Survival costs of reproduction vary with age in North American red squirrels

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1659, 2009, Pages 1129-1135

  Descamps, Sébastien ^a,b   Boutin, Stan ^c   McAdam, Andrew G ^d   Berteaux, Dominique ^a   Gaillard, Jean Michel ^b  

^a UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

Age structured population; Food supply; Survival; Tamiasciurus hudsonicus; Trade off

Indexed keywords

AGE-RELATED DIFFERENCE; FOOD SUPPLY; REPRODUCTIVE COST; RODENT; SENESCENCE; SURVIVAL;

TAMIASCIURUS; TAMIASCIURUS HUDSONICUS;

EID: 60049084398     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1401     Document Type: Article

References (55)

1. Allison, P. D. 1995 Survival analyses using the SAS system. A practical guide. Cary, NC: SAS Institute, Inc.
2. Berteaux, D. & Boutin, S. 2000 Breeding dispersal in female North American red squirrels. Ecology 81, 1311-1326.
3. Boutin, S., Wauters, L. A., McAdam, A. G., Humphries, M. M., Tosi, G. & Dhondt, A. A. 2006 Anticipatory reproduction and population growth in seed predators. Science 314, 1928-1930.
4. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference: a practical information-theoretic approach. New York, NY: Springer.
5. Cam, E. & Monnat, J.-Y. 2000 Stratification based on reproductive state reveals contrasting patterns of age-related variation in demographic parameters in the kittiwake. Oikos 90, 560-574.
6. Cam, E., Hines, J. E., Monnat, J.-Y., Nichols, J. D. & Danchin, E. 1998 Are adult nonbreeders prudent parents? The kittiwake model. Ecology 79, 2917-2930.
7. Cam, E., Link, W. A., Cooch, E. G., Monnat, J.-Y. & Danchin, E. 2002 Individual covariation in life-history traits: seeing the trees despite the forest. Am. Nat. 159, 96-105.
8. Clutton-Brock, T. H. 1984 Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 123, 212-229.
9. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. 1982 Red deer: behavior and ecology of two sexes. Chicago, IL: The University of Chicago Press.
10. Clutton-Brock, T. H., Albon, S. D. & Guiness, F. E. 1989 Fitness costs of gestation and lactation in wild mammals. Nature 337, 260-262.
11. Cody, M. L. 1966 A general theory of clutch size. Evolution 20, 174-184.
12. Davis, S. E., Nager, R. G. & Furness, R. W. 2005 Food availability affects adult survival as well as breeding success of parasitic Jaegers. Ecology 86, 1047-1056.
13. Descamps, S. 2006 Stratégies d'histoire de vie dans une population d'écureuils roux d'Amérique du Nord. PhD thesis, Université du Québec à Rimouski.
14. Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J.-M. 2006 Best squirrels trade a long life for an early reproduction. Proc. R. Soc. B 273, 2369-2374.
15. Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J.-M. 2007 Female red squirrels fit William's hypothesis of increasing reproductive effort with increasing age. J. Anim. Ecol. 76, 1192-1201.
16. Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J.-M. 2008a Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117, 1406-1416.
17. Descamps, S., Boutin, S., Berteaux, D., McAdam, A. G. & Gaillard, J.-M. 2008b Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success. J. Anim. Ecol. 77, 305-314.
18. Evans, R. M. 1990 The relationship between parental input and investment. Anim. Behav. 39, 797-798.
19. Festa-Bianchet, M. & Jorgenson, J. T. 1998 Selfish mothers: reproductive expenditure and resource availability in bighorn ewes. Behav. Ecol. 9, 144-150.
20. Festa-Bianchet, M., Gaillard, J.-M. & Jorgenson, J. T. 1998 Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am. Nat. 152, 367-379.
21. Fisher, R. A. 1930 The genetical theory of natural selection. Dover, NY: Claredon Press.
22. Gaillard, J.-M. & Yoccoz, N. G. 2003 Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84, 3294-3306.
23. Harshman, L. G. & Zera, A. J. 2006 The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22, 80-86.
24. Humphries, M. M. & Boutin, S. 2000 The determinants of optimal litter size in free-ranging red squirrels. Ecology 81, 2867-2877.
25. Hurlbert, S. H. 1984 Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187-211.
26. LaMontagne, J. M. 2007 Spatial and temporal variability in white spruce (Picea glauca) cone production: individual and population responses of North American red squirrels (Tamiasciurus hudsonicus). PhD thesis, Department of Biological Sciences, University of Alberta.
27. LaMontagne, J. M. & Boutin, S. 2007 Local-scale synchrony and variability in mast seed production patterns of Picea glauca. J. Ecol. 95, 991-1000.
28. LaMontagne, J. M., Peters, S. & Boutin, S. 2005 A visual index for estimating cone production for individual white spruce trees. Can. J. For. Res. 35, 3020-3026.
29. Lindström, K. 2001 Effects of resource distribution on sexual selection and the cost of reproduction in Sandgobies. Am. Nat. 158, 64-74.
30. Littell, R. C., Milliken, G. A., Stroup, W. W. & Wolfinger, R. S. 1996 SAS system for mixed models. Cary, NC: SAS Institute.
31. Mayor, S. 2004 Pregnancy and childbirth are leading causes of death in teenage girls in developing countries. Br. Med. J. 328, 1152.
32. McAdam, A. G. & Boutin, S. 2003 Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels. J. Evol. Biol. 16, 1249-1253.
33. McAdam, A. G., Boutin, S., Réale, D. & Berteaux, D. 2002 Maternal effects and the potential for evolution in a natural population of animals. Evolution 56, 846-851.
34. McAdam, A. G., Boutin, S., Sykes, A. K. & Humphries, M. M. 2007 Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Écoscience 14, 362-369.
35. Metcalfe, N. B. & Monaghan, P. 2001 Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254-260.
36. Millar, J. S. 1978 Energetics of reproduction in Peromyscus leucopus: the cost of lactation. Ecology 59, 1055-1061.
37. Nagelkerke, N. J. D. 1991 A note on a general definition of the coefficient of determination. Biometrika 78, 691-692.
38. Newcomb, W. W., Rodriguez, M. & Johnson, J. W. C. 1991 Reproduction in the older gravida: a literature-review. J. Reprod. Med. 36, 839-845.
39. Nichols, J. D. 1992 Capture-recapture methods. BioScience 42, 94-102.
40. Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J.-M. 2008 Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22, 393-406.
41. Penn, D. J. & Smith, K. R. 2007 Differential fitness costs of reproduction between the sexes. Proc. Natl Acad. Sci. USA 104, 553-558.
42. Réale, D., Boussès, P. & Chapuis, J.-L. 1999 Nursing behaviour and mother-lamb relationships in mouflon under fluctuating population densities. Behav. Process. 47, 81-94.
43. Reznick, D. 1985 Costs of reproduction: an evaluation of the empirical evidence. Oikos 44, 257-267.
44. Roff, D. A. 2002 Life history evolution. Sunderland, MA: Sinauer Associates, Inc.
45. Rose, M. 1991 Evolutionary biology of aging. New York, NY: Oxford University Press.
46. Schaffer, W. M. 1983 The application of optimal control theory to the general life history problem. Am. Nat. 121, 418-431.
47. Smith, C. C. 1968 The adaptive nature of social organization in the genus of three squirrels Tamiasciurus. Ecol. Monogr. 38, 31-63.
48. Tavecchia, G., Coulson, T., Morgan, B. J. T., Pemberton, J. M., Pilkington, J. C., Gulland, F. M. D. & Clutton-Brock, T. H. 2005 Predictors of reproductive cost in female Soay sheep. J. Anim. Ecol. 74, 201-213.
49. Thompson, S. D. & Nicoll, M. E. 1986 Basal metabolic rates and energetics of reproduction in therian mammals. Nature 321, 690-693.
50. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871-1971 (ed. B. Campbell), pp. 136-179. Chicago, IL: Aldine-Atherton.
51. Van de Pol, M. & Verhulst, S. 2006 Age-dependent traits: a new statisticalmodel to separate within- and between-individual effects. Am. Nat. 167, 766-773.
52. Van Noordwijk, A. J. & de Jong, G. 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137-142.
53. Vaupel, J. W. & Yashin, A. I. 1985 Heterogeneity's ruses: some surprising effects of selection on population dynamics. Am. Stat. 39, 176-185.
54. Weladji, R. B., Loison, A., Gaillard, J.-M., Holand, O., Mysterud, A., Yoccoz, N. G., Nieminen, M. & Stenseth, N. C. 2008 Heterogeneity in individual quality overrides costs of reproduction in female reindeer. Oecologia 156, 237-247.
55. Williams, G. C. 1966 Natural selection, the costs of reproduction and a refinement of Lack's principle. Am. Nat. 100, 687-690.