A long‐term study of reproductive performance in tree swallows: the influence of age and senescence on output

Robertson, Raleigh J.; Rendell, Wallace B.

doi:10.1046/j.0021-8790.2001.00555.x

Cited by 119 publications

(116 citation statements)

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“…We used a factorial experimental design with one factor being adult female age (young, 1 year; mid-age, 2 and 3 years; old, 4 years and older), following the age categories used by Robertson and Rendell (2001). Only individuals that could be unambiguously classified into these age categories based on their banding history were included in the experiment.…”

Section: Field Experimentsmentioning

confidence: 99%

“…Tree Swallows are small (;20 g) passerine birds in the family Hirundinidae and are widespread in North America (Robertson et al 1992). Although most individuals live only two to three years in the wild, the maximum reported lifespan for the species is 12 years (Robertson and Rendell 2001). Tree Swallows constitute an ideal system to study the costs of immunosenescence because we have already demonstrated that individuals in our study population show immunosenescence in the in vivo skin swelling (Haussmann et al 2005) and the in vitro lymphocyte proliferation (Palacios et al 2007) responses to phytohemagglutinin (PHA, a common mitogen that stimulates T-lymphocytes), with immune function decreasing steadily with age in adults ranging from 1 to 8 years of age.…”

Section: Introductionmentioning

confidence: 99%

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Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows

Palacios

Winkler

Klasing

et al. 2011

Ecology

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Immunosenescence, the aging of the immune system, is well documented in humans and laboratory models and is known to increase infection risk, morbidity, and mortality among the old. Immunosenescence patterns have recently been unveiled in various free-living populations, but their consequences in the wild have not been explored. We investigated the consequences of immunosenescence in free-living Tree Swallows Tachycineta bicolorthrough a field experiment simulating a bacterial infection (challenge with lipopolysaccharide, LPS) in females of different ages during the nestling rearing period. We assessed behavioral and physiological responses of females, as well as growth and quality of their offspring, to determine the costs associated with the simulated infection. Results of the experiment differed between the two years of study. In the first year, old females challenged with LPS lost more body mass and reduced their nest visitation rates more, and their offspring tended to grow slower compared to similarly challenged younger females. In contrast, in the second year, old females did not appear to suffer larger costs than younger ones. Interestingly, immunosenescence was only detected during the first year of the study, suggesting that it is the dysregulated immune function characteristic of immunosenescent individuals rather than age per se that can lead to higher costs of immune defense in old individuals. These results provide the first evidence of costs of immunosenescence in free-living animals and support the hypothesis that old, immunosenescent individuals pay higher costs than younger ones when faced with a challenge to their immune system. Our results also suggest that these costs are mediated by an exaggerated sickness behavior, as seen in laboratory models, and can be modulated by ecological factors such as weather conditions and food availability. Abstract. Immunosenescence, the aging of the immune system, is well documented in humans and laboratory models and is known to increase infection risk, morbidity, and mortality among the old. Immunosenescence patterns have recently been unveiled in various free-living populations, but their consequences in the wild have not been explored. We investigated the consequences of immunosenescence in free-living Tree Swallows Tachycineta bicolor through a field experiment simulating a bacterial infection (challenge with lipopolysaccharide, LPS) in females of different ages during the nestling rearing period. We assessed behavioral and physiological responses of females, as well as growth and quality of their offspring, to determine the costs associated with the simulated infection. Results of the experiment differed between the two years of study. In the first year, old females challenged with LPS lost more body mass and reduced their nest visitation rates more, and their offspring tended to grow slower compared to similarly challenged younger females. In contrast, in the second year, old females did not appear to suffer larger costs than younger ones. Int...

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Section: Field Experimentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows

Palacios

Winkler

Klasing

et al. 2011

Ecology

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“…Recently, several studies demonstrating senescence in free-living organisms through measurements of age-dependent mortality, reproduction and reproductive value have been published [e.g., Gustafsson and Pärt (1990); Perdeck and Cavé (1992); Newton and Rothery (1997); Bérubé et al (1999); Møller and de Lope (1999); Espie et al (2000); Sanz and Moreno (2000); Pyle et al (2001); Robertson and Rendell (2001); Cam et al (2002); Laaksonen et al (2002); Orell and Belda (2002); Reid et al (2003)]. Several of these studies have investigated patterns of age-specific fecundity and mortality, showing how reproductive performance and survival late in life are related to early performance.…”

Section: Introductionmentioning

confidence: 99%

Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: A study of avian ‘centenarians’

Møller

Lope

Saino

2005

AGE

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A. P. Moller, F. de Lope and N. Saino: Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: A study of avian Fcentenarians_. Senescence reflects the decrease in age-dependent residual reproductive value, and a previous study of a cohort of migratory barn swallows (Hirundo rustica) that had reached advanced ages for this species (at least five years old) provided evidence consistent with senescence such as reduced reproductive performance and increased abundance of parasites. We studied a population of migratory barn swallows over a number of years. Several questions were asked including 1) how do longer lived birds compare to shorter lived individuals of the same species, 2) is there a difference in individuals of the same species that live in different geographical regions, and 3) how do patterns of reproduction change during aging? We compared the phenotypes of 87 individuals from three populations in Denmark, Italy and Spain that had reached at least five years old with those of control individuals matched for sex, arrival date and breeding site. These controls only became one year old, i.e., they were not found thereafter and both groups of individuals were compared in their first year of life. Results showed that there were no significant differences in any of 11 morphological characters or in the abundance of three ectoparasites between the two groups of birds. Females that eventually became very old had relatively smaller first clutches as one year olds than did one year old controls, while males that eventually became very old had mates that laid clutches that were relatively larger than those of controls. Annual fecundity showed a similar pattern, with an increased sex difference in fecundity between birds from Spain than in Italy and in Denmark. Danish barn swallows that achieved older ages had relatively lower haematocrits than control individuals of the same sex, age and arrival date captured at the same site, while the difference in haematocrits between these two categories of individuals was small for Italian birds. Spring arrival date was relatively earlier in Danish males that eventually became very old compared to control males of the same age and tail length (a correlate of fitness) that arrived at the same site, while the two age categories of females did not differ in arrival date. In the Spanish population there was no difference in arrival date between the birds that aged most successfully and controls for either sex. We will discuss these findings in relation to current senescence theories.

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“…The rapidly growing literature on senescence in wild animal populations provides evidence for divergent aging patterns in female reproductive traits (48). Numerous studies of mammals, birds, and reptiles have presented simultaneous age-dependent estimates of female fecundity as well as estimates of offspring survival in mammals (11,20,24,49,50), birds (21,23,(51)(52)(53)(54), and reptiles (22,55). However, very few have formally compared the patterns of aging between these two measures.…”

Section: Discussionmentioning

confidence: 99%

“…Although observations suggest that maternal effect senescence may not proceed at the same rate as fertility senescence (12,(20)(21)(22)(23)(24), there is no evolutionary theory yet capable of explaining maternal effect senescence or its distinction from fertility senescence. Biologists have assumed that the age-related decline in selection that shapes fertility and survival generalizes to traits under the influence of IGEs, including maternal effects.…”

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confidence: 99%

Evolution of maternal effect senescence

Moorad

Nussey

2015

Proc. Natl. Acad. Sci. U.S.A.

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Increased maternal age at reproduction is often associated with decreased offspring performance in numerous species of plants and animals (including humans). Current evolutionary theory considers such maternal effect senescence as part of a unified process of reproductive senescence, which is under identical age-specific selective pressures to fertility. We offer a novel theoretical perspective by combining William Hamilton's evolutionary model for aging with a quantitative genetic model of indirect genetic effects. We demonstrate that fertility and maternal effect senescence are likely to experience different patterns of age-specific selection and thus can evolve to take divergent forms. Applied to neonatal survival, we find that selection for maternal effects is the product of age-specific fertility and Hamilton's age-specific force of selection for fertility. Population genetic models show that senescence for these maternal effects can evolve in the absence of reproductive or actuarial senescence; this implies that maternal effect aging is a fundamentally distinct demographic manifestation of the evolution of aging. However, brief periods of increasingly beneficial maternal effects can evolve when fertility increases with age faster than cumulative survival declines. This is most likely to occur early in life. Our integration of theory provides a general framework with which to model, measure, and compare the evolutionary determinants of the social manifestations of aging. Extension of our maternal effects model to other ecological and social contexts could provide important insights into the drivers of the astonishing diversity of lifespans and aging patterns observed among species.S enescence is the age-related deterioration of organismal function and fitness. Evolutionary theory explains its pervasiveness as the result of age-related declines in the strength of natural selection to preserve survival and reproduction (1). Genes deleterious to survival or fertility in late life can persist or even come to fixation as a result of this weakening of selection in old age (2-4). To date, most theoretical and empirical research into the evolution of senescence has focused on age-specific survival and fertility (vital rates), as these rates are most proximate to fitness. Both age-related declines in survival (actuarial senescence) and fertility (reproductive senescence) can evolve independently from initially nonsenescent life histories (1).These vital rates are a product of complex interactions among different physiological systems, phenotypic traits, and their environment. One important source of environmental contributions involves social interactions. The influence of other individuals in the environment on a particular phenotype can itself be heritable, and the importance of these so-called "indirect genetic effects" (IGEs) is now established within evolutionary biology (5-7). IGEs are known to readily alter the evolutionary predictions of standard quantitative genetic models incorporating only direct genetic ...

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A long‐term study of reproductive performance in tree swallows: the influence of age and senescence on output

Cited by 119 publications

References 94 publications

Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows

Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows

Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: A study of avian ‘centenarians’

Evolution of maternal effect senescence

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