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Behavioral Ecology and Sociobiology

, Volume 56, Issue 5, pp 449–457 | Cite as

Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis)

  • Eileen A. LaceyEmail author
Original Article

Abstract

In many social vertebrates, remaining in the natal group leads to at least short-term reductions in the direct fitness of philopatric animals. Among communally breeding rodents, the direct fitness costs of philopatry appear to increase as the frequency of successful natal dispersal decreases, suggesting a functional link between constraints on natal dispersal and the reproductive consequences of sociality. To explore this relationship empirically, I documented patterns of direct fitness among female colonial tuco-tucos (Ctenomys sociabilis), which are group-living subterranean rodents from southwestern Argentina. Demographic data suggest that successful natal dispersal is rare in this species, leading to the prediction that natal philopatry in C. sociabilis is associated with significant reductions in individual direct fitness. Using data obtained during 1996–2001, I compared the direct fitness of females that dispersed from their natal group and bred alone as yearlings to that of females that lived and bred in their natal group as yearlings. Philopatric yearlings reared significantly fewer young to weaning than did disperser (lone) yearlings. Although neither survival to a second breeding season nor the estimated lifetime number of pups reared to weaning differed between dispersal strategies, the annual direct fitness of group-living females was 23–40% less than expected, suggesting that philopatric animals experienced a substantial direct fitness cost by remaining in their natal group. These data yield important insights into the adaptive bases for group living in C. sociabilis and suggest that constraints on natal dispersal are an important factor favoring group living in this species.

Keywords

Communal breeding Direct fitness Philopatry Sociality Tuco-tucos 

Notes

Acknowledgements

For permission to work on Estancia Rincón Grande, I thank Alain Thouyaret and the Delegación Técnica de la Administración de Parques Nacionales Argentinas. For logistic help, I am particularly grateful to C. Chehebar, M. Christie, G. Iglesias, and E. Ramilo. Assistance in the field was provided by A. Chiesa, L. Good-Brummer, T. Hambuch, G. Izquierdo, M. Soares, A. Toloza, I. Tomasco, C. Toropova, R. Young, and, in particular, J. Wieczorek. Financial support was provided by the National Science Foundation (DEB-9704462), the National Geographic Society, the Miller Institute for Basic Research in Science, and the University of California, Berkeley. Previous versions of this manuscript benefited considerably from comments provided by E.H. DuVal, L.D. Hayes, R.L. Mumme, K.J. Nutt, M.M. Soares, N.G. Solomon, two anonymous reviewers and, especially, M.E. Hauber. This work was conducted in compliance with all applicable local and U.S. laws and was approved by the IACUC at the University of California, Berkeley.

References

  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Armitage KB (1991) Social and population dynamics of yellow-bellied marmots: results from long-term research. Annu Rev Ecol Syst 22:379–407CrossRefGoogle Scholar
  3. Armitage KB, Schwartz OA (2000) Social enhancement of fitness in yellow-bellied marmots. Proc Natl Acad Sci USA 97:12149–12152CrossRefPubMedGoogle Scholar
  4. Braude SH (2000) Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the mating system. Behav Ecol 11:7–12CrossRefGoogle Scholar
  5. Brown CR, Brown MB (1996) Coloniality in the cliff swallow: the effect of group size on social behavior. University of Chicago Press, ChicagoGoogle Scholar
  6. Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, PrincetonGoogle Scholar
  7. Busch C, Antinuchi CD, del Valle JC, Kittlein MJ, Malizia AI, Vassallo AI, Zenuto RR (2000) Population ecology of subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life underground: the biology of subterranean rodents. University of Chicago Press, Chicago, pp 182–226Google Scholar
  8. Clutton-Brock TH (ed) (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, ChicagoGoogle Scholar
  9. Clutton-Brock TH (1998) Reproductive skew, concessions, and limited control. Trends Ecol Evol 13:288–292CrossRefGoogle Scholar
  10. Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449CrossRefPubMedGoogle Scholar
  11. Courchamp F, Grenfell B, Clutton-Brock T (1999) Population dynamics of obligate cooperative breeders. Proc R Soc Lond B 266:557–563CrossRefGoogle Scholar
  12. Creel SR, Waser PM (1994) Inclusive fitness and reproductive strategies in dwarf mongooses. Behav Ecol 5:339–348Google Scholar
  13. Downhower JF, Armitage KB (1971) The yellow-bellied marmot and the evolution of polygamy. Am Nat 105:355–370CrossRefGoogle Scholar
  14. Emlen ST (1982) The evolution of helping. I. An ecological constraints model. Am Nat 119:29–39CrossRefGoogle Scholar
  15. Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell, Oxford, pp 301–337Google Scholar
  16. Emlen ST (1995) An evolutionary theory of the family. Proc Natl Acad Sci USA 92:8092–8099PubMedGoogle Scholar
  17. Erdfelder E, Faul F, Buchner A (1996) GPOWER: a general power analysis program. Behav Res Methods Instrum Comput 28:1–11Google Scholar
  18. Hayes LD (2000) To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim Behav 59:1–12PubMedGoogle Scholar
  19. Hoogland JL (1985) Infanticide in prairie dogs: lactating females kill offspring of close kin. Science 230:1037–1040Google Scholar
  20. Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. University of Chicago Press, ChicagoGoogle Scholar
  21. Johnston J (1991) Econometric methods. McGraw-Hill, New YorkGoogle Scholar
  22. Keller B (1985) Reproductive patterns. In: Tamarin RH (ed) Biology of New World Microtus. Spec Publ 8 American Society of Mammalogists, pp 725–768Google Scholar
  23. Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102.CrossRefGoogle Scholar
  24. Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150PubMedGoogle Scholar
  25. Koenig WD, Van Vuren D, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11:514–517CrossRefGoogle Scholar
  26. Lacey EA (2001) Microsatellite variation in solitary and social tuco-tucos: molecular properties and population dynamics. Heredity 86:628–637CrossRefPubMedGoogle Scholar
  27. Lacey EA, Sherman PW (1997) Cooperative breeding in naked mole-rats: implications for vertebrate and invertebrate sociality. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge,pp 267–301Google Scholar
  28. Lacey EA, Wieczorek JR (2003) The ecology of sociality in rodents: a ctenomyid perspective. J Mammal 84:1198–1211Google Scholar
  29. Lacey EA, Wieczorek JR (2004) Kinship in colonial tuco-tucos: evidence from group composition and population structure. Behav Ecol (in press)Google Scholar
  30. Lacey EA, Braude SH, Wieczorek JR (1997) Burrow sharing by colonial tuco-tucos (Ctenomys sociabilis). J Mammal 78:556–562Google Scholar
  31. Malizia A, Busch C (1997) Breeding biology of the fossorial rodent Ctenomys talarum (Rodentia: Octodontidae). J Zool 242:463–471Google Scholar
  32. Marin G, Pilastro A (1994) Communally breeding doormice, Glis glis, are close kin. Anim Behav 47:1485–1487CrossRefGoogle Scholar
  33. May RM, Anderson RM (1979) Population biology of infectious diseases. Part 2. Nature 280:455–461PubMedGoogle Scholar
  34. Mumme RL (1997) A bird’s eye view of mammalian cooperative breeding. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 364–388Google Scholar
  35. Mumme RL, Koenig WD, Pitelka FA (1983) Reproductive competition in the communal acorn woodpecker: sisters destroy each other’s eggs. Nature 306:583–584Google Scholar
  36. Pilastro A, Gomiero T, Marin G (1994) Factors affecting body mass of young fat dormice (Glis glis) at weaning and by hibernation. J Zool (Lond) 234:13–23Google Scholar
  37. Rabenold KN (1984) Cooperative enhancement of reproductive success in tropical wren societies. Ecology 65:871–885Google Scholar
  38. SAS Institute (1998) Statview 5.0.1. SAS Institute, Cary NCGoogle Scholar
  39. SAS Institute (2002) JMP 5.0. SAS Institute, Cary NCGoogle Scholar
  40. Sherman PW, Morton ML (1984) Demography of Belding’s ground squirrels. Ecology 65:1617–1628Google Scholar
  41. Sherman PW, Lacey EA, Reeve HK, Keller L (1995) The eusociality continuum. Behav Ecol 6:102–108Google Scholar
  42. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  43. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, New YorkGoogle Scholar
  44. Solomon NG (2003) A reexamination of factors that influence natal philopatry in rodents. J Mammal 84:1182–1197Google Scholar
  45. Solomon NG, French JA (1997) The study of mammalian cooperative breeding. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 1–10Google Scholar
  46. Solomon NG, Getz LL (1997) Examination of alternative hypotheses for cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 199–230Google Scholar
  47. Stacey PB, Koenig WD (1990) Introduction. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge, pp ix-xviiiGoogle Scholar
  48. StatSoft (2002) Statistica 6.0. StatSoft,Tulsa, OKGoogle Scholar
  49. Van Vuren D, Armitage KB (1994) Reproductive success of colonial and non-colonial female yellow-bellied marmots (Marmota flaviventris). J Mammal 75:950–955Google Scholar
  50. Vehrencamp SL (1977) Relative fecundity and parental effort in communally nesting anis, Crotophaga sucirostris. Science 197:403–405Google Scholar
  51. Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682Google Scholar
  52. Wolff JO (1994) Reproductive success of solitarily and communally nesting white-footed mice and deer mice. Behav Ecol 5:206–209Google Scholar
  53. Woodroffe R, Macdonald DW (2000) Helpers provide no detectable benefits in the European badger (Meles meles). J Zool (Lond) 250:113–119Google Scholar
  54. Woolfenden GE (1975) Florida scrub jay helpers at the nest. Auk 92:1–15Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Museum of Vertebrate Zoology and Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA

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