Elephants born in the high stress season have faster reproductive ageing

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Mumby, Hannah S ^a   Mar, Khyne U ^a   Hayward, Adam D ^a,b   Htut, Win ^c   Htut Aung, Ye ^d   Lummaa, Virpi ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c FOREST RESEARCH INSTITUTE   (Myanmar)

^d Department of Veterinary Medicine Yezin University   (Myanmar)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID;

AGING; ANIMAL; ELEPHANT; FEMALE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTION; SEASON;

AGING; ANIMALS; ELEPHANTS; FEMALE; GLUCOCORTICOIDS; REPRODUCTION; SEASONS; STRESS, PHYSIOLOGICAL;

EID: 84941584849     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13946     Document Type: Article

References (63)

1. Jones, O. R. et al. Diversity of ageing across the tree of life. Nature 505, 169-173 (2014).
2. Bateson, P. et al. Developmental plasticity and human health. Nature 430, 419-421 (2004).
3. Lummaa, V. Early developmental conditions and reproductive success in humans: Downstream effects of prenatal famine, birthweight, and timing of birth. Am. J. Hum. Biol. 15, 370-379 (2003).
4. Lindström, J. Early development and fitness in birds and mammals. Trends in Ecol. Evol. 14, 343-348 (1999).
5. Munch, D., Amdam, G. V. & Wolschin, F. Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee. Funct. Ecol. 22, 407-421 (2008).
6. Keller, L. & Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958-960 (1997).
7. Brakefield, P. M. et al. What are the effects of maternal and pre-adult environments on ageing in humans, and are there lessons from animal models? Mech. Ageing Dev. 126, 431-438 (2005).
8. Bourke, A. F. G. Kin selection and the evolutionary theory of aging. Annu. Rev. Ecol. Evol. Syst. 38, 103-128 (2007).
9. Mangel, M. Environment, damage and senescence: modelling the life-history consequences of variable stress and caloric intake. Funct. Ecol. 22, 422-430 (2008).
10. Balbontn, J. & Møller, A. Environmental conditions during early life accelerate the rate of senescence in a short-lived passerine bird. Ecology 96, 948-959, (2015).
11. Nussey, D. H., Kruuk, L. E. B., Morris, A. & Clutton-Brock, T. H. Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr. Biol. 17, R1000-R1001 (2007).
12. Millon, A., Petty, S. J., Little, B. & Lambin, X. Natal conditions alter age-specific reproduction but not survival or senescence in a long-lived bird of prey. J. Anim. Ecol. 80, 968-975.
13. Descamps, S., Boutin, S., Berteaux, D., McAdam, A. G. & Gaillard, J.-M. 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 (2008).
14. McNamara, J. M., Houston, A. I., Barta, Z., Scheuerlein, A. & Fromhage, L. Deterioration, death and the evolution of reproductive restraint in late life. P. Roy. Soc. Lond. B Bio. 276, (2009).
15. Hales, C. N. & Barker, D. J. P. The thrifty phenotype hypothesis. Brit. Med. Bull. 60, 5-20 (2001).
16. Michels, K. B. et al. Birthweight as a risk factor for breast cancer. The Lancet 348, 1542-1546 (1996).
17. Rich-Edwards, J. W. et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. Brit. Med. J 315, 396-400 (1997).
18. Rickard, I. J. et al. Intergenerational effects of maternal birth season on offspring size in rural Gambia. Proc. Biol. Sci 279, 4253-4262 (2012).
19. Hayward, A. D., Rickard, I. J. & Lummaa, V. Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population. P. Natl. Acad. Sci. 110, 13886-13891 (2013).
20. Clubb, R. et al. Compromised Survivorship in Zoo Elephants. Science 322, 1649-1649 (2008).
21. Robinson, M. R., Mar, K. U. & Lummaa, V. Senescence and age-specific trade-offs between reproduction and survival in female Asian elephants. Ecol. Lett. 15, 260-266 (2012).
22. Monaghan, P., Charmantier, A., Nussey, D. H. & Ricklefs, R. E. The evolutionary ecology of senescence. Funct. Ecol. 22, 371-378 (2008).
23. Nussey, D. H., Coulson, T., Festa-Bianchet, M. & Gaillard, J. M. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22, 393-406 (2008).
24. Jones, O. R. et al. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol. Lett. 11, 664-673 (2008).
25. McCleery, R. H., Perrins, C. M., Sheldon, B. C. & Charmantier, A. Age-specific reproduction in a long-lived species: the combined effects of senescence and individual quality. P. Roy. Soc. Lond. B Bio. 275, 963-970 (2008).
26. Partridge, L. Evolutionary theories of ageing applied to long-lived organisms. Exp. Gerontol. 36, 641-650 (2001).
27. Sukumar, R. The Asian elephant: Ecology and management. Cambridge University Press (1989).
28. Sukumar, R. The living elephants: Evolutionary ecology, behavior and conservation. Oxford University Press (2003).
29. Aung, M. On the distribution, status and conservation of wild elephants in Myanmar. Gajah 18, 47-55 (1997).
30. Lueders, I. et al. Gestating for 22 months: luteal development and pregnancy maintenance in elephants. P. Roy. Soc. Lond. B Bio. 279, 3687-3696 (2012).
31. Mumby, H. S., Courtiol, A., Mar, K. U. & Lummaa, V. Birth seasonality and calf mortality in a large population of Asian elephants. Ecol. Evol. 3, 3794-3803 (2013).
32. Foley, C. A. H., Papageorge, S. & Wasser, S. K. Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conserv. Biol. 15, 1134-1142 (2001).
33. Moss, C. J., Croze, H. & Lee, P. C. (eds). The Amboseli Elephants. University of Chicago Press (2011).
34. Foley, C., Pettorelli, N. & Foley, L. Severe drought and calf survival in elephants. Biol. Lett 4, 541-544 (2008).
35. IUCN. IUCN red list of threatened species. (2014). Available at http://www.iucnredlist.org (Accessed 3rd November 2014).
36. Leimgruber, P. et al. Modeling population viability of captive elephants in Myanmar (Burma): implications for wild populations. Anim. Conserv. 11, 198-205 (2008).
37. Mumby, H. S., Courtiol, A., Mar, K. U. & Lummaa, V. Climatic variation and age-specific survival in Asian elephants from Myanmar. Ecology 94, 1131-1141 (2013).
38. Mumby, H. S. et al. Stress and body condition are associated with climate and demography in Asian elephants. Conservation Physiology 3, cov030 (2015).
39. Serrano, M. & Blasco, M. A. Putting the stress on senescence. Curr. Opin. Cell. Biol. 13, 748-753 (2001).
40. Chen, B. et al. Changes in vegetation photosynthetic activity trends across the Asia-Pacific region over the last three decades. Remote Sens. Environ. 144, 28-41 (2014).
41. Langley-Evans, S. C., Welham, S. J. M., Sherman, R. C. & Jackson, A. A. Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin. Sci. 91, 607-615 (1996).
42. Nyirenda, M. J. et al. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J. Clin. Invest. 101, 2174-2181 (1998).
43. Painter, R. C., Roseboom, T. J. & Bleker, O. P. Prenatal exposure to the Dutch famine and disease in later life: An overview. Reprod. Toxicol. 20, 345-352 (2005).
44. Pryor, J. L., Hughes, C., Foster, W., Hales, B. F. & Robaire, B. Critical windows of exposure for childrens health: the reproductive system in animals and humans. Environ. Health Perspect. 108, 491-503 (2000).
45. Oksanen, T. A., Koivula, M., Koskela, E. & Mappes, T. The cost of reproduction induced by body size at birth and breeding density. Evolution 61, 2822-2831 (2007).
46. Hayward, A. D., Mar, K. U., Lahdenperä, M. & Lummaa, V. Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants. J. Evol. Biol 27, 772-783 (2014).
47. Doblhammer, G. & Vaupel, J. W. Lifespan depends on month of birth. P. Natl. Acad. Sci. 98, 2934-2939 (2001).
48. Lummaa, V. & Tremblay, M. Month of birth predicted reproductive success and fitness in pre-modern Canadian women. P. Roy. Soc. Lond. B Bio. 270, 2355-2361 (2003).
49. Lampic, C., Svanberg, A. S., Karlström, P. & Tydén, T. Fertility awareness, intentions concerning childbearing, and attitudes towards parenthood among female and male academics. Hum. Reprod. 21, 558-564 (2006).
50. Huxley, R. et al. Is birth weight a risk factor for ischemic heart disease in later life? Am. J. Clin. Nutr. 85, 1244-1250 (2007).
51. de Bruin, J. P. et al. The role of genetic factors in age at natural menopause. Hum. Reprod. 16, 2014-2018 (2001).
52. Gluckman, P. D., Hanson, M. A. & Spencer, H. G. Predictive adaptive responses and human evolution. Trends Ecol. Evol. 20, 527-533 (2005).
53. Hayward, A. D., Nenko, I. & Lummaa, V. Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans. P. Roy. Soc. Lond. B Bio. 282 (2015).
54. Devevey, G., Bize, P., Fournier, S., Person, E. & Christe, P. Testing the predictive adaptive response in a host-parasite system. Funct. Ecol. 24, 178-185 (2010).
55. Sukumar, R. A brief review of the status, distribution and biology of wild Asian elephants - Elephas maximus. International Zoo Yearbook 40, 1-8 (2006).
56. Campos-Arceiz, A., Lin, T. Z., Htun, W., Takatsuki, S. & Leimgruber, P. Working with mahouts to explore the diet of work elephants in Myanmar (Burma). Ecol. Res. 23, 1057-1064 (2008).
57. Toke Gale, U. Burmese Timber Elephants. Trade Corportation (1974).
58. Mar, K. U. The demography and life history strategies of timber elephants in Myanmar (PhD thesis). UCL (2007).
59. Mar, K. U., Lahdenperä, M. & Lummaa, V. Causes and correlates of calf mortality in captive Asian elephants (Elephas maximus). PloS One 7, e32335 (2012).
60. de Silva, S., Webber, C. E., Weerathunga, U. S., Pushpakumara, T. V., Weerakoon, D. K. & Wittemyer, G. Demographic Variables for Wild Asian Elephants Using Longitudinal Observations. PLoS One 8, e82788 (2013).
61. Lee, P. C., Lindsay, W. K. & Moss, C. J. Ecological patterns of variability in demographic rates. In: The Amboseli Elephants (eds Moss, C. J., Croze, H. & Lee, P. C.) University of Chicago Press (2011).
62. Moss, C. J. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J. Zool 255, 145-156 (2001).
63. Watson, R. et al. Development of a versatile enzyme immunoassay for non-invasive assessment of glucocorticoid metabolites in a diversity of taxonomic species. Gen. Comp. Endocrinol 186, 16-24 (2013).