Alloparental care in social muroid rodents Gromov V.S. P. 150-161 The article concerns fitness effects of alloparental care, or helping (i.e., assistance of young individuals in rearing offspring that are not their own) in social muroid rodents (Meriones unguiculatus, Microtus ochrogaster, Microtus pinetorum, Lasiopodomys mandarinus, Peromyscus polionotus, and Rhabdomys pumilio) that are characterized by a family-group lifestyle and biparental care. According to inclusive fitness theory, alloparenting may alter both direct and indirect fitness. In particular, helpers may benefit indirectly if breeders that receive assistance subsequently produce more offspring. In laboratory studies, however, neither the presence of alloparents nor greater numbers of alloparents affected litter size at weaning. The results of the experimental studies also provide little support to the hypothesis that breeders benefit directly by increasing their lifetime reproductive success. In some species, helpers may decrease the workload of breeders, but the effects of alloparenting were found to be slight and often mixed. However, there is evidence that alloparental care yields direct benefits to helpers by providing experience that allow them to become more successful parents. It seems unlikely that helping behavior evolved merely to kin selection in consistence with ‘Hamilton’s rule’. A more appropriate explanation is that helping behavior in rodents is a by-product of the evolution of sociality, i.e. the transition to a family-group lifestyle with biparental care. Extended family groups with helpers form due to delayed dispersal of offspring, and the latter may gain direct and/or indirect fitness benefits from staying within their natal groups. Alloparenting could be considered a form of cooperation due to which both breeding pairs and their older offspring being helpers may gain direct or indirect fitness benefits.
DOI: 10.15298/rusjtheriol.22.2.08References- Ågren G., Zhou Q. & Zhong W. 1989. Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China // Animal Behaviour. Vol.37. P.11–27.
- Bales K., Dietz J., Baker A., Miller K. & Tardif S.D. 2000. The effects of allocare-givers on fitness of infants and parents in callitricid primates // Folia Primatologica. Vol.7. P.27–38.
- Bales K.L., O’Herron M., Baker A.J. & Dietz J. 2001. Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia) // American Journal of Primatology. Vol.54. P.211–221.
- Brotherton P.N.M., Clutton-Brock T.H., O’Riain M.J., Gainor D., Sharpe L., Kansky R. & McIlrath G.M. 2001. Offspring food allocation by parents and helper in a cooperative mammal // Behavioral Ecology. Vol.12. P.590–599.
- Brown J.L. 1974. Alternative routes to sociality in jays. With a theory for the evolution of altruism and communal breeding // American Zoologist. Vol.14. P.63–80.
- Brown J.L. 1987. Helping and communal breeding in birds. Princeton: Princeton Univ. Press. 284 p.
- Brown J.L., Brown E.R., Brown S.D. & Dow D.D. 1982. Helpers: effects of experimental removal on reproductive success // Science. Vol.215. P.421–422.
- Carter C.S. & Getz L.L. 1985. Social and hormonal determinants of reproductive patterns in the prairie vole // Gilles R. & Balthazart J. (eds.) Neurobiology. Berlin, Heidelberg, New York: Springer. P.18–36.
- Carter C.S. & Getz L.L. 1993. Monogamy and the prairie vole // Scientific American. Vol.268. P.100–106.
- Charnov E.L. 1977. An elementary treatment of the genetical theory of kin selection // Journal of Theoretical Biology. Vol.66. P.541–550.
- Clark M.M., Desousa D., Vonk J. & Galef B.G. 1997. Parenting and potency: Alternative routes to reproductive success in male Mongolian gerbils // Animal Behaviour. Vol.54. P.635–642.
- Davies N.B., Krebs J.R. & West S.A. 2012. An introduction to behavioural ecology. 4th edn. Oxford: Blackwell Scientific. 506 p.
- Elwood R.W. 1975. Paternal and maternal behaviour in the Mongolian gerbil // Animal Behaviour. Vol.23. P.766–772.
- Elwood R.W. & Broom D.M. 1978. The influence of litter size and parental behaviour on the development of Mongolian gerbil pups // Animal Behaviour. Vol.26. P.438–454.
- Emlen S.T. 1978. The evolution of cooperative breeding in birds // Krebs J.R. & Davies N.B. (eds.) Behavioural ecology. Sunderland, MA: Sinauer. P.245–281.
- Emlen S.T. 1982. The evolution of helping. I. An ecological constraints model // American Naturalist. Vol.119. P.29–39.
- Emlen S.T. 1991. Evolution of cooperative breeding in birds and mammals // Krebs J.R. & Davies N.B. (eds.). Behavioural ecology: An evolutionary approach. London: Blackwell Scientific. P.301–335.
- Emlen S. T. & Wrege P. H. 1989. A test of alternative hypotheses for helping behavior in white-fronted bee-eaters of Kenya // Behavioral Ecology and Sociobiology. Vol.25. P.303–319.
- Emlen S.T., Reeve H.K., Sherman P.W., Wrege P.H., Ratnieks F.L.W. & Shellman-Reeve J. 1991. Adaptive versus nonadaptive explanations of behavior: the case of alloparental helping // American Naturalist. Vol.138. P.259–270.
- 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. P.183–187.
- Foltz D.W. 1981. Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus // American Naturalist. Vol.117. P.665–675.
- French J.A. 1994. Alloparents in the Mongolian gerbil: impact on long-term reproductive performance of breeders and opportunities for independent reproduction // Behavioral Ecology. Vol.5. P.273–279.
- Getz L.L. & Carter C.S. 1996. Prairie-vole partnerships // American Scientist. Vol.84. P.56–62.
- Getz L.L. & Hofmann J.E. 1986. Social organization in free-living prairie voles, Microtus ochrogaster // Behavioral Ecology and Sociobiology. Vol.18. P.275–282.
- Getz L. L., Carter C. S. & Gavish L. 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding // Behavioral Ecology and Sociobiology. Vol.8. P.189–194.
- 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. P.909–920.
- Getz L.L., McGuire B., Pizzuto T., Hofmann J.E. & Frase B. 1993. Social organization of the prairie vole (Microtus ochrogaster) // Journal of Mammalogy. Vol.74. P.44–58.
- Gromov V.S. 2009. Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behaviour of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions // Biology Bulletin. Vol.36. P.479–488.
- Gromov V.S. 2011. Biparental care, tactile stimulation, and evolution of sociality in rodents // Journal of Evolutionary Biology Research. Vol.3. P.33–43.
- Gromov V.S. 2017. The spatial-and-ethological population structure, cooperation, and the evolution of sociality in rodents // Behaviour. Vol.154. P.609–649.
- Gromov V.S. 2018. The evolution of sociality in rodents: Environments and selective forces promoting grouping. LAP LAMBERT Academic Publishing, 163 pp.
- Gromov V.S. 2020. Epigenetic programming of phenotypic differences in behaviour and the evolution of sociality in rodents // Biology Bulletin Reviews. Vol.10. No.4. P.338–350.
- Gromov V.S. 2022. Ecology and social behaviour of the Mongolian gerbil: A generalised review // Behaviour. Vol.159. P.403–441.
- Gromov V.S. 2023. Ecology and social behaviour of the Brandt’s vole: A generalised review // Journal of Arid Environments. Vol.214. P.104994. DOI:10.1016/j.jaridenv.2023.104994.
- Gruder-Adams S. & Getz L.L. 1985. Comparison of the mating system and paternal behaviour in Microtus ochrogaster and Microtus pennsylvanicus // Journal of Mammalogy. Vol.66. P.165–167.
- Hamilton W.D. 1964. The genetical evolution of social behaviour // Journal of Theoretical Biology. Vol.7. P.1–52.
- Hayes L.D. & Solomon N.G. 2004. Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster) // Behavioral Ecology and Sociobiology. Vol.56. P.585–593.
- Hayne D.W. 1977. Survival rates of pine voles in North Carolina orchards // Proceedings of Pine and Meadow Voles Symposium. Vol.1. P.70–75.
- Horsfall F.Jr., Webb R.E. & Byers R.E. 1973. How to successfully meet pine voles on their own terms // Va Fruit. Vol.61. P.3–15.
- Huber S., Hoffmann I.E., Millesi E., Dittami J. & Arnold W. 2001. Explaining the seasonal decline in litter size in European ground squirrels // Ecography. Vol.24. P.205–211.
- Jamieson I. 1991. The unselected hypothesis for the evolution of helping behavior: too much or too little emphasis on natural selection? // American Naturalist. Vol.137. P.271–282.
- Jamieson I. & Craig J.L. 1987. Critique of helping behaviour in birds: a departure from functional explanations // Bateson P. & Klopfer P. (eds.). Perspectives in ethology. New York: Plenum. P.79–98.
- Jia R., Tai F., An S., Zhang X. & Broders H. 2009. Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles // Behavioural Processes. Vol.82. P.271–278.
- Kleiman D.G. 1977. Monogamy in mammals // Quarterly Review of Biology. Vol.52. P.39–69.
- Kokko H. & Johnstone R.A. 1999. Social queuing in animal societies: A dynamic model of reproductive skew // Proceedings of the Royal Society of London, Series B. Vol.266. P.571–578.
- Koenig W.D. & Pitelka F.A. 1981. Ecological factors and kin selection in the evolution of cooperative breeding in birds // Alexander R.D. & Tinkle D.W. (eds.). Natural selection and social behavior: Recent research and new theory. New York: Chiron. P.261–280.
- Lancaster J.B. 1971. Play-mothering: the relations between juvenile females and young infants among free-ranging vervet monkeys (Cercopithecus aethiops) // Folia Primatologica. Vol.15. P.161–182.
- Lepri J. & Vandenbergh J.B. 1986. Puberty in pine voles, Microtus pinetorum, and the influence of chemosignals in female reproduction // Biology of Reproduction. Vol.34. P.370–377.
- Ligon J.D. 1981. Demographic patterns and communal breeding in the green woodhoopoe, Phoeniculus purpureus // Alexander R.D. & Tinkle D.W. (eds.) Natural selection and social behavior. New York: Chiton Press. P.231–243.
- Ligon J.D. & Ligon S.H. 1978. Green woodhoopoes: life-history traits and sociality // Stacey P.B. & Koenig W.D. (eds.). Cooperative breeding in birds: long-term studies on ecology and behaviour. Cambridge: Cambridge University Press. P.33–65.
- Linksvayer T.A. & Wade M.J. 2005. The evolutionary origin and elaboration of sociality in the aculeate hymenoptera: Maternal effects, sib-social effects, and heterochrony // Quarterly Review of Biology. Vol.80. P.317–336.
- Lonstein J.S. & De Vries G.J. 1999. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster // Physiology & Behavior. Vol.66. P.33–45.
- Margulis S.W. 1997. Inbreeding-based bias in parental responsiveness to litters of oldfield mice // Behavioral Ecology and Sociobiology. Vol.41. P.177–184.
- Margulis S.W. 1998. Relationships among parental inbreeding, parental behavior and offspring viability in oldfield mice // Animal Behaviour. Vol.55. P.427–438.
- Margulis S.W., Nabong M., Alaks G., Walsh A. & Lacy R.C. 2005. Effects of early experience on subsequent parental behaviour and reproductive success in oldfield mice, Peromyscus polionotus // Animal Behaviour. Vol.69. P.627–634.
- Maynard-Smith J. 1964. Group selection and kin selection // Nature. Vol.201. P.1145–1147.
- McGuire B. & Novak M. 1984. A comparison of maternal behaviour in the meadow vole (Mictotus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum) // Animal Behaviour. Vol.32. P.1132–1141.
- Nunes S. 2007. Dispersal and philopatry // Wolff J.O & Sherman P.W. (eds.) Rodent Societies: An Ecological & Evolutionary Perspective. Chicago: University of Chicago Press. P.150–162.
- Oliveras D. & Novak M.A. 1986. A comparison of paternal behavior in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster // Animal Behaviour. Vol.34. P.519–526.
- Ostermeyer M.C. & Elwood R.W. 1984. Helpers (?) at the nest in the Mongolian gerbil, Meriones unguiculatus // Behaviour. Vol.91. P.61–77.
- Pillay N. & Rymer T.L. 2015. Alloparenting enhances the emotional, social and cognitive performance of female African striped mice, Rhabdomys pumilio // Animal Behaviour. Vol.99. P.43–52.
- Powell R.A. & Fried J.J. 1992. Helping by juvenile pine voles (Microtus pinetorum), growth and survival of younger siblings, and the evolution of pine vole sociality // Behavioral Ecology. Vol.3. P.325–333.
- Roberts R.L., Williams J.R., Wang A.K. & Carter C.S. 1998. Cooperative breeding and monogamy in prairie voles: Influence of the sire and geographic variation // Animal Behaviour. Vol.55. P.1131–1140.
- Rood J.P. 1990. Group size, survival, reproduction, and routes to breeding in dwarf mongooses // Animal Behaviour. Vol.39. P.566–572.
- Russell A.F., Brotherton P.N.M., McIlrath G.M., Sharpe L.L. & Clutton-Brock T.H. 2003. Breeding success in cooperative breeding meerkats: effects of helper number and maternal state // Behavioral Ecology. Vol.14. P.486–492.
- Rymer T.L. & Pillay N. 2014. Alloparental care in the African striped mouse Rhabdomys pumilio is age-dependent and influences the development of paternal care // Ethology. Vol.120. P.11–20.
- Salo A.L. & French J.A. 1989. Early experience, reproductive success, and development of parental behaviour in Mongolian gerbils // Animal Behaviour. Vol.38. P.693–702.
- Scantlebury M., Bennett N.C., Speakman J.R., Pillay N. & Schradin C. 2006: Huddling in groups leads to daily energy savings in free-living African four-striped grass mice, Rhabdomys pumilio // Functional Ecology. Vol.20. P.166–173.
- Schadler M.H. & Butterstein G.M. 1979. Reproduction in the pine vole, Microtus pinetorum // Journal of Mammalogy. Vol.60. P.841–844.
- Schradin C. 2005: When to live alone and when to live in groups: ecological determinants of sociality in the African striped mouse (Rhabdomys pumilio, Sparrman, 1784) // Belgium Journal of Zoology. Vol.135. P.77–82.
- Schradin C. 2008. Differences in prolactin levels between three alternative male reproductive tactics in striped mice (Rhabdomys pumilio) // Proceedings of the Royal Society of London, Series B. Vol.275. P.1047–1052.
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