Previous investigation of our study population had already suggested age-specificity, including a late-life decline, for female recruit production at the population level (Perrins & Moss 1974
), and our replication with a sixfold larger dataset confirmed this: cross-sectionally, the number of recruits produced declines from 4 years, which encompasses on average 9 per cent of breeding females each year. The decline does not, however, provide unbiased estimates of the rate and age at onset of within-individual reproductive senescence, as it is confounded by selective disappearance. We find that females with low reproductive success cease reproduction at a younger age than females with higher reproductive success, and their disappearance from the breeding population inflates initial improvement, but partly masks senescence. Within individuals, deterioration of recruit production starts on average at the age of three, and affects 21 per cent of breeding females each year. That the process of senescence hence occurs for more than twice as many individuals as would be inferred from a cross-sectional analysis, suggests that senescence may be more common in wild populations than is often assumed.
Our finding of a positive relationship between reproductive lifespan and average annual recruit production in itself is not new (e.g. Van Noordwijk & Van Balen 1988
), but at a within-individual level it has not yet been established for a reproductive fitness measure directly affecting population dynamics. We can therefore only compare our result to ALR effects tested for underlying reproductive traits, for which the results appear equivocal. Selective disappearance was found to mask performance declines at the population level for offspring birth weight, but not calving date in red deer (Nussey et al. 2006
). Similarly, age-specific laying date and clutch size improved with ALR in mute swans (McCleery et al. 2008
), but not in barn swallows Hirundo rustica
(Balbontin et al. 2007
). Our own results for reproductive traits underlying recruitment show that, for any given age, female great tits of longer reproductive lifespan do not lay more eggs, hatch more chicks or raise more fledglings than females of shorter lifespan. That despite their seemingly similar breeding effort up to fledging, they do differ in the resulting success in terms of recruited offspring, could either reflect a negative relationship between maternal reproductive lifespan and a chick's probability of emigrating from our study population, or a positive relationship between survival of a mother and her offspring. We did not have data to relate emigration to maternal ALR directly, but we did add ALR to our model of natal dispersal distance (see electronic supplementary material, (a) and table S1). We found a significant, negative relationship (ALR: −0.32±0.12√m yr−1
=0.01), which indicates that offspring of mothers with long reproductive lifespan disperse less far within the study site. Why this is so, and whether this translates to a negative relationship between maternal ALR and a chick's probability of emigrating from the population, or whether maternal breeding dispersal and chick natal dispersal are also related remain intriguing questions for future investigation. In addition, our finding of a positive association between recruit production and reproductive lifespan, comparable to recent findings in kittiwakes Rissa tridactyl a
(Cam et al. 2002
) and four species of ungulate (Weladji et al. 2008
; Hamel et al. 2009
), raises the question of how quality differences between females are maintained. The absence of heritability of reproductive lifespan or recruit production (e.g. McCleery et al. (2004)
for our population) provides an answer, but raises the new question of how quality differences between females arise.
Unlike some bird species (e.g. black-legged kittiwakes and common gulls: Coulson & Fairweather 2001
; Rattiste 2004
), Wytham great tits show no sign of net terminal effects, either negative through terminal illness, or positive through terminal investment. Although in principle it is possible that compared to kittiwakes and gulls, great tits are too short-lived for our models to adequately separate gradual senescent effects from abrupt terminal effects, our dataset did comprise 341 females which bred at least twice after the estimated onset of senescence. With the effect size of the term LR being almost half that of the effect of age, we can therefore be confident that late-life age-specific recruit production is best characterized by a gradual, linear decline.
The finding that a substantial proportion of female great tits undergo at least one breeding season of deteriorated reproductive success because of senescence raises the question of its proximate mechanisms. We tested for within-individual age-specificity of clutch size, brood size and number of fledglings, and quantified the proportional contribution of these traits to the fitness-level senescence effect. We found significant quadratic relations that compare to those found for performance traits of other species (reviewed by Nussey et al. 2008
), although initial increases with age were followed by performance declines for brood size and number of fledglings only. The fact that clutch size peaks late and does not deteriorate with age is consistent with it not contributing to the overall senescence effect. Instead, its change with age even masked a small part of the senescent decline in recruit production. Late-life declines in brood size and fledgling number did, however, explain 12 and 39 per cent of the effect of age on recruitment respectively, leaving 49 per cent unexplained.
Half of the decline in female reproductive success with age therefore originates from egg and nestling mortality in the pre-fledging period, during which the partner could potentially alleviate female senescence effects (see Rauser et al. (2005)
for an example in Drosophila melanogaster
). The brood size effect suggests that fertilization success (Pizzari et al. 2008
), incubation behaviour (Catry et al. 2006
) or egg composition and quality might play a role. In great tits the latter two are female-specific traits (although the male may affect them via territory quality or nuptial feeding), but fertilization success mainly depends on male sperm quality, which has been shown to decline with age in wild birds (e.g. Møller et al. 2009
). Chick provisioning is also shared with the male, but little is known about age-specific provisioning behaviour in male or female birds. Detailed future study of male reproductive senescence, and interactions between male and female age-effects, will have to add to our understanding of the proximate mechanisms underlying senescence, as well as that of mate choice and sexual selection.
The remaining 49 per cent of female reproductive senescence could find its origin in the post-fledging period, where the reproductive quality difference between females of different lifespan arises too. At present, comparatively little is known about what happens during this period, as birds are much harder to individually follow, but the substantial rate of chick mortality during post-fledging care (Naef-Daenzer et al. 2001
), as well as its duration (Verhulst & Hut 1996
) suggest that there is ample scope for further parental age effects. Fledgling condition may play a role too, although in our study fledgling mass was independent of maternal age (S. Bouwhuis, B. C. Sheldon, S. Verhulst & A. Charmantier 2009, unpublished analysis). Either way, its importance for senescence and individual quality does call for further investigation of this reproductive phase.
In conclusion, our results illustrate the importance of modelling individual variation in the study of senescence, show an important part of females in our population to undergo late-life declines in reproductive success, and point to the stages at which this effect is most strongly expressed. This contradicts early ideas that senescence is negligible in wild birds (Holmes et al. 2003
), but confirms its ubiquity in a range of vertebrate species (Jones et al. 2008