoidance in the choice of social and genetic mates // Animal Behaviour. Vol.71. No.3. P.631–639.
• Zorenko T.A., Smorkatcheva A.V. & Aksenova T.G. 1994. [Reproduction and postnatal ontogenesis of mandarin vole Lasiopodomys mandarinus (Rodentia, Arvicolinae)] // Zoologicheskii Zhurnal. Vol.73. P.120–129 [in Russian, with English summary].
• Zorenko T.A. & Kaprale L. 2003. [Inbreeding avoidance and reproductive strategy in some species of voles Arvicolinae] // Golenishchev F.N. & Nikulina N.A. (eds.). Theriologicheskie Issledovaniya. Saint Petersburg: ZIN RAS. P.124–137 [in Russian, with English summary].