Parental Age and Lifespan Influence Offspring Recruitment: A Long-Term Study in a Seabird

Recent studies of wild populations provide compelling evidence that survival and reproduction decrease with age because of senescence, a decline in functional capacities at old ages. However, in the wild, little is known about effects of parental senescence on offspring quality. We used data from a 21-year study to examine the role of parental age on offspring probability of recruitment in a long-lived bird, the blue-footed booby (Sula nebouxii). Offspring probability of recruiting into the breeding population varied over the life of parents and effects age were similar in mothers and fathers. Offspring recruitment was high when parents were roughly 6–12 years old and low before and after then. Effects of parental age on offspring recruitment varied with lifespan (parental age at last reproduction) and previous breeding experience. Offspring recruitment from young and old parents with long reproductive lifespans was greater than that of offspring from parents with short lifespans at young and old ages. For parents with little previous breeding experience recruitment of offspring decreased with their hatch date, but experienced parents were no similarly affected. We found evidence of terminal effects on offspring recruitment in young parents but not in older parents, suggesting that senescence is more likely a gradual process of deterioration than a process of terminal illness. Failure to recruit probably reflects mortality during the first years after independence but also during the fledgling transition to full independence. Our results show effects of parental age and quality on offspring viability in a long-lived wild vertebrate and support the idea that wild populations are composed of individuals of different quality, and that this individual heterogeneity can influence the dynamics of age-structured populations.

[1]  G. Williams Adaptation and Natural Selection , 2018 .

[2]  H. Drummond,et al.  Senescent males carry premutagenic lesions in sperm , 2011, Journal of evolutionary biology.

[3]  H. Drummond,et al.  Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird , 2011, Oecologia.

[4]  H. Drummond,et al.  Evolvability of an avian life history trait declines with father’s age , 2011, Journal of evolutionary biology.

[5]  E. Bignal,et al.  Parent age, lifespan and offspring survival: structured variation in life history in a wild population. , 2010, The Journal of animal ecology.

[6]  D. Oro,et al.  Climatic influence on demographic parameters of a tropical seabird varies with age and sex. , 2010, Ecology.

[7]  B. Sheldon,et al.  Trans‐generational effects on ageing in a wild bird population , 2010, Journal of evolutionary biology.

[8]  H. Drummond,et al.  Senescence of Maternal Effects: Aging Influences Egg Quality and Rearing Capacities of a Long‐Lived Bird , 2010, The American Naturalist.

[9]  A. Houston,et al.  Deterioration, death and the evolution of reproductive restraint in late life , 2009, Proceedings of the Royal Society B: Biological Sciences.

[10]  B. Sheldon,et al.  Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle , 2009, Proceedings of the Royal Society B: Biological Sciences.

[11]  J. Balthazart,et al.  Local adaptation of timing of reproduction: females are in the driver's seat , 2009 .

[12]  A. MØller,et al.  Senescent sperm performance in old male birds , 2009, Journal of evolutionary biology.

[13]  R. Pradel,et al.  THE COST OF REPRODUCTION AND EXPERIENCE-DEPENDENT VITAL RATES IN A SMALL PETREL. , 2008, Ecology.

[14]  A. Velando,et al.  Avoiding bad genes: oxidatively damaged DNA in germ line and mate choice. , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[15]  E. Danchin,et al.  Multiple deleterious effects of experimentally aged sperm in a monogamous bird , 2008, Proceedings of the National Academy of Sciences.

[16]  J. Gaillard,et al.  Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence , 2008 .

[17]  J. Gaillard,et al.  Senescence rates are determined by ranking on the fast-slow life-history continuum. , 2008, Ecology letters.

[18]  R. Ricklefs The evolution of senescence from a comparative perspective , 2008 .

[19]  J. Gaillard,et al.  Measuring senescence in wild animal populations: towards a longitudinal approach , 2008 .

[20]  C. Perrins,et al.  Age-specific reproduction in a long-lived species: the combined effects of senescence and individual quality , 2008, Proceedings of the Royal Society B: Biological Sciences.

[21]  Christopher M. Perrins,et al.  THE TIMING OF BIRDS‘ BREEDING SEASONS , 2008 .

[22]  E. Curio Why de young birds reproduce less well , 2008 .

[23]  M. Bonsall,et al.  The evolutionary ecology of pre- and post-meiotic sperm senescence. , 2008, Trends in ecology & evolution.

[24]  A. N. Bozcuk,et al.  Maternal age effects on longevity in Drosophila melanogaster populations of different origin , 2008, Biogerontology.

[25]  L. Kruuk,et al.  Reproductive Senescence in a Long‐Lived Seabird: Rates of Decline in Late‐Life Performance Are Associated with Varying Costs of Early Reproduction , 2008, The American Naturalist.

[26]  Linda Partridge,et al.  Benchmarks for ageing studies , 2007, Nature.

[27]  A. Velando,et al.  Male reproductive senescence: the price of immune-induced oxidative damage on sexual attractiveness in the blue-footed booby. , 2007, The Journal of animal ecology.

[28]  S. Wulff SAS for Mixed Models , 2007 .

[29]  H. Weimerskirch,et al.  Age, experience and reproductive performance in a long-lived bird: a hormonal perspective , 2007, Behavioral Ecology and Sociobiology.

[30]  L. Kruuk,et al.  The rate of senescence in maternal performance increases with early-life fecundity in red deer. , 2006, Ecology letters.

[31]  R. Phillips,et al.  Senescence effects in an extremely long-lived bird: the grey-headed albatross Thalassarche chrysostoma , 2006, Proceedings of the Royal Society B: Biological Sciences.

[32]  H. Drummond,et al.  Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis , 2006, Proceedings of the Royal Society B: Biological Sciences.

[33]  Rivka L. Glaser,et al.  Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Verhulst,et al.  Age‐Dependent Traits: A New Statistical Model to Separate Within‐ and Between‐Individual Effects , 2006, The American Naturalist.

[35]  J. Tower,et al.  Stem cell aging in the Drosophila ovary , 2005, AGE.

[36]  A. Baudisch Hamilton's indicators of the force of selection. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  H. Weimerskirch,et al.  ENVIRONMENTAL CONDITIONS AND BREEDING EXPERIENCE AFFECT COSTS OF REPRODUCTION IN BLUE PETRELS , 2005 .

[38]  K. Rattiste,et al.  Reproductive success in presenescent common gulls (Larus canus): the importance of the last year of life , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  T. Nikola,et al.  The short-term and long-term effects of parental age in the bean weevil (Acanthoscelides obtectus) , 2004, Evolutionary Ecology.

[40]  P. J. Moore,et al.  Is a decline in offspring quality a necessary consequence of maternal age? , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  A. Velando,et al.  Differential body condition regulation by males and females in response to experimental manipulations of brood size and parental effort in the blue‐footed booby , 2003 .

[42]  E. Bignal,et al.  Age‐specific reproductive performance in red‐billed choughs Pyrrhocorax pyrrhocorax: patterns and processes in a natural population , 2003 .

[43]  V. V. Krishnan,et al.  Buffered Development: Resilience after Aggressive Subordination in Infancy , 2003, The American Naturalist.

[44]  Nicholas K. Priest,et al.  THE ROLE OF PARENTAL AGE EFFECTS ON THE EVOLUTION OF AGING , 2002, Evolution; international journal of organic evolution.

[45]  I. Owens,et al.  Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction , 2002 .

[46]  T. Pärt Experimental evidence of environmental effects on age–specific reproductive success: the importance of resource quality , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  P. Thompson,et al.  Lagged effects of ocean climate change on fulmar population dynamics , 2001, Nature.

[48]  S. Stearns,et al.  DECLINE IN OFFSPRING VIABILITY AS A MANIFESTATION OF AGING IN DROSOPHILA MELANOGASTER , 2001, Evolution; international journal of organic evolution.

[49]  J. Coulson,et al.  Reduced reproductive performance prior to death in the Black-legged Kittiwake: senescence or terminal illness? , 2001 .

[50]  Leonard Hayflick,et al.  The future of ageing , 2000, Nature.

[51]  Steven N. Austad,et al.  Why do we age? , 2000, Nature.

[52]  F. Pirchner Genetics and Analysis of Quantitative Traits. , 2000 .

[53]  A. Velando The importance of hatching date for dominance in young shags , 2000, Animal Behaviour.

[54]  E. Cam,et al.  Apparent inferiority of first‐time breeders in the kittiwake: the role of heterogeneity among age classes , 2000 .

[55]  H. Drummond,et al.  Does large size make daughters of the blue‐footed booby more expensive than sons? , 1999 .

[56]  W. Ewens Genetics and analysis of quantitative traits , 1999 .

[57]  Michael P. Harris,et al.  Experimental evidence that age-specific reproductive success is independent of environmental effects , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  E. Jones,et al.  Aging and reproductive potential in women. , 1998, The Yale journal of biology and medicine.

[59]  J. Komdeur Influence of age on reproductive performance in the Seychelles warbler , 1996 .

[60]  D. Price,et al.  Good genes and old age: Do old mates provide superior genes? , 1995 .

[61]  H. Drummond,et al.  NATAL DISPERSAL AND DEFERRED BREEDING IN THE BLUE-FOOTED BOOBY , 1993 .

[62]  Thomas E. Johnson,et al.  Evolutionary biology of aging , 1990 .

[63]  James N. M. Smith,et al.  Effects of Age and Breeding Experience on Seasonal Reproductive Success in the Song Sparrow , 1987 .

[64]  T. Clutton‐Brock,et al.  Reproductive Effort and Terminal Investment in Iteroparous Animals , 1984, The American Naturalist.

[65]  W. J. Smith,et al.  The Sulidae: Gannets and Boobies , 1979 .

[66]  W. Hamilton The moulding of senescence by natural selection. , 1966, Journal of theoretical biology.

[67]  T. Clutton‐Brock,et al.  Reproductive senescence in a cooperatively breeding mammal. , 2010, The Journal of animal ecology.

[68]  H. Drummond,et al.  Simultaneous positive and negative density-dependent dispersal in a colonial bird species. , 2009, Ecology.

[69]  P. Vergara,et al.  Younger, weaker white stork (Ciconia ciconia) nestlings become the best breeders , 2007 .

[70]  H. Drummond,et al.  Lifetime Philopatry in the Blue-footed Booby: a Longitudinal Study , 2007 .

[71]  Jean-Dominique Lebreton,et al.  Recruitment to a seabird population depends on environmental factors and on population size. , 2006, The Journal of animal ecology.

[72]  M. West-Eberhard Developmental plasticity and evolution , 2003 .

[73]  Jan‐Åke Nilsson Fitness consequences of timing of reproduction , 1999 .

[74]  D. Srivastava Using local–regional richness plots to test for species saturation: pitfalls and potentials , 1999 .

[75]  C. Fox,et al.  Maternal effects as adaptations , 1998 .

[76]  H. Drummond,et al.  Reversed Sexual Size Dimorphism and Parental Care: Minimal Division of Labour in the Blue-Footed Booby , 1995 .

[77]  S. Daan,et al.  Family Planning in the Kestrel (Falco tinnunculus) , 1990 .

[78]  S. Daan,et al.  Family Planning in the Kestrel (Falco tinnunculus): The Ultimate Control of Covariation of Laying Date and Clutch Size , 1990 .