The evolution of sociality in rodents: a family affair
Gromov V.S.
P. 47-65
Sociality means group-living. Among rodents, the most social species live in family groups that consist as a rule of not numerous individuals. Hence, the evolution of sociality among rodents is not a group-size evolution. A family-group lifestyle is associated with long-lasting pair bonds, participation of both parents in care of young, and cooperation in different activities. In family groups, cooperation starts from the very beginning when a breeding pair establishes, protects and marks its home range, digs burrows or constructs other shelters, and provides care-giving activities. Direct parental care (especially paternal care) by means of tactile stimulation of the young is suggested to promote long-lasting pair bonds and development of subsequent parental behaviors in sub-adult and adult males that is so typical of highly social rodent species. This phenomenon has an epigenetic nature and could be considered as ‘stimulation of similar with the similar’. Cooperation extends and intensifies when the size of family groups increases as a result of delayed dispersal of the offspring. According to the proposed conceptual model, family groups could be formed under any ecological conditions, irrespective of predation pressure or resource distribution, given that mating pairs and, furthermore, family groups are more competitive due to cooperation than solitary conspecifics. The main driving forces are proximate mechanisms related to tactile stimulation of young individuals during their early postnatal development and cooperation. This conceptual model provides a better understanding of the evolution of sociality (i.e. transition to a family-group lifestyle) in different rodent taxa.DOI: 10.15298/rusjtheriol.16.1.05
- Ågren G., Zhou Q. & Zhong W. 1989a. Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China // Animal Behaviour. Vol.37. P.11–27.
- Ågren G., Zhou Q. & Zhong W. 1989b. Territoriality, cooperation and resource priority in the Mongolian gerbil, Meriones unguiculatus // Animal Behaviour. Vol.37. P.28–32.
- Alexander R.D. 1974. The evolution of social behavior // Annual Reviews in Ecology and Systematics. Vol.5. P.325–383.
- Armitage K.B. 1962. Social behavior of the yellow-bellied marmot (Marmota flaviventris) // Animal Behaviour. Vol.10. P.319–331.
- Armitage K.B. 1981. Sociality as a life-history tactic of ground squirrels // Oecologia (Berlin). Vol.48. P.36–49.
- Armitage K.B. 1999. Evolution of sociality in marmots // Journal of Mammalogy. Vol.80. P.1–10.
- Armitage K.B. 2007. Evolution of sociality in marmots: It begins with hibernation // Wolff J.O. & Sherman P.W. (eds.). Rodent societies: An ecological and evolutionary perspective. Chicago: University of Chicago Press. P.356–367.
- Arnold W. 1990a. The evolution of marmot sociality: I. Why disperse late? // Behavioral Ecology and Sociobiology. Vol.27. P.229–237.
- Arnold W. 1990b. The evolution of marmot sociality: II. Costs and benefits of joint hibernation // Behavioral Ecology and Sociobiology. Vol.27. P.239–246.
- Arnold W. 1993. Energetics of social hibernation // Carey C., Florant G.L., Wunder B.A. & Horwitz B.B. (eds.). Life in the cold: Ecological, physiological and molecular mechanisms. Colorado: Westview Press. P.65–80.
- Barash D.P. 1973. The social biology of the Olympic marmot (Marmota olympus) // Animal Behavior Monographs. Vol.6. P.171–245.
- Barash D.P. 1974. The evolution of marmot societies: a general theory // Science. Vol.185. P.415–420.
- Barash D.P. 1976. Social behaviour and individual differences in free-living alpine marmots (Marmota marmota) // Animal Behaviour. Vol.24. P.27–35.
- Bennett N.C. & Faulkes C.G. 2000. African mole-rats: ecology and eusociality. Cambridge: Cambridge University Press. 189 p.
- Blumstein D.T. 1996. How much does social group size influence golden marmot vigilance? // Behaviour. Vol.133. P.1133–1151.
- Blumstein D.T. & Armitage K.B. 1997. Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls // American Naturalist. Vol.150. P.179–200.
- Blumstein D.T. & Armitage K.B. 1998. Life history consequences of social complexity: a comparative study of ground-dwelling sciurids // Behavioral Ecology. Vol.9. P.8–19.
- Blumstein D.T., Steinmetz J. & Armitage K.B. 1997. Alarm calling on yellow-bellied marmots. II. The importance of direct fitness // Animal. Behaviour. Vol.53. P.173–184.
- Bonthuis P.J., Patteson J.K. & Rissman E.F. 2011. Acquisition of sexual receptivity: roles of chromatin acetylation, estrogen receptor-alpha, and ovarian hormones // Endocrinology. Vol.152. P.3172–3181.
- Brown R.E. & Moger W.H. 1983. Hormonal correlates of parental behavior in male rats // Hormones and Behavior. Vol.17. P.356–365.
- Bujalska G. & Saitoh T. 2000. Territoriality and its consequences // Polish Journal of Ecology. Vol.48. Suppl. P.37–49.
- Burda H. 1990. Constraints of pregnancy and evolution of sociality in mole-rats with special reference to reproductive and social patterns in Cryptomys hottentotus (Bathiergidae, Rodentia) // Zeitschrift fьr Zoologie und Systematische Evolutionsforschung. Bd.28. S.26–39.
- Burda H., Honeycutt R.H., Begall S., Locker-Grütjen O. & Scharff A. 2000. Are naked and common mole-rats eusocial, and if so, why? // Behavioral Ecology and Sociobiology. Vol.47. P.293–303.
- Busher P. 2007. Social organization and monogamy in the beaver // Wolff J.O. & Sherman P.W. (eds.). Rodent societies: An ecological and evolutionary perspective. Chicago: University of Chicago Press. P.280–290.
- Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M. & Meaney M.J. 1998. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat // Proceedings of National Academy of Sciences. Vol.95. P.5335–5340.
- Carey H.V. & Moore P. 1986. Foraging and predation risk in yellow-bellied marmots // American Midland Naturalist. Vol.116. P.267–275.
- Carr G.M. & Macdonald D.W. 1986. The sociality of solitary foragers: A model based on resource dispersion // Animal Behaviour. Vol.34. P.1540–1549.
- Carter C.S. & Getz L.L. 1993. Monogamy and prairie vole // Scientific American. Vol.268. P.100–106.
- Carter C.S. & Roberts R.L. 1997. The psychobiology of cooperative breeding in rodents // Solomon N.G. & French J. (eds.). Cooperative breeding in mammals. Cambridge: Cambridge University Press. P.231–266.
- Carter C.S., De Vries A.C. & Getz L.L. 1995. Physiological substrates of mammalian monogamy: the prairie vole model // Neuroscience and Biobehavior Reviews. Vol.19. P.303–314.
- Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M. & Meaney M.J. 2006. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring // Endocrinology. Vol.147. P.2909–2915.
- Clark M. & Galef B.G., Jr. 2000. Why some male Mongolian gerbils may help at the nest: testosterone, asexuality and alloparenting // Animal Behaviour. Vol.59. P.801–806.
- Clark M.M., vom Saal F.S. & Galef B.G. 1992. Intrauterine positions and testosterone levels of adult male gerbils are correlated // Physiology and Behavior. Vol.51. P.957-960.
- Clark 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.
- Clark M.M., Vonk J. & Galef B.G., Jr. 1998. Intrauterine position, parenting, and nest site-attachment in male Mongolian gerbils // Developmental Psychobiology. Vol.32. P.177–181.
- Clutton-Brock T.H. 1974. Primate social organization and ecology // Nature. Vol.250. P.539–542.
- Corbet N.U. & van Aarde R.J. 1996. Social organization and space use in the Cape porcupine in a southern African savanna // African Journal of Ecology. Vol.34. P.1–14.
- Crook J.H. 1970a. The socio-ecology of primates // Crook J.H. (ed.). Social behaviour in birds and mammals. London: Academic Press. P.103–156.
- Crook J.H. 1970b. Social organization and the environment: aspects of contemporary social ethology // Animal Behaviour. Vol.18. P.197–209.
- Daly M. & Daly S. 1974. Spatial distribution of a leaf-eating Saharan gerbil (Psammomys obesus) in relation to its food // Mammalia. Vol.38. P.591–603.
- Danielson B.J. & Gaines M.S. 1987. Spatial patterns in two synoptic species of microtines: Microtus ochrogaster and Synaptomys cooperi // Journal of Mammalogy. Vol.68. P.313–322.
- De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M. & Auger C.J. 2002. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits // Journal of Neuroscience. Vol.22. P.9005–9014.
- Dewsbury D.A. 1985. Paternal behavior in rodents // American Zoologist. Vol.25. P.841–852.
- Ebensperger L.A. & Cofrй H. 2001. On the evolution of group-living in the New World cursorial hystricognath rodents // Behavioral Ecology. Vol.12. P.227–236.
- Ebensperger L.A., Wallem P.K. 2002. Grouping increases the ability of the social rodent, Octodon degus, to detect predators when using exposed mictohabitats // Oikos. Vol.98. P.491–497.
- Ebensperger L.A., Veloso C. & Wallem P.K. 2002. Do female degus communally nest and nurse their pups? // Journal of Ethology. Vol.20. P.143–146.
- Ebensperger L.A., Hurtado M.J. & Ramos-Jiliberto R. 2006. Vigilance and collective detection of predators in degus (Octodon degus) // Ethology. Vol.112. P.879–887.
- Ebensperger L.A., Sobrero R., Quirici V., Castro R., Tolhuysen L.O., Vargas F., Burger J.R., Quispe R., Villavicencio C.P., Vasquez R.A. & Hayes L.D. 2012. Ecological drivers of group living in two populations of the communally rearing rodent, Octodon degus // Behavioral Ecology and Sociobiology. Vol.66. P.261–275.
- Eisenberg J.F., Muckenhirn N.A. & Rudran R. 1972. The relation between ecology and social structure in primates // Science. Vol.176. P.863–874.
- Elwood R.W. 1975. Paternal and maternal behaviour in the Mongolian gerbil // Animal Behaviour. Vol.23. P.766–772.
- Elwood R.W. 1979. Maternal and paternal behaviour of the Mongolian gerbil: a correlation study // Behavioral and Neural Biology. Vol.25. P.555–562.
- 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.
- Faulkes C.G., Bennett N.C., Bruford M.W., O’Brien H.P., Aguilar G.H. & Jarvis J.U.M. 1997. Ecological constraints drive social evolution in African mole-rats // Proceedings of Royal Society, London, Series B. Vol.264. P.1619–1627.
- Fleming A.S. & Luebke C. 1981. Timidity prevents the nulliparous female from being a good mother // Physiology and Behavior. Vol.27. P.863–868.
- Fleming A.S. & Sarker J. 1990. Experience-hormone interactions and maternal behavior in rats // Physiology and Behavior. Vol.47. P.1165–1173.
- Fleming A.S., O’Day D.H. & Kraemer G.W. 1999. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations // Neuroscience and Biobehavior Reviews. Vol.23. P.673–685.
- Fleming A.S., Kraemer G.W., Gonzalez A., Lovic V., Rees S. & Melo A. 2002. Mothering begets mothering: the transmission of behavior and it neurobiology across generations // Pharmacology and Biochemical Behavior. Vol.73. P.61–75.
- Foster J. & Gaines M.S. 1991. The effects of successional habitat mosaic on a small mammal community // Ecology. Vol.72. P.1358–1373.
- Francis D., Diorio J., Liu D. & Meany M.J. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat // Science. Vol.286. P.1155–1158.
- 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.
- Gatewood J.D., Wills A., Shetty S., Xu J., Arnold A.P. & Burgoyne P.S. 2006. Sex chromosome complement and gonadal sex influence on aggressive and parental behaviors in mice // Journal of Neuroscience. Vol.26. P.2335–2342.
- Gerling S. & Yahr P. 1979. Effect of the male parent on pup survival in Mongolian gerbils // Animal Behaviour. Vol.27. P.310–311.
- Getz L.L. 1985. Habitats // Tamarin R.H. (ed.). Biology of New World Microtus. Stillwater, Oklahoma: The American Society of Mammalogists. P.286–309.
- 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., 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.
- Gonzalez A., Lovic V., Ward G.R., Wainwright P.E. & Fleming A.S. 2001. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats // Developmental Psychobiology. Vol.38. P.11–32.
- Gromov V.S. 2001. Day-time activity and social interactions in a colony of the fat sand rats, Psammomys obesus, at the Negev Highlands, Israel // Mammalia. Vol.65. P.13–28.
- Gromov V.S. 2005. [Ritualized agonistic behavior in rodents] // Uspekhi Sovremennoi Biologii. Vol.125. P.522–533 [in Russian, with English summary].
- Gromov V.S. 2007. Spatial ethological structure and evolution of sociality in rodents // Doklady Biological Sciences. Vol.412. P.46–48.
- Gromov V.S. 2008. [The spatial-and-ethological population structure in rodents]. Moscow: KMK Scientific Press. 581 p. [in Russian].
- Gromov V.S. 2009. Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behavior of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions // Biology Bulletin. Vol.36. P.479–488.