Sex differences in senescence: The role of intra-sexual competition in early adulthood

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1811, 2015, Pages

  Beirne, Christopher ^a   Delahay, Richard ^b   Young, Andrew ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Ageing; Disposable soma; Individual variation; Mammal; Senescence; Wild population

Indexed keywords

ADAPTATION; AGE; COMPETITION (ECOLOGY); INDIVIDUAL VARIATION; INTRASEXUAL INTERACTION; MUSTELID; PARENTAL INVESTMENT; REPRODUCTIVE COST; SENESCENCE; SEX-RELATED DIFFERENCE; WILD POPULATION;

MAMMALIA; MELES MELES;

AGING; ANIMAL; COMPETITIVE BEHAVIOR; ENGLAND; FEMALE; LONGITUDINAL STUDY; MALE; MUSTELIDAE; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

AGING; ANIMALS; COMPETITIVE BEHAVIOR; ENGLAND; FEMALE; LONGITUDINAL STUDIES; MALE; MUSTELIDAE; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84937598310     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.1086     Document Type: Article

References (50)

1. Nussey DH, Froy H, Lemaitre JFJ, 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)
2. Maklakov A, Lummaa V. 2013 Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35, 717–724. (doi:10.1002/bies.201300021)
3. 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)
4. Promislow D. 1992 Costs of sexual selection in natural populations of mammals. Proc. R. Soc. Lond. B 247, 203–210.(doi:10.1098/rspb.1992.0030)
5. Nussey DH, Kruuk LEB, Morris A, Clements MN, Pemberton JM, Clutton-Brock TH. 2009 Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am. Nat. 174, 342–357. (doi:10.1086/603615)
6. 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)
7. Tafani M, Cohas A, Bonenfant C, Gaillard JM, Lardy S, Allaine D. 2012 Sex-specific senescence in body mass of a monogamous and monomorphic mammal: the case of Alpine marmots. Oecologia 172, 427–436. (doi:10.1007/s00442-012-2499-1)
8. Barrett ELB, Richardson DS. 2011 Sex differences in telomeres and lifespan. Aging Cell 44, 913–921. (doi:10.1111/j.1474-9726.2011.00741.x)
9. Lemaıtre JF, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard JM. 2015 Early-late life trade-offs and the evolution of ageing in the wild. Proc. R. Soc. B 282, 20150209. (doi:10.1098/rspb.2015.0209)
10. Williams G. 1957 Pleiotropy, natural selection, and the evolution of senescence. Evolution. 11, 398–411. (doi:10.2307/2406060)
11. Kirkwood TB. 1977 Evolution of ageing. Nature 270, 301–304. (doi:10.1038/270301a0)
12. Andersson MB. 1994 Sexual selection. Princeton, NJ: Princeton University Press.
13. Graves BM. 2007 Sexual selection effects on the evolution of senescence. Evol. Ecol. 21, 663–668. (doi:10.1007/s10682-006-9144-6)
14. 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)
15. Sharp SP, Clutton-Brock TH. 2011 Competition, breeding success and ageing rates in female meerkats. J. Evol. Biol. 24, 1756–1762. (doi:10.1111/j.1420-9101.2011.02304.x)
16. 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)
17. Gaillard JM, Festa-Bianchet M, Delorme D, Jorgenson J. 2000 Body mass and individual fitness in female ungulates: bigger is not always better. Proc. R. Soc. Lond. B 267, 471–477. (doi:10.1098/rspb.2000.1024)
18. Bérubé C, Festa-Bianchet M, Jorgenson J. 1999 Individual differences, longevity, and reproductive senescence in bighorn ewes. Ecology 80, 2555–2565. (doi:10.1890/0012-9658(1999)080[2555:IDLARS]2.0.CO;2)
19. Nussey DH, Coulson T, Delorme D, Clutton-Brock TH, Pemberton JM, Festa-Bianchet M, Gaillard JM. 2011 Patterns of body mass senescence and selective disappearance differ among three species of freeliving ungulates. Ecology 92, 1936–1947. (doi:10.1890/11-0308.1)
20. Mysterud A, Solberg EJ, Yoccoz NG. 2005 Ageing and reproductive effort in male moose under variable levels of intrasexual competition. J. Anim. Ecol. 74, 742–754. (doi:10.1111/j.1365-2656.2005.00965.x)
21. Woodroffe R, MacDonald DW. 1995 Female/female competition in European badgers Meles meles: effects on breeding success. J. Anim. Ecol. 64, 12–20. (doi:10.2307/5823)
22. Dugdale H, Griffiths A, Macdonald D. 2011 Polygynandrous and repeated mounting behaviour in European badgers, Meles meles. Anim. Behav. 82, 1287–1297. (doi:10.1016/j.anbehav.2011.09.008)
23. Macdonald DW, Newman C, Buesching CD, Nouvellet P. 2010 Are badgers ‘under the weather’? Direct and indirect impacts of climate variation on European badger (Meles meles) population dynamics. Glob. Chang. Biol. 16, 2913–2922. (doi:10.1111/j.1365-2486.2010.02208.x)
24. Dugdale HL, Pope LC, Newman C, Macdonald DW, Burke T. 2011 Age-specific breeding success in a wild mammalian population: selection, constraint, restraint and senescence. Mol. Ecol. 20, 3261–3274. (doi:10.1111/j.1365-294X.2011.05167.x)
25. Mcdonald JL, Smith GC, Mcdonald RA, Delahay RJ, Hodgson D. 2014 Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife–disease interactions. Proc. R. Soc. B 281, 20140526. (doi:10.1098/rspb.2014.0526)
26. Dugdale HL, Macdonald DW, Pope LC, Burke T. 2007 Polygynandry, extra-group paternity and multiplepaternity litters in European badger (Meles meles) social groups. Mol. Ecol. 16, 5294–5306. (doi:10.1111/j.1365-294X.2007.03571.x)
27. Annavi G, Newman C, Dugdale HL, Buesching CD, Sin YW, Burke T, Macdonald DW. 2014 Neighbouring-group composition and within-group relatedness drive extra-group paternity rate in the European badger (Meles meles). J. Evol. Biol. 27, 2191–2203. (doi:10.1111/jeb.12473)
28. Dugdale H, Macdonald D, Pope L. 2008 Reproductive skew and relatedness in social groups of European badgers, Meles meles. Mol. Ecol. 17, 1815–1827. (doi:10.1111/j.1365-294X.2008.03708.x)
29. Delahay RJ, Walker NJ, Forrester GJ. 2006 Demographic correlates of bite wounding in Eurasian badgers, Meles meles L, in stable and perturbed populations. Anim. Behav. 71, 1047–1055. (doi:10.1016/j.anbehav.2005.07.018)
30. Graham J, Smith GC, Delahay RJ, Bailey T, McDonald RA, Hodgson D. 2013 Multi-state modelling reveals sexdependent transmission, progression and severity of tuberculosis in wild badgers. Epidemiol. Infect. 141, 1429–1436. (doi:10.1017/S0950268812003019)
31. 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)
32. Van De Pol M, Verhulst S. 2006 Age-dependent traits: a new statistical model to separate withinand between-individual effects. Am. Nat. 167, 766–773. (doi:10.1086/503331)
33. Delahay RJ, Brown JA, Mallinson PJ, Spyvee PD, Handoll D, Rogers LM, Cheeseman CL. 2000 The use of marked bait in studies of the territorial organization of the European badger (Meles meles). Mamm. Rev. 30, 73–87. (doi:10.1046/j.1365-2907.2000.00058.x)
34. Tomlinson AJ, Chambers M, Wilson GJ, McDonald RA, Delahay RJ. 2013 Sex-related heterogeneity in the life-history correlates of Mycobacterium bovis infection in European badgers (Meles meles). Transbound. Emerg. Dis. 60, 37–45. (doi:10.1111/tbed.12097)
35. Roper TJ. 2010 Badger. London, UK: Collins.
36. Bates DM. 2005 Fitting linear mixed models in R. R News. 5, 27–31.
37. R Development Core Team. 2007 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
38. Delahay RJ, Carter SP, Forrester GJ, Mitchell A, Cheeseman CL. 2006 Habitat correlates of group size, bodyweight and reproductive performance in a high-density Eurasian badger (Meles meles) population. J. Zool. 270, 437–447. (doi:10.1111/j.1469-7998.2006.00165.x)
39. Hämäläinen A et al. 2014 Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate. Proc. R. Soc. B 281, 20140830. (doi:10.1098/rspb.2014.0830)
40. Froy H, Phillips RA, Wood AG, Nussey DH, Lewis S. 2013 Age-related variation in reproductive traits in the wandering albatross: evidence for terminal improvement following senescence. Ecol. Lett. 16, 642–649. (doi:10.1111/ele.12092)
41. Burnham K, Anderson DR. 2002 Model selection and multi-model inference: a practical informationtheoretic approach. Berlin, Germany: Springer.
42. Richards S, Whittingham M, Stephens P. 2011 Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav. Ecol. Sociobiol. 65, 77–89. (doi:10.1007/s00265-010-1035-8)
43. Nakagawa S, Schielzeth H. 2013 A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142. (doi:10.1111/j.2041-210x.2012.00261.x)
44. Macdonald D, Newman C, Stewart P, Domingo- Roura X, Johnson PJ. 2002 Density-dependent regulation of body mass and condition in badgers (Meles meles) from Wytham Woods. Ecology 83, 2056–2061. (doi:10.1890/0012-9658(2002)083[2056:DDROBM]2.0.CO;2)
45. Robertson A, McDonald RA, Delahay RJ, Kelly SD, Bearhop S. 2014 Individual foraging specialisation in a social mammal: the European badger (Meles meles). Oecologia 176, 409–421. (doi:10.1007/s00442-014-3019-2)
46. Rogers LM, Delahay R, Cheeseman CL, Langton S, Smith GC, Clifton-Hadley RS. 1998 Movement of badgers (Meles meles) in a high-density population: individual, population and disease effects. Proc. R. Soc. Lond. B 265, 1269–1276. (doi:10.1098/rspb.1998.0429)
47. Rogers L, Cheeseman C, Langton S. 1997 Body weight as an indication of density-dependent population regulation in badgers (Meles meles) at Woodchester Park, Gloucestershire. J. Zool. 242, 597–604. (doi:10.1111/j.1469-7998.1997.tb03857.x)
48. Stockley P, Campbell A. 2013 Female competition and aggression: interdisciplinary perspectives. Phil. Trans. R. Soc. B 368, 20130073. (doi:10.1098/rstb.2013.0073)
49. Cant M, Young A. 2013 Resolving social conflict among females without overt aggression. Phil. Trans. R. Soc. B 368, 20130076. (doi:10.1098/rstb.2013.0076)
50. Young A, Bennett NC. 2013 Intra-sexual selection in cooperative mammals and birds: why are not females bigger and better armed? Phil. Trans. R. Soc. B 368, 20130075. (doi:10.1098/rstb.2013.0075)