The size-life span trade-off decomposed: Why large dogs die young

American Naturalist

Volumn 181, Issue 4, 2013, Pages 492-505

  Kraus, Cornelia ^a,b   Pavard, Samuel ^a,c   Promislow, Daniel E L ^d  

^a MAX PLANCK INSTITUTE FOR DEMOGRAPHIC RESEARCH   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c Université Diderot Paris 7   (France)

^d University of Georgia ^*  (United States)

Author keywords

Aging rate; Baseline hazard; Dogs; Life span; Onset of senescence; Size

Indexed keywords

AGING; BODY SIZE; CANID; DOMESTIC SPECIES; ECOLOGICAL MODELING; LIFE CYCLE; LIFE EXPECTANCY; MORTALITY; SENESCENCE; SURVIVAL; TRADE-OFF;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; DOG; HISTOLOGY; LONGEVITY; PHYSIOLOGY;

ANIMALS; BODY SIZE; DOGS; LONGEVITY; MODELS, BIOLOGICAL;

CANIS FAMILIARIS; MAMMALIA;

EID: 84875496047     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/669665     Document Type: Article

References (86)

1. Anisimov, V. N., K. G. Arbeev, I. G. Popovic, M. A. Zabezhinksi, S. V. Rosenfeld, T. S. Piskunova, L. S. Arbeeva, A. V. Semenchenko, and A. I. Yashin. 2004. Body weight is not always a good predictor of longevity in mice. Experimental Gerontology 39:305-319.
2. Austad, S. N. 2005. Diverse aging rates in metazoans: targets for functional genomics. Mechanisms of Ageing and Development 126:43-49.
3. Austad, S. N. 2010. Animal size, metabolic rate, and survival, among and within species. Pp. 27-41 in N. S. Wolf, ed. The comparative biology of aging. Springer, Dordrecht.
4. Bartke, A., K. Coshigano, J. Kopchick, V. Chandrashekar, J. Mattison, B. Kinney, and S. Hauck. 2001a. Genes that prolong life: relationships of growth hormone and growth to aging and life span. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 56:B340-B349.
5. Bartke, A., J. C. Wright, J. A. Mattison, D. K. Ingram, R. A. Miller, and G. S. Roth. 2001b. Longevity: extending the lifespan of longlived mice. Nature 414:412.
6. Berryman, D. E., J. S. Christiansen, G. Johannsson, M. O. Thorner, and J. J. Kopchick. 2008. Role of the GH/IGF-1 axis in lifespan and healthspan: lessons from animal models. Growth Hormone and IGF Research 18:455-471.
7. Blanckenhorn, W. U. 2000. The evolution of body size: what keeps organisms small? Quarterly Review of Biology 75:385-407.
8. Bonnett, B. N., A. Egenvall, A. Hedhammar, and P. Olson. 2005. Mortality in over 350,000 insured Swedish dogs from 1995-2000. I. Breed-, gender-, age-and cause-specific rates. Acta Veterinaria Scandinavica 46:105-120.
9. Bonsall, M. B. 2006. Longevity and ageing: appraising the evolutionary consequences of growing old. Philosophical Transactions of the Royal Society B: Biological Sciences 361:119-135.
10. Boyko, A. R., P. Quignon, L. Li, J. J. Schoenebeck, J. D. Degenhardt, K. E. Lohmueller, K. Y. Zhao, et al. 2010. A simple genetic architecture underlies morphological variation in dogs. PLoS Biology 8:e1000451.
11. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
12. Charnov, E. L. 1993. Life history invariants. Oxford University Press, New York.
13. Charnov, E. L., and D. Berrigan. 1991. Dimensionless numbers and the assembly rules for life histories. Philosophical Transactions of the Royal Society B: Biological Sciences 332:41-48.
14. Chen, D., K. Z. Pan, J. E. Palter, and P. Kapahi. 2007. Longevity determined by developmental arrest genes in Caenorhabditis elegans. Aging Cell 6:525-533.
15. Cichon, M. 1997. Evolution of longevity through optimal resource allocation. Proceedings of the Royal Society B: Biological Sciences 264:1383-1388.
16. Cooley, D. M., D. L. Schlittler, L. T. Glickman, M. Hayek, and D. J. Waters. 2003. Exceptional longevity in pet dogs is accompanied by cancer resistance and delayed onset of major diseases. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 58:1078-1084.
17. Dammrich, K. 1991. Relationship between nutrition and bonegrowth in large and giant dogs. Journal of Nutrition 121:S114-S121.
18. Davis, T., and D. Kipling. 2005. Telomeres and telomerase biology in vertebrates: progress towards a non-human model for replicative senescence and ageing. Biogerontology 6:371-385.
19. de Magalhaes, J. P., J. Costa, and G. M. Church. 2007. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:149-160.
20. Desai, M., and C. N. Hales. 1997. Role of fetal and infant growth in programming metabolism in later life. Biological Reviews of the Cambridge Philosophical Society 72:329-348.
21. Drapeau, M. D., E. K. Gass, M. D. Simison, L. D. Mueller, and M. R. Rose. 2000. Testing the heterogeneity theory of late-life mortality plateaus by using cohorts of Drosophila melanogaster. Experimental Gerontology 35:71-84.
22. Eigenmann, J. E., A. Amador, and D. F. Patterson. 1988. Insulin-like growth factor-1 levels in proportionate dogs, chondrodystrophic dogs and giant dogs. Acta Endocrinologica 118:105-108.
23. Favier, R. P., J. A. Mol, H. S. Kooistra, and A. Rijnberk. 2001. Large body size in the dog is associated with transient GH excess at a young age. Journal of Endocrinology 170:479-484.
24. Finch, C. E., and E. M. Crimmins. 2004. Inflammatory exposure and historical changes in human life-spans. Science 305:1736-1739.
25. Fleming, J. M., K. E. Creevy, and D. E. L. Promislow. 2011. Mortality in North American dogs from 1984 to 2004: an investigation into age-, size-, and breed-related causes of death. Journal of Veterinary Internal Medicine 25:187-198.
26. Gaillard J.-M., M. Festa-Bianchet, D. Delorme, and J. Jorgenson. 2000. Body mass and individual fitness in female ungulates: bigger is not always better. Proceedings of the Royal Society B: Biological Sciences 267:471-477.
27. Gaillard, J.-M., D. Pontier, D. Allainé, J. D. Lebreton, J. Trouvilliez, and J. Clobert. 1989. An analysis of demographic tactics in birds and mammals. Oikos 56:59-76.
28. Galis, F., I. Van Der Sluijs, T. J. M. Van Dooren, J. A. J. Metz, and M. Nussbaumer. 2007. Do large dogs die young? Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 308B:119-126.
29. Gompertz, B. 1825. On the nature of the function expressive of the law of human mortality, and on the mode of determining the value of life contingencies. Philosophical Transactions of the Royal Society 115:513-585.
30. Greer, K., L. Hughes, and M. Masternak. 2011. Connecting serum IGF-1, body size, and age in the domestic dog. Age 33:475-483.
31. Greer, K. A., S. C. Canterberry, and K. E. Murphy. 2007. Statistical analysis regarding the effects of height and weight on life span of the domestic dog. Research in Veterinary Science 82:208-214.
32. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.
33. Hawthorne, A. J., D. Booles, P. A. Nugent, G. Gettinby, and J. Wilkinson. 2004. Body-weight changes during growth in puppies of different breeds. Journal of Nutrition 134:2027S-2030S.
34. Jones, O. R., J. M. Gaillard, S. Tuljapurkar, J. S. Alho, K. B. Armitage, P. H. Becker, and P. Bize, et al. 2008. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecology Letters 11:664-673.
35. Juckett, D. A., and B. Rosenberg. 1993. Comparison of the Gompertz and Weibull functions as descriptors for human mortality distributions and their intersections. Mechanisms of Ageing and Development 69:1-31.
36. Kang, H. M., N. A. Zaitlen, C. M. Wade, A. Kirby, D. Heckerman, M. J. Daly, and E. Eskin. 2008. Efficient control of population structure in model organism association mapping. Genetics 178: 1709-1723.
37. Kaplan, H. S., and A. J. Robson. 2009. We age because we grow. Proceedings of the Royal Society B: Biological Sciences 276:1837-1844.
38. Kenyon, C. 2005. The plasticity of aging: insights from long-lived mutants. Cell 120:449-460.
39. Khazaeli, A. A., W. J. Van Voorhies, and W. Curtsinger. 2005. The relationship between life span and adult body size is highly strainspecific in Drosophila melanogaster. Experimental Gerontology 40: 377-385.
40. Kirkwood, J. K. 1985. The influence of size on the biology of the dog. Journal of Small Animal Practice 26:97-110.
41. Kirkwood, T. B. L. 2005. Understanding the odd science of aging. Cell 120:437-447.
42. Klein, J. P., and M. L. Moeschberger. 2005. Survival analysis: techniques for censored and truncated data. Springer, Berlin.
43. Levitis, D. A. 2011. Before senescence: the evolutionary demography of ontogenesis. Proceedings of the Royal Society B: Biological Sciences 278:801-809.
44. Li, Y., B. Deeb, W. Pendergrass, and N. Wolf. 1996. Cellular proliferative capacity and life span in small and large dogs. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 51: B403-B408.
45. Lindblad-Toh, K., C. M. Wade, T. S. Mikkelsen, E. K. Karlsson, D. B. Jaffe, M. Kamal, M. Clamp, et al. 2005. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803-819.
46. Metcalfe, N. B., and P. Monaghan. 2003. Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology 38:935-940.
47. Michell, A. R. 1999. Longevity of British breeds of dog and its relationships with sex, size, cardiovascular variables and disease. Veterinary Record 145:625-629.
48. Miller, R. A., C. Chrisp, and W. Atchley. 2000. Differential longevity in mouse stocks selected for early life growth trajectory. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 55:B455-B461.
49. Miller, R. A., J. M. Harper, A. Galecki, and D. T. Burke. 2002. Big mice die young: early life body weight predicts longevity in genetically heterogeneous mice. Aging Cell 1:22-29.
50. Monaghan, P., A. Charmantier, D. H. Nussey, and R. E. Ricklefs. 2008. The evolutionary ecology of senescence. Functional Ecology 22:371-378.
51. Moody, J. A., L. A. Clark, and K. E. Murphy. 2006. Canine history and breed clubs. Pages 1-18 in E. A. Ostrander and F. Galibert, eds. The dog and its genome. CSHL, New York.
52. Moorad, J. A., D. E. L. Promislow, N. Flesness, and R. A. Miller. 2012. A comparative assessment of univariate longevity measures using zoological animal records. Aging Cell 11:940-948, doi: 10.1111/j.1474-9726.2012.00861.x.
53. Morgan, I. J., I. D. McCarthy, and N. B. Metcalfe. 2000. Life-history strategies and protein metabolism in overwintering juvenile Atlantic salmon: growth is enhanced in early migrants through lower protein turnover. Journal of Fish Biology 56:637-647.
54. Nasir, L., P. Devlin, T. McKevitt, G. Rutteman, and D. J. Argyle. 2001. Telomere lengths and telomerase activity in dog tissues: a potential model system to study human telomere and telomerase biology. Neoplasia 3:351-359.
55. Nelder, J. A., and R. Mead. 1965. A simplex algorithm for function minimization. Computer Journal 7:308-313.
56. Olsson, M., and R. Shine. 2002. Growth to death in lizards. Evolution 56:1867-1870.
57. Parker, H. G., L. V. Kim, N. B. Sutter, S. Carlson, T. D. Lorentzen, T. B. Malek, G. S. Johnson, et al. 2004. Genetic structure of the purebred domestic dog. Science 304:1160-1164.
58. Partridge, L., and N. H. Barton. 1996. On measuring the rate of ageing. Proceedings of the Royal Society B: Biological Sciences 263: 1365-1371.
59. Patronek, G. J., D. J. Waters, and L. T. Glickman. 1997. Comparative longevity of pet dogs and humans: implications for gerontology research. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 52:B171-B178.
60. Peron, G., O. Gimenez, A. Charmantier, J. M. Gaillard, and P. A. Crochet. 2010. Age at the onset of senescence in birds and mammals is predicted by early-life performance. Proceedings of the Royal Society B: Biological Sciences 277:2849-2856.
61. Pletcher, S. D., and J. W. Curtsinger. 1998. Mortality plateaus and the evolution of senescence: why are old-age mortality rates so low? Evolution 52:454-464.
62. Promislow, D. E. L. 1991. Senescence in natural populations of mammals: a comparative study. Evolution 45:1869-1887.
63. Promislow, D. E. L., and P. H. Harvey. 1990. Living fast and dying young: a comparative analysis of life-history variation among mammals. Journal of Zoology (London) 220:417-437.
64. Promislow, D. E. L., M. Tatar, S. Pletcher, and J. R. Carey. 1999. Below-threshold mortality: implications for studies in evolution, ecology and demography. Journal of Evolutionary Biology 12:314-328.
65. Proschowsky, H. F., H. Rugbjerg, and A. K. Ersboll. 2003. Mortality of purebred and mixed-breed dogs in Denmark. Preventive Veterinary Medicine 58:63-74.
66. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
67. Reznick, D., L. Nunney, and A. Tessier. 2000. Big houses, big cars, superfleas and the costs of reproduction. Trends in Ecology and Evolution 15:421-425.
68. Ricklefs, R. E. 2006. Embryo development and ageing in birds and mammals. Proceedings of the Royal Society B: Biological Sciences 273:2077-2082.
69. Ricklefs, R. E., and A. Scheuerlein. 2001. Comparison of aging-related mortality among birds and mammals. Experimental Gerontology 36:845-857.
70. Ricklefs, R. E., and A. Scheuerlein. 2002. Biological implications of the Weibull and Gompertz models of aging. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 57:B69-B76.
71. Rollo, C. D. 2002. Growth negatively impacts the life span of mammals. Evolution and Development 4:55-61.
72. Samaras, T. J. 2009. Should we be concerned over increasing body height and weight? Experimental Gerontology 44:83-92.
73. Sauer, J. R., and N. A. Slade. 1987. Uinta ground squirrel demography: is body mass a better categorical variable than age? Ecology 68:642-650.
74. Siler, W. 1979. A competing-risk model for animal mortality. Ecology 60:750-757.
75. Speakman, J. R., A. van Acker, and E. J. Harper. 2003. Age-related changes in the metabolism and body composition of three dog breeds and their relationship to life expectancy. Aging Cell 2:265-275.
76. Sutter, N., D. Mosher, M. Gray, and E. Ostrander. 2008. Morphometrics within dog breeds are highly reproducible and dispute Rensch's rule. Mammalian Genome 19:713-723.
77. Sutter, N. B., C. D. Bustamante, K. Chase, M. M. Gray, K. Y. Zhao, L. Zhu, B. Padhukasahasram, et al. 2007. A single IGF1 allele is a major determinant of small size in dogs. Science 316:112-115.
78. Sutter, N. B., and E. A. Ostrander. 2004. Dog star rising: the canine genetic system. Nature Reviews Genetics 5:900-910.
79. Tatar, M., A. Bartke, and A. Antebi. 2003. The endocrine regulation of aging by insulin-like signals. Science 299:1346-1351.
80. Teuschl, Y., C. Reim, and W. U. Blanckenhorn. 2006. Correlated response to artificial selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies. Journal of Evolutionary Biology 20:87-103.
81. Thatcher, A. R., V. Kannisto, and J. W. Vaupel. 1998. The force of mortality at ages 80 to 120. Odense Monographs on Population Aging 5. Odense University Press, Odense.
82. van der Most, P. J., B. de Jong, H. K. Parmentier, and S. Verhulst. 2011. Trade-off between growth and immune function: a metaanalysis of selection experiments. Functional Ecology 25:74-80.
83. Vaupel, J. W., and A. I. Yashin. 1985. Heterogeneity ruses: some surprising effects of selection on population dynamics. American Statistician 39:176-185.
84. Weibull, W. 1951. A statistical distribution function of wide applicability. Journal of Applied Mechanics 18:293-297.
85. Williams, P. D., T. Day, Q. Fletcher, and L. Rowe. 2006. The shaping of senescence in the wild. Trends in Ecology and Evolution 21: 458-463.
86. Wilson, D. L. 1994. The analysis of survival (mortality) data: fitting Gompertz, Weibull, and logistic functions. Mechanisms of Ageing and Development 74:15-33.