Early-late life trade-offs and the evolution of ageing in the wild

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1806, 2015, Pages

  Lemaître, Jean Francois ^a   Berger, Verane ^a   Bonenfant, Christophe ^a   Douhard, Mathieu ^b   Gamelon, Marlene ^c   Plard, Floriane ^d   Gaillard, Jean Michel ^d  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Antagonistic; Body growth; Disposable soma theory; Energy allocation theory; Life history theory; Pleiotropy theory; Senescence

Indexed keywords

AGING POPULATION; EMPIRICAL ANALYSIS; EVOLUTIONARY THEORY; FITNESS; LIFE HISTORY TRAIT; PLEIOTROPY; RESOURCE ALLOCATION; RESOURCE AVAILABILITY; SENESCENCE; SEX-RELATED DIFFERENCE; TRADE-OFF; VERTEBRATE; WILD POPULATION;

VERTEBRATA;

AGING; ANIMAL; BIRD; EVOLUTION; FEMALE; MALE; MAMMAL; PHYSIOLOGY; REPRODUCTION; REPTILE; SEXUAL DEVELOPMENT;

AGING; ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; FEMALE; MALE; MAMMALS; REPRODUCTION; REPTILES; SEX CHARACTERISTICS;

EID: 84926335539     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.0209     Document Type: Article

References (99)

1. Brommer JE, Wilson AJ, Gustafsson L. 2007 Exploring the genetics of aging in a wild passerine bird. Am. Nat. 170, 643–650. (doi:10.1086/521241)
2. Lemaˆıtre JF, Gaillard JM, Lackey LB, Clauss M, Müller DW. 2013 Comparing free-ranging and captive populations reveals intra-specific variation in aging rates in large herbivores. Exp. Gerontol. 48, 162–167. (doi:10.1016/j.exger.2012.12.004)
3. Jones OR et al. 2014 Diversity of ageing across the tree of life. Nature 505, 169–173. (doi:10.1038/nature12789)
4. Promislow DE, Fedorka KM, Burger JM. 2006 Evolutionary biology of aging: future directions. In Handbook of the biology of aging (eds EJ Masoro, SN Austad), pp. 217–242. Burlington, MA: Academic Press.
5. Nussey DH, Froy H, Lemâıtre JF, Gaillard JM, Austad SN. 2013 Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12, 214–225. (doi:10.1016/j.arr.2012.07.004)
6. Medawar PB. 1952 An unsolved problem of biology. London, UK: Lewis.
7. Hamilton WD. 1966 The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45. (doi:10.1016/0022-5193(66)90184-6)
8. Jones OR et al. 2008 Senescence rates are determined by ranking on the fast– slow life-history continuum. Ecol. Lett. 11, 664–673. (doi:10.1111/j.1461-0248.2008.01187.x)
9. Caswell H, Salguero-Gómez R. 2013 Age, stage and senescence in plants. J. Ecol. 101, 585–595. (doi:10.1111/1365-2745.12088)
10. Williams GC. 1957 Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411. (doi:10.2307/2406060)
11. Kirkwood T. 1977 Evolution of ageing. Nature 270, 301–304. (doi:10.1038/270301a0)
12. Kirkwood TB, Rose MR. 1991 Evolution of senescence: late survival sacrificed for reproduction. Phil. Trans. R. Soc. Lond. B 332, 15–24. (doi:10.1098/rstb.1991.0028)
13. Kirkwood TBL, Austad SN. 2000 Why do we age? Nature 408, 233–238. (doi:10.1038/35041682)
14. Gavrilov LA, Gavrilova NS. 2002 Evolutionary theories of aging and longevity. Sci. World J. 2, 339–356. (doi:10.1100/tsw.2002.96)
15. Robins C, Conneely KN. 2014 Testing evolutionary models of senescence: traditional approaches and future directions. Hum. Genet. 133, 1451–1465. (doi:10.1007/s00439-014-1492-7)
16. Bonduriansky R, Maklakov A, Zajitschek F, Brooks R. 2008 Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22, 443–453. (doi:10.1111/j.1365-2435.2008 01417.x)
17. Pyle P, Nur N, Sydeman WJ, Emslie SD. 1997 Cost of reproduction and the evolution of deferred breeding in the western gull. Behav. Ecol. 8, 140–147. (doi:10.1093/beheco/8.2.140)
18. Orell M, Belda EJ. 2002 Delayed cost of reproduction and senescence in the willow tit Parus montanus. J. Anim. Ecol. 71, 55–64. (doi:10.1046/j.0021-8790.2001.00575.x)
19. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P. 2003 Age-specific reproductive performance in red-billed choughs Pyrrhocorax pyrrhocorax: patterns and processes in a natural population. J. Anim. Ecol. 72, 765–776. (doi:10.1046/j.1365-2656.2003.00750.x)
20. Millon A, Petty SJ, Lambin X. 2010 Pulsed resources affect the timing of first breeding and lifetime reproductive success of tawny owls. J. Anim. Ecol. 79, 426–435. (doi:10.1111/j.1365-2656.2009.01637.x)
21. Kim SY, Velando A, Torres R, Drummond H. 2011 Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird. Oecologia 166, 615–626. (doi:10.1007/s00442-011-1914-3)
22. Reed TE, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP. 2008 Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. Am. Nat. 171, E89–E101. (doi:10.1086/524957)
23. Charmantier A, Perrins C, McCleery RH, Sheldon BC.2006 Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc. Natl Acad. Sci. USA 103, 6587–6592. (doi:10.1073/pnas.0511123103)
24. Gustafsson L, Pärt T. 1990 Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347, 279–281. (doi:10.1038/347279a0)
25. Bouwhuis S, Charmantier A, Verhulst S, Sheldon BC. 2010 Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population. J. Anim. Ecol. 79, 1251–1261. (doi:10.1111/j.1365-2656.2010.01730.x)
26. Aubry LM, Koons DN, Monnat JY, Cam E. 2009 Consequences of recruitment decisions and heterogeneity on age-specific breeding success in a long-lived seabird. Ecology 90, 2491–2502. (doi:10.1890/08-1475.1)
27. Hammers M, Richardson DS, Burke T, Komdeur J. 2013 The impact of reproductive investment and early-life environmental conditions on senescence: support for the disposable soma hypothesis. J. Evol. Biol. 26, 1999–2007. (doi:10.1111/jeb.12204)
28. Boonekamp JJ, Salomons M, Bouwhuis S, Dijkstra C, Verhulst S. 2014 Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol. Lett. 17, 599–605. (doi:10.1111/ele.12263)
29. Green WC, Rothstein A. 1991 Trade-offs between growth and reproduction in female bison. Oecologia 86, 521–527. (doi:10.1007/BF00318318)
30. Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH. 2007 Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr. Biol. 17, R1000–R1001. (doi:10.1016/j.cub.2007.10.005)
31. Nussey DH, Kruuk LE, Donald A, Fowlie M, Clutton-Brock TH. 2006 The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol. Lett. 9, 1342–1350. (doi:10.1111/j.1461-0248.2006.00989.x)
32. Lemaître JF, Gaillard JM, Pemberton JM, Clutton-Brock TH, Nussey DH. 2014 Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer. Proc. R. Soc. B 281, 20140792. (doi:10.1098/rspb.2014.0792)
33. Hadley GL, Rotella JJ, Garrott RA, Nichols JD. 2006 Variation in probability of first reproduction of Weddell seals. J. Anim. Ecol. 75, 1058–1070. (doi:10.1111/j.1365-2656.2006.01118.x)
34. Blomquist GE. 2009 Trade-off between age of first reproduction and survival in a female primate. Biol. Lett. 5, 339–342. (doi:10.1098/rsbl.2009.0009)
35. Dugdale HL, Nouvellet P, Pope LC, Burke T, Macdonald DW. 2010 Fitness measures in selection analyses: sensitivity to the overall number of offspring produced in a lifetime. J. Evol. Biol. 23, 282–292. (doi:10.1111/j.1420-9101.2009.01896.x)
36. Bérubé CH, Festa-Bianchet M, Jorgenson JT. 1999 Individual differences, longevity, and reproductive senescence in bighorn ewes. Ecology 80, 2555–2565. (doi:10.1890/0012-9658(1999)0802555:IDLARS2.0.CO;2)
37. Weladji RB, Loison A, Gaillard JM, Holand Ø, Mysterud A, Yoccoz NG, Nieminen M, Stenseth NC. 2008 Heterogeneity in individual quality overrides costs of reproduction in female reindeer. Oecologia 156, 237–247. (doi:10.1007/s00442-008-0961-x)
38. Ransome RD. 1995 Earlier breeding shortens life in female greater horseshoe bats. Phil. Trans. R. Soc. Lond. B 350, 153-161. (doi:10.1098/rstb.1995.0149)
39. Neuhaus P, Broussard DR, Murie JO, Dobson FS. 2004 Age of primiparity and implications of early reproduction on life history in female Columbian ground squirrels. J. Anim. Ecol. 73, 36–43. (doi:10.1111/j.1365-2656.2004.00793.x)
40. Descamps S, Boutin S, Berteaux D, Gaillard JM. 2006 Best squirrels trade a long life for an early reproduction. Proc. R. Soc. B 273, 2369–2374. (doi:10.1098/rspb.2006.3588)
41. Massot M, Clobert J, Montes-Poloni L, Haussy C, Cubo J, Meylan S. 2011 An integrative study of ageing in a wild population of common lizards. Funct. Ecol. 25, 848–858. (doi:10.1111/j.1365-2435.2011.01837.x)
42. Sparkman AM, Arnold SJ, Bronikowski AM. 2007 An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophis elegans. Proc. R. Soc. B 274, 943–950. (doi:10.1098/rspb.2006.0072)
43. Kawasaki N, Brassil CE, Brooks RC, Bonduriansky R. 2008 Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 172, 346–357. (doi:10.1086/589519)
44. Clutton-Brock TH, Sheldon BC. 2010 Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol. Evol. 25, 562–573. (doi:10.1016/j.tree.2010.08.002)
45. Reznick D, Ghalambor C, Nunney L. 2002 The evolution of senescence in fish. Mech. Ageing Dev. 123, 773–789. (doi:10.1016/S0047-6374(01)00423-7)
46. Rothstein HR, Sutton AJ, Borenstein M. 2006 Publication bias in meta-analysis: prevention, assessment and adjustments. Chichester, UK: John Wiley and Sons.
47. Lim JN, Senior AM, Nakagawa S. 2014 Heterogeneity in individual quality and reproductive trade-offs within species. Evolution 8, 2306–2318.
48. Wilson AJ, Nussey DH. 2010 What is individual quality? An evolutionary perspective. Trends Ecol. Evol. 25, 207–214. (doi:10.1016/j.tree.2009.10.002)
49. Gaillard JM, Sempéré AJ, Boutin JM, Van Laere GV, Boisaubert B. 1992 Effects of age and body weight on the proportion of females breeding in a population of roe deer (Capreolus capreolus). Can. J. Zool. 70, 154–1545. (doi:10.1139/z92-212)
50. Dmitriew CM. 2011 The evolution of growth trajectories: what limits growth rate? Biol. Rev. 86, 97–116. (doi:10.1111/j.1469-185X.2010.00136.x)
51. Lee WS, Monaghan P, Metcalfe NB. 2013 Experimental demonstration of the growth rate– lifespan trade-off. Proc. R. Soc. B 280, 20122370. (doi:10.1098/rspb.2012.2370)
52. Walker LC, Herndon JG. 2010 Mosaic aging. Med. Hypotheses 74, 1048–1051. (doi:10.1016/j.mehy.2009.12.031)
53. Hamel S, Gaillard JM, Yoccoz NG, Loison A, Bonenfant C, Descamps S. 2010 Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol. Lett. 13, 915–935. (doi:10.1111/j.1461-0248.2010.01478.x)
54. Van Noordwijk AJ, de Jong G. 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137–142. (doi:10.1086/284547)
55. Gaillard JM, Yoccoz NG. 2003 Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84, 3294–3306. (doi:10.1890/02-0409)
56. Bouwhuis S, Choquet R, Sheldon BC, Verhulst S. 2012 The forms and fitness cost of senescence: age-specific recapture, survival, reproduction, and reproductive value in a wild bird population. Am. Nat. 179, E15–E27. (doi:10.1086/663194)
57. Preston BT, Jalme MS, Hingrat Y, Lacroix F, Sorci G. 2011 Sexually extravagant males age more rapidly. Ecol. Lett. 14, 1017–1024. (doi:10.1111/j.1461-0248.2011.01668.x)
58. Van de Pol M, Verhulst S. 2006 Age-dependent traits: a new statistical model to separate within-and between-individual effects. Am. Nat. 167, 766–773. (doi:10.1086/503331)
59. Nussey D, Coulson T, Festa-Bianchet M, Gaillard JM. 2008 Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22, 393–406. (doi:10.1111/j.1365-2435.2008.01408.x)
60. Speakman JR, Król E. 2010 The heat dissipation limit theory and evolution of life histories in endotherms: time to dispose of the disposable soma theory? Integr. Comp. Biol. 50, 793–807. (doi:10.1093/icb/icq049)
61. Li Y, de Magalhães JP. 2013 Accelerated protein evolution analysis reveals genes and pathways associated with the evolution of mammalian longevity. Age 35, 301–314. (doi:10.1007/s11357-011-9361-y)
62. Monaghan P, Metcalfe NB, Torres R. 2009 Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75–92. (doi:10.1111/j.1461-0248.2008.01258.x)
63. Metcalfe NB, Alonso-Alvarez C. 2010 Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 24, 984–996. (doi:10.1111/j.1365-2435.2010.01750.x)
64. Selman C, Blount JD, Nussey DH, Speakman JR. 2012 Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol. Evol. 27, 570–577. (doi:10.1016/j.tree.2012.06.006)
65. Speakman JR, Garratt M. 2014 Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays 36, 93–106. (doi:10.1002/bies.201300108)
66. Nussey DH, Pemberton JM, Pilkington JG, Blount JD. 2009 Life history correlates of oxidative damage in a free-living mammal population. Funct. Ecol. 23, 809–817. (doi:10.1111/j.1365-2435.2009.01555.x)
67. Bergeron P, Careau V, Humphries MM, Reale D, Speakman JR, Garant D. 2011 The energetic and oxidative costs of reproduction in a free-ranging rodent. Funct. Ecol. 25, 1063–1071. (doi:10.1111/j.1365-2435.2011.01868.x)
68. Fletcher QE, Selman C, Boutin S, McAdam AG, Woods SB, Seo AY, Leeuwenburgh C, Speakman JR, Humphries MM. 2013 Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution 67, 1527–1536.
69. Partridge L, Barton NH. 1993 Optimality, mutation and the evolution of ageing. Nature 362, 305–311. (doi:10.1038/362305a0)
70. Charmantier A, Brommer JE, Nussey DH. 2014 Quantitative genetics of senescence in wild animals. In Quantitative genetics in the wild (eds A CharmantierD Garant, LEB Kruuk), pp. 68–83. Oxford, UK: Oxford University Press.
71. Kirkwood TB, Holliday R. 1979 The evolution of ageing and longevity. Proc. R. Soc. Lond. B 205, 53–546. (doi:10.1098/rspb.1979.0083)
72. Kirkwood TB. 2002 Evolution of ageing. Mech. Ageing Dev. 123, 737–745. (doi:10.1016/S0047-6374(01)00419-5)
73. Kirkwood TB. 2005 Understanding the odd science of aging. Cell 120, 437-447. (doi:10.1016/j.cell.2005.01.027)
74. Nussey DH, Wilson AJ, Morris A, Pemberton J, Clutton-Brock TH, Kruuk LE. 2008 Testing for genetic trade-offs between early-and late-life reproduction in a wild red deer population. Proc. R. Soc. B 275, 745–750. (doi:10.1098/rspb.2007.0986)
75. Corbo RM, Ulizzi L, Piombo L, Scacchi R. 2008 Study on a possible effect of four longevity candidate genes (ACE, PON1, PPAR-g, and APOE) on human fertility. Biogerontology 9, 317–323. (doi:10.1007/s10522-008-9143-9)
76. Cody ML. 1966 A general theory of clutch size. Evolution 20, 174–184. (doi:10.2307/2406571)
77. Stearns S. 1992 The evolution of life histories. Oxford, UK: Oxford University Press.
78. Baudisch A, Vaupel JW. 2012 Getting to the root of aging. Science 338, 618–619. (doi:10.1126/science.1226467)
79. Péron G, Crochet PA, Choquet R, Pradel R, Lebreton JD, Gimenez O. 2010 Capture–recapture models with heterogeneity to study survival senescence in the wild. Oikos 119, 524–532. (doi:10.1111/j.1600-1706.2009.17882.x)
80. Descamps S, Boutin S, Berteaux D, Gaillard JM. 2008 Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117, 1406–1416. (doi:10.1111/j.0030-1299.2008.16545.x)
81. Bouwhuis S, Charmantier A, Verhulst S, Sheldon BC. 2010 Trans-generational effects on ageing in a wild bird population. J. Evol. Biol. 23, 636–642. (doi:10.1111/j.1420-9101.2009.01929.x)
82. Millon A, Petty SJ, Little B, Lambin X. 2011 Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey. J. Anim. Ecol. 80, 968–975. (doi:10.1111/j.1365-2656.2011.01842.x)
83. Cartwright SJ, Nicoll MA, Jones CG, Tatayah V, Norris K. 2014 Anthropogenic natal environmental effects on life histories in a wild bird population. Curr. Biol. 24, 536–540. (doi:10.1016/j.cub.2014.01.040)
84. Nettle D, Frankenhuis WE, Rickard IJ. 2013 The evolution of predictive adaptive responses in human life history. Proc. R. Soc. B 280, 20131343. (doi:10.1098/rspb.2013.1343)
85. Maklakov AA, Lummaa V. 2013 Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35, 717–724. (doi:10.1002/bies.201300021)
86. Regan JC, Partridge L. 2013 Gender and longevity: why do men die earlier than women? Comparative and experimental evidence. Best Pract. Res. Clin. Endocrinol. Metab. 27, 467–479. (doi:10.1016/j. beem.2013.05.016)
87. Adler MI, Bonduriansky R. 2014 Sexual conflict, life span, and aging. Cold Spring Harb. Perspect. Biol. 6, a017566. (doi:10.1101/cshperspect.a017566)
88. Carey JR, Judge DS. 2000 Longevity records: life spans of mammals, birds, amphibians, reptiles, and fish. Odense, Denmark: Odense University Press.
89. Lemaˆıtre JF, Gaillard JM. 2013 Male survival patterns do not depend on male allocation to sexual competition in large herbivores. Behav. Ecol. 24, 421–428. (doi:10.1093/beheco/ars179)
90. Clutton-Brock TH, Isvaran K. 2007 Sex differences in ageing in natural populations of vertebrates. Proc. R. Soc. B 274, 3097–3104. (doi:10.1098/rspb.2007.1138)
91. Gamelon M et al. 2014 Do age-specific survival patterns of wild boar fit current evolutionary theories of senescence? Evolution 68, 3636–3643. (doi:10.1111/evo.12519)
92. Bobek B, Perzanowski K, Weiner J. 1990 Energy expenditure for reproduction in male red deer. J. Mammal. 71, 230–232. (doi:10.2307/1382171)
93. Tennenhouse EM, Weladji RB, Holand Ø, Røed KH, Nieminen M. 2011 Mating group composition influences somatic costs and activity in rutting dominant male reindeer (Rangifer tarandus). Behav. Ecol. Sociobiol. 65, 287–295. (doi:10.1007/s00265-010-1043-8)
94. Liker A, Székely T. 2005 Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59, 890–897. (doi:10.1111/j.0014-3820.2005.tb01762.x)
95. Andersson MB. 1994 Sexual selection. Princeton, NJ: Princeton University Press.
96. Thomson DL, Monaghan P, Furness RW. 1998 The demands of incubation and avian clutch size. Biol. Rev. 73, 293–304. (doi:10.1017/S000632319800 5180)
97. Speakman JR. 2008 The physiological costs of reproduction in small mammals. Phil. Trans. R. Soc. B 363, 375–398. (doi:10.1098/rstb.2007.2145)
98. Rubolini D et al. 2012 Sex-related effects of reproduction on biomarkers of oxidative damage in free-living barn swallows (Hirundo rustica). PLoS ONE 7, e48955. (doi:10.1371/journal.pone.0048955)
99. Cornwallis CK, Uller T. 2010 Towards an evolutionary ecology of sexual traits. Trends Ecol. Evol. 25, 145–152. (doi:10.1016/j.tree.2009.09.008)