Growth versus lifespan: perspectives from evolutionary ecology

There are many ecological advantages to attaining a large body size as fast as possible (such as reduced risks of being caught by predators or increased reproductive success). However, studies in several taxa indicate that fast growth in itself can have negative as well as positive effects. There appears to be a link between accelerated growth and lifespan: rapid growth early in life is associated with impaired later performance and reduced longevity. In this review we assess the evidence for such within individual trade-offs between growth rate and lifespan, and the potential physiological mechanisms that might underlie them. We discuss the fitness implications of any reduction in lifespan, and point out that certain environmental circumstances may favour a 'grow fast and die young' strategy if this increases overall reproductive success. However, investigation of the intra-specific relationships among growth rate, lifespan and fitness is not straightforward; few studies have controlled for confounding variables such as adult body size or duration of the growth period, and none to date have measured fitness in an appropriate ecological setting. We suggest a number of experimental approaches that might allow the true relationships between growth rate and future performance to be elucidated.

[1]  Mariusz Cichoń,et al.  Evolution of longevity through optimal resource allocation , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  Clive Osmond,et al.  Growth and living conditions in childhood and hypertension in adult life: a longitudinal study , 2002, Journal of hypertension.

[3]  A. Houston,et al.  State-dependent life histories , 1996, Nature.

[4]  N. Metcalfe,et al.  Life-history strategies and protein metabolism in overwintering juvenile Atlantic salmon: growth is enhanced in early migrants through lower protein turnover , 2000 .

[5]  T. Birkhead,et al.  Nestling diet, secondary sexual traits and fitness in the zebra finch , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  A. Bartke,et al.  Genes that prolong life: relationships of growth hormone and growth to aging and life span. , 2001, The journals of gerontology. Series A, Biological sciences and medical sciences.

[7]  W. Blanckenhorn The Evolution of Body Size: What Keeps Organisms Small? , 2000, The Quarterly Review of Biology.

[8]  T. Clutton‐Brock,et al.  Parental investment and sex differences in juvenile mortality in birds and mammals , 1985, Nature.

[9]  D. Wilson,et al.  Scale strength as a cost of rapid growth in sunfish , 2001 .

[10]  S. Hinsley,et al.  Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  C. Carter,et al.  A critical analysis of the role of growth hormone and IGF-1 in aging and lifespan. , 2002, Trends in genetics : TIG.

[12]  K. Gotthard Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. , 2000, The Journal of animal ecology.

[13]  H. Richner,et al.  The Effect of Extra Food on Fitness in Breeding Carrion Crows , 1992 .

[14]  Derek A. Roff,et al.  The evolution of life histories : theory and analysis , 1992 .

[15]  C. Rollo Growth negatively impacts the life span of mammals , 2002, Evolution & development.

[16]  A. Comfort,et al.  EFFECT OF DELAYED AND RESUMED GROWTH ON THE LONGEVITY OF A FISH (LEBISTES RETICULATUS, PETERS) IN CAPTIVITY. , 1963, Gerontologia.

[17]  E. Cren,et al.  Estimates of the Numbers, Biomass and Year-Class Strengths of Perch (Perca fluviatilis L.) in Windermere from 1967 to 1977 and Some Comparisons with Earlier Years , 1979 .

[18]  S. Ozanne,et al.  Early programming of glucose–insulin metabolism , 2002, Trends in Endocrinology & Metabolism.

[19]  D. Barker Fetal programming of coronary heart disease , 2002, Trends in Endocrinology & Metabolism.

[20]  J. Craig Growth and Production of the 1955 to 1972 Cohorts of Perch, Perca fluviatilis L., in Windermere , 1980 .

[21]  N. Metcalfe,et al.  Compensation for a bad start: grow now, pay later? , 2001, Trends in ecology & evolution.

[22]  I. Cuthill,et al.  Body mass regulation in response to changes in feeding predictability and overnight energy expenditure , 2000 .

[23]  J. Montani,et al.  Pathways from weight fluctuations to metabolic diseases: focus on maladaptive thermogenesis during catch-up fat , 2002, International Journal of Obesity.

[24]  N. Metcalfe,et al.  Seasonal variation in catch-up growth reveals state-dependent somatic allocations in salmon , 2002 .

[25]  S. Ludsin,et al.  FIRST‐YEAR RECRUITMENT OF LARGEMOUTH BASS: THE INTERDEPENDENCY OF EARLY LIFE STAGES , 1997 .

[26]  J. Arendt,et al.  Adaptive Intrinsic Growth Rates: An Integration Across Taxa , 1997, The Quarterly Review of Biology.

[27]  D. Reznick,et al.  The evolution of senescence in fish , 2002, Mechanisms of Ageing and Development.

[28]  Pitts Gc Cellular aspects of growth and catch-up growth in the rat: a reevaluation. , 1986 .

[29]  B. Merry,et al.  Effect of dietary restriction on aging – an update , 1995 .

[30]  R. Shine,et al.  GROWTH TO DEATH IN LIZARDS , 2002, Evolution; international journal of organic evolution.

[31]  B. J. Jennings,et al.  Nutrition, oxidative damage, telomere shortening, and cellular senescence: individual or connected agents of aging? , 2000, Molecular genetics and metabolism.