Correction: Reproductive aging and age-dependent parental effects on offspring in a long-lived seabird.

Reproductive aging is a widespread process in wild populations, affecting both females and males across many species. It also plays a key role in shaping parental effects as older parents are expected to be unable to invest optimally in reproduction late in life, or such investments may be compromised by the detrimental consequences of aging. In most species, reproductive performance increases over the first breeding attempts, reaches a plateau, and then declines at older ages. Many long-lived species, however, deviate from this pattern, with older individuals maintaining high breeding performance or even improving it, often resulting in offspring of higher quality. Studies examining sex-specific patterns of reproductive aging in long-lived species from natural populations and their consequences for offspring fitness remain scarce compared to the extensive human literature. We used a long-term longitudinal dataset of reproductive data collected from a population of a long-lived seabird, the Scopoli's shearwater, to analyze (i) how a set of parental traits (i.e., reproductive success, body mass and egg size) change with maternal and paternal age, and (ii) potential age-dependent parental effects on the body mass and skeletal traits of the offspring. We found that age strongly affected reproductive success. Early-life improvement was steeper in females than in males, whereas both sexes showed the typical late-life decline expected with advancing age. Adult body mass followed a similar, though partially reversed, pattern: males gained mass more rapidly than females early in life before reaching a plateau. Age also affected female egg volume and width, with older and heavier females laying larger and wider eggs. Parental effects on offspring body mass were mainly driven by pair experience, whereas skeletal traits depended only on chick age and sex. Our study shows that reproductive aging varies across traits in long-lived species, providing support for the asynchronous theory of aging, and reveals unexpected sex-specific patterns of age-related reproductive changes in monogamous species. Moreover, it suggests that advanced parental age is not necessarily associated with negative effects on offspring fitness.

An individual's age at first reproduction and investment in successive reproductive attempts are involved in mechanisms that can impede somatic repair, resulting in a decline in reproductive abilities with age (reproductive senescence). We used long-term data from the Black-legged Kittiwake, a long-lived seabird, to address the relationship between recruitment age, age-specific breeding success (BS), and reproductive senescence, while accounting for breeding experience and temporal variation in BS. We first detected late-life improvement in BS across all recruitment groups, which we recognized as "within-generation selection" or the selective disappearance of "frail" phenotypes. When such heterogeneity was accurately accounted for, we showed that all individuals suffered reproductive senescence. We first highlighted how different combinations of pre- and post-recruitment experience across recruitment groups resulted in maximal BS at intermediate ages. BS increased in early recruits as they gained post-recruitment experience, whereas late recruits gained pre-recruitment experience that led to high BS at recruitment. Only individuals recruiting at intermediate ages balanced their pre- and post-recruitment experience. Consistent with the "cumulative reproductive cost hypothesis," we also observed a faster decline in BS in early recruits at advanced ages, whereas individuals delaying recruitment experienced the slowest decline in BS with age. Early recruits, however, reached the highest levels of BS at intermediate ages, sensus stricto (10-13 years old), whereas individuals delaying recruitment experienced the lowest at similar ages. These divergent trajectories may reflect a "delayed trade-off" balancing a maximization of midlife BS against reproductive senescence at advanced ages. Additionally, annual variation in BS had a greater effect on individuals early in life, suggesting that experienced individuals were able to buffer out the effects of temporal variation on BS, which can ultimately improve fitness in stochastic environments. Our findings stress that (1) both observed and unobserved heterogeneity are important in detecting within-individual senescence, and (2) short-term trade-offs may be rare in long-lived species; thus, cumulated reproductive costs should be invoked as an alternative mechanism underlying reproductive senescence.

The conditions under which individuals are reared vary and sensitivity of offspring to such variation is often sex-dependent. Parental age is one important natal condition with consequences for aspects of offspring fitness, but reports are mostly limited to short-term fitness consequences and do not take into account offspring sex. Here we used individual-based data from a large colony of a long-lived seabird, the common tern Sterna hirundo, to investigate longitudinal long-term fitness consequences of parental age in relation to both offspring and parental sex. We found that recruited daughters from older mothers suffered from reduced annual reproductive success. Recruited sons from older fathers were found to suffer from reduced life span. Both effects translated to reductions in offspring lifetime reproductive success. Besides revealing novel sex-specific pathways of transgenerational parental age effects on offspring fitness, which inspire studies of potential underlying mechanisms, our analyses show that reproductive senescence is only observed in the common tern when including transgenerational age effects. In general, our study shows that estimates of selective pressures underlying the evolution of senescence, as well as processes such as age-dependent mate choice and sex allocation, will depend on whether causal transgenerational effects exist and are taken into account.

BackgroundWomen experience adverse changes in cardiovascular health in mid-life; whether the menopausal transition influences these remains strongly debated. The aim of this study was to examine associations of reproductive age (time since final menstrual period (FMP)) with change in carotid intima media thickness (CIMT) and cardiovascular risk factors and determine the role of chronological and reproductive age.MethodsWe used data from 1702 women from a pregnancy-based UK cohort who had up to four repeat cardiovascular health measures between mean age 51 (SD = 4.0) and 56 (SD = 3.6) years and experienced a natural menopause. Multilevel models were used to assess the relationship between cardiovascular measures and time since FMP (reproductive age), whilst adjusting for the underlying effects of chronological age and confounders (socioeconomic factors, body mass index, smoking, alcohol, parity, age at menarche). In addition, we looked at the relationship between cardiovascular measures by chronological age according to menopausal stages (pre-menopause, peri-menopause and post-menopause) using information from women who had and had not experienced menopause (N = 3892).ResultsThere was no strong evidence that reproductive age was associated with CIMT (difference in mean 0.8 μm/year, 95% CI − 0.4, 2.1), whereas there was a strong positive association of chronological age (7.6 μm/year, 95% CI 6.3, 8.9). Consistent with this, we found weaker linear associations of reproductive compared with chronological age for atherosclerotic risk factors, such as with systolic blood pressure (− 0.1 mmHg/year, 95% CI − 0.3, 0.1, and 0.4 mmHg/year, 95% CI 0.2, 0.5, respectively) and non-HDL-cholesterol (0.02 mmol/l/year, 95% CI 0.005, 0.03, and 0.06, 95% CI 0.04, 0.07, respectively). In contrast, associations with fat mass (0.06 kg/m2/year, 95% CI 0.03, 0.10, and 0 kg/m2/year, 95% CI − 0.04, 0.04, respectively) and C-reactive protein (0.01, 95% CI 0.001, 0.02, and 0.01, 95% CI − 0.001, 0.02 natural logged mg/l/year, respectively) were stronger for reproductive compared with chronological age. Both reproductive and chronological age were (weakly) positively associated with glucose (0.002, 95% CI 0.0001, 0.003, and 0.002, 95% CI 0.0001, 0.003 natural logged mmol/l/year, respectively).ConclusionsOur results suggest that going through the menopausal transition does not further increase women’s risk of atherosclerosis (measured by CIMT) beyond effects of ageing. Menopausal transition may, in additional to ageing, modestly increase adiposity and glucose levels and therefore a possible associated diabetes risk.

While the number of studies providing evidence of actuarial senescence is increasing, and covers a wide range of taxa, the process of reproductive senescence remains poorly understood. In fact, quite high reproductive output until the last years of life has been reported in several vertebrate species, so that whether or not reproductive senescence is widespread remains unknown. We compared age-specific changes of reproductive parameters between two closely related species of long-lived seabirds: the small-sized snow petrel Pagodroma nivea, and the medium-sized southern fulmar Fulmarus glacialoides. Both are sympatric in Antarctica. We used an exceptional dataset collected over more than 40 years to assess age-specific variations of both breeding probability and breeding success. We found contrasted age-specific reproductive patterns between the two species. Reproductive senescence clearly occurred from 21 years of age onwards in the southern fulmar, in both breeding probability and success, whereas we did not report any decline in the breeding success of the snow petrel, although a very late decrease in the proportion of breeders occurred at 34 years. Such a contrasted age-specific reproductive pattern was rather unexpected. Differences in life history including size or migratory behaviour are the most likely candidates to account for the difference we reported in reproductive senescence between these sympatric seabird species.

**Abstract:** Age and experience affect key life-history traits, influencing evolutionary processes in a variety of ways. Timing of breeding in relation to optimal environmental conditions (e.g. peaks in prey availability) can also influence breeding success, and studies of closely-related, allochronic species may help disentangle the effects of phenological mismatch on ageing patterns. Here, we test for the effects of age and experience on the survival and reproduction of two long-lived seabirds with different timing of breeding and divergent population trajectories. At South Georgia, populations of the northern (NGP, Macronectes halli) and southern giant petrel (SGP, M. giganteus), are increasing and stable, respectively. In early adulthood, first-time breeders of both species had lower breeding success and annual survival. Breeding success improved markedly with age until around 20 years, driven by within-individual factors, but was lower in SGP which also experienced earlier reproductive senescence. Pre-fledging body mass in NGP showed a broadly quadratic relationship with parental age, suggesting that the age-specific pattern in breeding success was partially related to variation in foraging performance. Furthermore, pre-fledging body mass increased rapidly with parental age among first-time breeders in both species, but breeding success did not, further demonstrating the importance of foraging performance rather than breeding experience per se. Due to allochrony, NGP rear their chicks when the availability of seasonally-limited, high-calorie food (seal and penguin carrion) is higher. This would explain their delayed reproductive senescence and, potentially, improved performance in adulthood due to better neonatal nutrition. In addition, it contributes to the divergent population trajectories of the two species at South Georgia. These findings provide empirical evidence for the influence of phenological mismatch on reproductive senescence. **Authors:** Dimas Gianuca¹, Richard Phillips², Andrew Wood², Deborah Pardo², Stephen Votier³ ¹Projeto Albatroz, ²British Antarctic Survey, ³University of Exeter

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Niño event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.

The effect of reproductive age (chronologic age at conception minus menarcheal age) and chronologic age on the risks of low birth weight, preterm delivery and intrauterine growth retardation were studied in 1198 primiparous women whose pregnancies ended in singleton live births at Yale-New Haven Hospital, 1980-1982. After adjustment for maternal race and other important confounding variables, neither young reproductive age (less than 8 years) nor young chronologic age (less than 20 years) were strongly related to any of the reproductive outcomes. Older chronologic age (greater than 29 years) was also not strongly related to any of these outcomes, but older reproductive age (greater than 15 years) was moderately associated with low birth weight (OR 1.9; 95% CI 0.9, 3.8) after adjusting for maternal race, religion and smoking status. In addition, extremely young reproductive age (less than 2 years) appeared to be associated with an increased risk of preterm delivery (OR 3.1; 95% CI 0.7, 14.6), but our sample was too small to adjust for confounding factors in this group of women. Reproductive age appears to reflect extremes in menarcheal age, whereas chronologic age does not, and this association may account for any relationship between reproductive age and pregnancy risk in primiparous women.

Quail and other short-lived birds.

Ageing refers to a decline in individual performance with increasing age that ultimately leads to a reduction in organismal fitness. Although the physiological causes of ageing are likely diverse, a decrease in mitochondrial function may play a central role, as mitochondria generate over 90% of the energy used by eukaryotic cells. Despite support from human and laboratory studies, the effect of age on mitochondrial function, and the extent to which it may differ between males and females, has largely remained unexplored in wild populations. As such, we investigated mitochondrial respiratory function in a long-lived seabird, the common tern (Sterna hirundo), sampling 161 breeding individuals of known sex and ranging in age from 2 to 24 years. We found that older birds showed reduced maximum electron transport system activity and proton leak, suggesting an age-related decline in mitochondrial capacity. Mitochondrial efficiency in ATP production, however, increased with age, suggesting it to be a potential marker of individual quality and survival. Mitochondrial efficiency, as well as spare respiratory capacity, also showed the highest level of individual repeatability between years, indicating consistent individual differences. Although sex differences in age-related trends were not evident, females exhibited significantly higher mitochondrial respiration, potentially due to the energetic demands of egg laying. Overall, these results contribute to our understanding of the role of mitochondrial respiratory function as one of the physiological mechanisms underlying individual performance and ageing in wild animals.

Actuarial and reproductive senescence in a long-lived seabird: preliminary evidence

Understanding the selective pressures shaping the number of offspring per breeding event is a key area in the study of life-history strategies. However, in species with parental care, costs incurred in offspring production, rather than rearing, have been largely ignored in both theoretical and empirical studies until relatively recently. Furthermore, the few experimental studies that have manipulated production costs have not yet teased apart effects that operate via the parental phenotype from effects on the quality of the resulting young. To examine whether increased egg production influences parental brood rearing capacity independently of effects operating via egg quality, we experimentally increased egg production in gulls and then examined their capacity to rear a control clutch. We found that the capacity of parents to rear the control brood was substantially reduced solely as a consequence of having themselves produced one extra egg. The paradox that, in many species, parents apparently aim for fewer young per breeding event than the experimentally and theoretically demonstrated optimum, has partly arisen from the failure to take into account the constraints imposed by production costs.

The questions about why and how senescence occurs in the wild are among the most pertinent ones in evolutionary ecology. Telomere length is a commonly used marker for aging, while other biomarkers of aging have received considerably less attention. Here we studied how another potent indicator of aging-skin pentosidine concentration-relates to age and blood telomere length in a long-lived seabird with well-documented reproductive senescence. We found no associations between telomere length, skin pentosidine and chronological age in male common gulls (Larus canus), aging from 2 to 30 years. However, the variance in telomere length was 4.6 times higher among the birds older than 13 years, which hints at relaxed selection on telomere length among the birds that have passed their prime age of reproduction. These results suggest that physiological and chronological ages may be largely uncoupled in our study system. Furthermore, our findings do not support a hypothesis about the presence of a common physiological factor (e.g., such as oxidative stress) that would cause covariation between two independent markers of aging.

Reproductive senescence is an age related decline in reproductive performance, and is commonly studied in terms of age-related patterns of offspring production. However, parental fitness arises via offspring performance as well as production, so both components require attention to gain a more complete understanding of the trajectory and fitness consequences of reproductive senescence. Here we utilise a longitudinal dataset from a long-term study of European badgers (Meles meles) to investigate maternal and paternal reproductive senescence, and quantify how both offspring production and lifetime performance vary with parental age. First, we show that badgers of both sexes experience a senescent decline in annual offspring production, which occurs with a similar age of onset in the two sexes. Second, we show evidence of deleterious maternal age effects on offspring performance; offspring mortality risk increases and offspring lifespan and life-time reproductive success decreases with within-mother increases in maternal age. Crucially, the maternal ages of onset of these declines in offspring performance are significantly earlier than those for offspring production, such that failure to account for them would lead to underestimation of the severity (in terms of timing and fitness consequences) of maternal reproductive senescence. Finally, we found no evidence of paternal age effects on offspring mortality, lifespan or life-time reproductive success. Overall, our findings illustrate the potential importance of attending to parental age-related changes in offspring performance as well as production, and the potential for sex differences in the relative contributions of these two components to the overall fitness consequences of reproductive senescence.

Selection bias due to parity-conditioning in studies of time trends in fertility.