Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird

Evolution

Volumn 69, Issue 7, 2015, Pages 1760-1771

  Bouwhuis, Sandra ^a   Vedder, Oscar ^a,b   Becker, Peter H ^a  

^a INSTITUTE OF AVIAN RESEARCH VOGELWARTE HELGOLAND   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Ageing; Fitness; Lansing effect; Life history evolution; Sexual dimorphism; Transgenerational effects

Indexed keywords

FITNESS; PARENTAGE; REPRODUCTIVE SUCCESS; SEABIRD; SENESCENCE; SEX-RELATED DIFFERENCE;

STERNA HIRUNDO;

AGING; ANIMAL; CHARADRIIFORMES; FEMALE; GENETICS; GERMANY; LONGITUDINAL STUDY; MALE; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS;

AGING; ANIMALS; CHARADRIIFORMES; FEMALE; GENETIC FITNESS; GERMANY; LONGITUDINAL STUDIES; MALE; REPRODUCTION;

EID: 84937730615     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12692     Document Type: Article

References (67)

1. Badyaev, A. V., and T. Uller 2009. Parental effects in ecology and evolution: mechanisms, processes and implications. Philos. Trans. R. Soc. B Biol. Sci. 364:1169-1177.
2. Barks, P. M., and R. A. Laird 2015. Senescence in duckweed: age-related declines in survival, reproduction and offspring quality. Funct. Ecol. 29:540-548.
3. Bauch, C., P. H. Becker, and S. Verhulst 2013. Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc. R. Soc. B Biol. Sci. 280:20122540.
4. Bauch, C. 2014. Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird. Mol. Ecol. 23:300-310.
5. Beaulieu, M., A. M. Thierry, T. Raclot, Y. Maho, Y. Ropert-Coudert, H. Gachot-Neveu, and A. Ancel 2009. Sex-specific parental strategies according to the sex of offspring in the Adelie penguin. Behav. Ecol. 20:878-883.
6. Becker, P. H., and J. D. Ludwigs 2004. Sterna hirundo common tern. Pp. 91-127 in D. Parkin, ed. Birds of the Western Palearctic. Oxford Univ. Press, Oxford, U.K.
7. Becker, P. H., and M. Wink 2003. Influences of sex, sex composition of brood and hatching order on mass growth in common terns Sterna hirundo. Behav. Ecol. Sociobiol. 54:136-146.
8. Becker, P. H., T. Dittmann, J. D. Ludwigs, B. Limmer, S. C. Ludwig, C. Bauch, A. Braasch, and H. Wendeln 2008. Timing of initial arrival at the breeding site predicts age at first reproduction in a long-lived migratory bird. Proc. Natl. Acad. Sci. USA 105:12349-12352.
9. Bonduriansky, R., and T. Day 2009. Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40:103-125.
10. Bonduriansky, R., A. J. Crean, and T. Day 2012. The implications of nongenetic inheritance for evolution in changing environments. Evol. Appl. 5:192-201.
11. Bouwhuis, S., and O. Vedder In press. Avian escape artists? Patterns, processes and costs of senescence in wild birds. In R. P. Shefferson, O. R. Jones, and R. Salguero-Gomez, eds. The evolution of senescence in the tree of life. Cambridge Univ. Press, Cambridge, U.K.
12. Bouwhuis, S., B. C. Sheldon, S. Verhulst, and A. Charmantier 2009. Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proc. R. Soc. Lond. Ser. B Biol. Sci. 276:2769-2777.
13. Bouwhuis, S., A. Charmantier, S. Verhulst, and B. C. Sheldon 2010a. Trans-generational effects on ageing in a wild bird population. J. Evol. Biol. 23:636-642.
14. Bouwhuis, S., A. J. vanNoordwijk, B. C. Sheldon, S. Verhulst, and M. E. Visser 2010b. Similar patterns of age-specific reproduction in an island and mainland population of great tits, Parus major. J. Avian Biol. 41:615-620.
15. Carnes, B. A., R. Riesch, and I. Schlupp 2012. The delayed impact of parental age on offspring mortality in mice. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 67:351-357.
16. Descamps, S., S. Boutin, D. Berteaux, and J. M. Gaillard 2008. Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117:1406-1416.
17. Ducatez, S., M. Baguette, V. M. Stevens, D. Legrand, and H. Freville 2012. Complex interactions between paternal and maternal effects: parental experience and age at reproduction affect fecundity and offspring performance in a butterfly. Evolution 66:3558-3569.
18. Ezard, T. H. G., P. H. Becker, and T. Coulson 2007. Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496-2504.
19. Foerster, K., T. Coulson, B. C. Sheldon, J. M. Pemberton, T. H. Clutton-Brock, and L. E. B. Kruuk 2007. Sexually antagonistic genetic variation for fitness in red deer. Nature 447:1107-1110.
20. Fox, C. W., M. L. Bush, and W. G. Wallin 2003. Maternal age affects offspring lifespan of the seed beetle, Callosobruchus maculatus. Funct. Ecol. 17:811-820.
21. Gavrilov, L. A., and N. S. Gavrilova 1997. Parental age at conception and offspring longevity. Rev. Clin. Gerontol. 7:5-12.
22. Gillespie, D. O. S., A. F. Russell, and V. Lummaa 2013. The effect of maternal age and reproductive history on offspring survival and lifetime reproduction in preindustrial humans. Evolution 67:1964-1974.
23. González-Solís, J., H. Wendeln, and P. H. Becker 1999. Within and between season nest-site and mate fidelity in common terns (Sterna hirundo). J. Fur Ornithol. 140:491-498.
24. Hager, R., J. M. Cheverud, L. J. Leamy, and J. B. Wolf 2008. Sex dependent imprinting effects on complex traits in mice. BMC Evol. Biol. 8.
25. Hamilton, W. D. 1966. Moulding of senescence by natural selection. J. Theor. Biol. 12:12-45.
26. Haussmann, M. F., D. W. Winkler, and C. M. Vleck 2005. Longer telomeres associated with higher survival in birds. Biol. Lett. 1:212-214.
27. Hoffman, C. L., J. P. Higham, A. Mas-Rivera, J. E. Ayala, and D. Maestripieri 2010. Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav. Ecol. 21:972-978.
28. Jablonka, E., and G. Raz 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84:131-176.
29. Jaeger, A., A. Goutte, V. J. Lecomte, P. Richard, O. Chastel, C. Barbraud, H. Weimerskirch, and Y. Cherel 2014. Age, sex, and breeding status shape a complex foraging pattern in an extremely long-lived seabird. Ecology 95:2324-2333.
30. Jones, K. S., S. Nakagawa, and B. C. Sheldon 2009. Environmental sensitivity in relation to size and sex in birds: meta-regression analysis. Am. Nat. 174:122-133.
31. Kawasaki, N., C. E. Brassil, R. C. Brooks, and R. Bonduriansky 2008. Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis. Am. Nat. 172:346-357.
32. Kemkes-Grottenthaler, A. 2004. Parental effects on off spring longevity-evidence from 17th to 19th century reproductive histories. Ann. Human Biol. 31:139-158.
33. Lecomte, V. J., G. Sorci, S. Cornet, A. Jaeger, B. Faivre, E. Arnoux, J. M. Gaillard, C. Trouvé, D. Besson, O. Chastel, et al. 2010. Patterns of aging in the long-lived wandering albatross. Proc. Natl. Acad. Sci. USA 107:6370-6375.
34. Limmer, B., and P. H. Becker 2009. Improvement in chick provisioning with parental experience in a seabird. Anim. Behav. 77:1095-1101.
35. Limmer, B. 2010. Improvement of reproductive performance with age and breeding experience depends on recruitment age in a long-lived seabird. Oikos 119:500-507.
36. Lind, M. I., E. C. Berg, G. Alavioon, and A. A. Maklakov 2015. Evolution of differential maternal age effects on male and female offspring development and longevity. Evolution 29:104-110.
37. Ludwig, S. C., and P. H. Becker 2008. Supply and demand: causes and consequences of assortative mating in common terns Sterna hirundo. Behav. Ecol. Sociobiol. 62:1601-1611.
38. Medawar, P. B. 1952. An unsolved problem in biology. H.K. Lewis & Co. Ltd, London.
39. Mousseau, T. A., and C. W. Fox 1998. The adaptive significance of maternal effects. Trends Ecol. Evol. 13:403-407.
40. Nussey, D. H., L. E. B. Kruuk, A. Donald, M. Fowlie, and T. H. Clutton-Brock 2006. The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol. Lett. 9:1342-1350.
41. Nussey, D. H., T. Coulson, M. Festa-Bianchet, and J. M. Gaillard 2008. Measuring senescence in wild animal populations: towards a longitudinal approach. Funct. Ecol. 22:393-406.
42. Olsson, M., A. Pauliny, E. Wapstra, T. Uller, T. Schwartz, and D. Blomqvist 2011. Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival. PLoS One 6.
43. Priest, N. K., B. Mackowiak, and D. E. L. Promislow 2002. The role of parental age effects on the evolution of aging. Evolution 56:927-935.
44. Rasbash, J., F. Steele, W. J. Browne, and B. Prosser 2005. A user's guide to MLwiN-version 2.0. Centre for Multilevel Modelling, University of Bristol, London, U.K.
45. Rebke, M., T. Coulson, P. H. Becker, and J. W. Vaupel 2010. Reproductive improvement and senescence in a long-lived bird. Proc. Natl. Acad. Sci. USA 107:7841-7846.
46. Rödel, H. G., D. vonHolst, and C. Kraus 2009. Family legacies: short- and long-term fitness consequences of early-life conditions in female European rabbits. J. Anim. Ecol. 78:789-797.
47. Salomons, H. M., G. A. Mulder, L. vande Zande, M. F. Haussmann, M. H. K. Linskens, and S. Verhulst 2009. Telomere shortening and survival in free-living corvids. Proc. R. Soc. B Biol. Sci. 276:3157-3165.
48. Schroeder, J., T. Burke, M. E. Mannarelli, D. A. Dawson, and S. Nakagawa 2011. Maternal effects and heritability of annual productivity. J. Evol. Biol. 25:149-156.
49. Schroeder, J., S. Nakagawa, M. Rees, M.-E. Mannarelli, and T. Burke 2015. Reduced fitness in progeny from old parents in a natural population. Proc. Natl. Acad. Sci. USA 112:4021-4025.
50. Szostek, K. L., and P. H. Becker 2012. Terns in trouble: demographic consequences of low breeding success and recruitment on a common tern population in the German Wadden Sea. J. Ornithol. 153:313-326.
51. Torres, R., H. Drummond, and A. Velando 2011. Parental age and lifespan influence offspring recruitment: a long-term study in a seabird. PLoS One 6.
52. Trivers, R. L., and D. E. Willard 1973. Natural-selection of parental ability to vary sex-ratio of offspring. Science 179:90-92.
53. Uller, T. 2006. Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios. Biol. Rev. 81:207-217.
54. vande Pol, M., and S. Verhulst 2006. Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am. Nat. 167:766-773.
55. vande Pol, M., and J. Wright 2009. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77:753-758.
56. Vedder, O., S. Bouwhuis, M. M. Benito, and P. H. Becker unpubl. ms. Sex allocation follows Fisher's principle, but changes with age, in a long-lived seabird.
57. Vigé, A., C. Gallou-Kabani, and C. Junien 2008. Sexual dimorphism in non-Mendelian inheritance. Pediatr. Res. 63:340-347.
58. Wendeln, H. 1997. Body mass of female common terns (Sterna hirundo) during courtship: relationships to male quality, egg mass, diet, laying date and age. Colon. Waterbird. 20:235-243.
59. Wendeln, H., and P. H. Becker 1999. Effects of parental quality and effort on the reproduction of common terns. J. Anim. Ecol. 68:205-214.
60. West, S. A., and B. C. Sheldon 2002. Constraints in the evolution of sex ratio adjustment. Science 295:1685-1688.
61. Wiggins, D. A., and R. D. Morris 1987. Parental care of the common tern Sterna hirundo. Ibis 129:533-540.
62. Wilkin, T. A., and B. C. Sheldon 2009. Sex differences in the persistence of natal environmental effects on life-histories. Curr. Biol. 19:1998-2002.
63. Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398-411.
64. Wolf, J. B., and M. J. Wade 2001. On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol. 14:347-356.
65. Zhang, H., M. Rebke, P. H. Becker, and S. Bouwhuis 2015a. Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird. J. Anim. Ecol. 84:199-207.
66. Zhang, H., O. Vedder, P. H. Becker, and S. Bouwhuis 2015b. Contrasting between- and within-individual trait effects on mortality risk in a long-lived seabird. Ecology 96:71-79.
67. Zhang, H., O. Vedder, P. H. Becker, and S. Bouwhuis Age-dependent trait variation: the relative contribution of within-individual change, selective appearance and disappearance in a long-lived seabird. J. Anim. Ecol. 84:797-807.