The sperm of aging male bustards retards their offspring's development

Nature Communications

Volumn 6, Issue , 2015, Pages

  Preston, Brian T ^a,d   Saint Jalme, Michel ^b   Hingrat, Yves ^c   Lacroix, Frederic ^c   Sorci, Gabriele ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c RENECO Wildlife Preservation ^*  (United Arab Emirates)

^d LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; BIRD; CAPTIVE POPULATION; DNA; EGG PRODUCTION; EVOLUTIONARY BIOLOGY; MATERNAL EFFECT; REPRODUCTION; SPERM;

AGING; ARTIFICIAL INSEMINATION; CHICK; GAMETE; GERM LINE; PREDICTION; PROGENY; SPERM; AGE; ANIMAL; BIRD; BODY SIZE; CLUTCH SIZE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS; SEMEN ANALYSIS; SPERMATOZOON; ZYGOTE;

CHLAMYDOTIS UNDULATA; OTIDIDAE;

AGE FACTORS; AGING; ANIMALS; BIRDS; BODY SIZE; CLUTCH SIZE; FEMALE; GENETIC FITNESS; INSEMINATION, ARTIFICIAL; MALE; REPRODUCTION; SEMEN ANALYSIS; SPERMATOZOA; ZYGOTE;

EID: 84946919327     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7146     Document Type: Article

References (44)

1. Rose, M. R. Evolutionary Biology of Aging (Oxford Univ. Press, 1994).
2. Jones, O. R. et al. Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol. Lett. 11, 664-673 (2008).
3. Bonduriansky, R., Maklakov, A., Zajitschek, F. & Brooks, R. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22, 443-453 (2008).
4. Monaghan, P., Charmantier, A., Nussey, D. H. & Ricklefs, R. E. The evolutionary ecology of senescence. Funct. Ecol. 22, 371-378 (2008).
5. Pizzari, T., Dean, R., Pacey, A., Moore, H. & Bonsall, M. B. The evolutionary ecology of pre- and post-meiotic sperm senescence. Trends. Ecol. Evol. 23, 131-140 (2008).
6. Nussey, D. H. et al. Inter and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am. Nat. 174, 342-357 (2009).
7. Dean, R. et al. Male reproductive senescence causes potential for sexual conflict over mating. Curr. Biol. 20, 1192-1196 (2010).
8. Garratt, M., Stockley, P., Armstrong, S. D., Beynon, R. J. & Hurst, J. L. The scent of senescence: sexual signalling and female preference in house mice. J. Ecol. Biol. 24, 2398-2409 (2011).
9. Sartorius, G. A. & Nieschlag, E. Paternal age and reproduction. Hum. Reprod. Update 16, 65-79 (2010).
10. Radwan, J. Male age, germline mutations and the benefits of polyandry. Ecol. Lett. 6, 581-586 (2003).
11. Ellegren, H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc. Biol. Sci. 274, 1-10 (2007).
12. Preston, B. T., Saint Jalme, M., Hingrat, Y., Lacroix, F. & Sorci, G. Sexually extravagant males age more rapidly. Ecol. Lett. 14, 1017-1024 (2011).
13. Loyau, A. & Lacroix, F. Watching sexy displays improves hatching success and offspring growth through maternal allocation. Proc. R. Soc. 277, 3453-3460 (2010).
14. Beamonte-Barrientos, R., Velando, A., Drummond, H. & Torres, R. Senescence of maternal effects: Aging influences egg quality and rearing capacities of a long-lived bird. Am. Nat. 175, 469-480 (2010).
15. 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).
16. White, J. et al. Multiple deleterious effects of experimentally aged sperm in a monogamous bird. Proc. Natl Acad. Sci. USA 105, 13947-13952 (2008).
17. Preston, B. T., Stevenson, I. R., Pemberton, J. M. & Wilson, K. Dominant rams lose out by sperm depletion. Nature 409, 681-682 (2001).
18. Metcalfe, N. B. & Monaghan, P. Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254-260 (2001).
19. Krist, M. Egg size and offspring quality: a meta-analysis in birds. Biol. Rev. 86, 692-716 (2011).
20. Parker, G. A. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theor. Biol. 96, 281-294 (1982).
21. Parker, G. A. Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45, 525-567 (1970).
22. Wetton, J. H. & Parkin, D. T. An association between fertility and cuckoldry in the house sparrow, Passer-domesticus. Proc. R. Soc. 245, 227-233 (1991).
23. Lesobre, L. et al. Absence of male reproductive skew, along with high frequency of polyandry and conspecific brood parasitism in the lekking Houbara bustard Chlamydotis undulata undulata. J. Avian Biol. 41, 117-127 (2010).
24. Bernardo, J. Maternal effects in animal ecology. Am. Zool. 36, 83-105 (1996).
25. Drummond, H. & Chavelas, C. G. Food shortage influences sibling aggression in the blue-footed booby. Anim. Behav. 37, 806-819 (1989).
26. Siikamaki, P. Nestling growth and mortality of Pied Flycatchers Ficedula hypoleuca in relation to weather and breeding effort. Ibis 138, 471-478 (1996).
27. Kong, A. et al. Rate of de novo mutations and the importance of father's age to disease risk. Nature 488, 471-475 (2012).
28. Ozmen, B., Koutlaki, N., Youssry, M., Diedrich, K. & Al-Hasani, S. DNA damage of human spermatozoa in assisted reproduction: origins, diagnosis, impacts and safety. Reprod. Biomed. Online 14, 384-395 (2007).
29. Zini, A., Jamal, W., Cowan, L. & Al-Hathal, N. Is sperm dna damage associated with IVF embryo quality? A systematic review. J. Assist. Reprod. Genet. 28, 391-397 (2011).
30. Horvathova, T., Nakagawa, S. & Uller, T. Strategic female reproductive investment in response to male attractiveness in birds. Proc. Biol. Sci. 279, 163-170 (2012).
31. Bogdanova, M. I., Nager, R. G. & Monaghan, P. Age of the incubating parents affects nestling survival: an experimental study of the herring gull Larus argentatus. J. Avian Biol. 38, 83-93 (2007).
32. Torres, R., Drummond, H. & Velando, A. Parental age and lifespan influence offspring recruitment: a long-term study in a seabird. PLoS ONE 6, e27245 (2011).
33. Trivers, R. L. in Sexual Selection and the Descent of Man 1871-1971. (ed Campbell, B.) 136-179 (Heinemann, 1972).
34. Manning, J. T. Choosy females and correlates of male age. J. Theor. Biol. 116, 349-354 (1985).
35. Malo, A. F., Roldan, E. R. S., Garde, J., Soler, A. J. & Gomendio, M. Antlers honestly advertise sperm production and quality. Proc. Biol. Sci. 272, 149-157 (2005).
36. Brooks, R. & Kemp, D. J. Can older males deliver the good genes? Trends Ecol. Evol. 16, 308-313 (2001).
37. Johnson, S. L. & Gemmell, N. J. Are old males still good males and can females tell the difference? Bioessays 34, 609-619 (2012).
38. Lacroix, F. The Emirates Center for Wildlife Propagation: developing a comprehensive strategy to secure a self-sustaining population of houbara bustards in eastern Morocco. Houbara News 5, 2 (2003).
39. Chargé, R. et al. Does recognized genetic management in supportive breeding prevent genetic changes in life-history traits? Evol. Appl. 7, 521-532 (2014).
40. Saint Jalme, M., Gaucher, P. & Paillat, P. Artificial insemination in houbara bustards (Chlamydotis undulata) - Influence of the number of spermatozoa and insemination frequency on fertility and ability to hatch. J. Reprod. Fertil. 100, 93-103 (1994).
41. Lake, P. E. & Ravie, O. An exploration of cryoprotective compounds for fowl spermatozoa. Br. Poult. Sci. 25, 145-150 (1984).
42. Nussey, D. H., Kruuk, L. E. B., Donald, A., Fowlie, M. & Clutton-Brock, T. H. The rate of senescence in maternal performance increases with early-life fecundity in red deer. Ecol. Lett. 9, 1342-1350 (2006).
43. Genstat 5 Committee. Genstat 5 Reference Manual (Clarendon Press, 1993).
44. McCullagh, P. & Nelder, J. A. Generalized Linear Models (Chapman and Hall, 1983).