Behavioral plasticity shapes population aging patterns in a long-lived avian scavenger.

Studying the mechanisms shaping age-related changes in behavior ("behavioral aging") is important for understanding population dynamics in our changing world. Yet, studies that capture within-individual behavioral changes in wild populations of long-lived animals are still scarce. Here, we used a 15-y GPS-tracking dataset of a social obligate scavenger, the griffon vulture (Gyps fulvus), to investigate age-related changes in movement and social behaviors, and disentangle the role of behavioral plasticity and selective disappearance in shaping such patterns. We tracked 142 individuals for up to 12 y and found a nonlinear increase in site fidelity with age: a sharp increase in site fidelity before sexual maturity (<5 y old), stabilization during adulthood (6 to 15 y), and a further increase at old age (>15 y). This pattern resulted from individuals changing behavior throughout their life (behavioral plasticity) and not from selective disappearance. Mature vultures increased the predictability of their movement routines and spent more nights at the most popular roosting sites compared to younger individuals. Thus, adults likely have a competitive advantage over younger conspecifics. These changes in site fidelity and movement routines were mirrored in changes to social behavior. Older individuals interacted less with their associates (decreasing average strength with age), particularly during the breeding season. Our results reveal a variety of behavioral aging patterns in long-lived species and underscore the importance of behavioral plasticity in shaping such patterns. Comprehensive longitudinal studies are imperative for understanding how plasticity and selection shape the persistence of wild animal populations facing human-induced environmental changes.

Evidence of maternal and paternal age effects on speed in thoroughbred racehorses.

Effects of parental age on offspring viability have been reported in a wide range of species. However, to what extent parental age influences offspring traits beyond viability remains unclear. Moreover, previous research has primarily focused on maternal age effects. The purpose of this study was to test for paternal and maternal age effects on offspring speed in thoroughbred racehorses. We analysed over 900 000 race performances by over 100 000 horses on British racecourses between 1996 and 2019. With knowledge of the age of all 41 107 dams and 2 887 sires at offspring conception, we jointly modelled maternal and paternal age effects using a 'within-individual centring' approach. Within-parents, we identified a significant effect of maternal age on offspring speed of -0.017 yards s-1 yr-1 and a corresponding paternal age effect of -0.011 yards s-1 yr-1. Although maternal age effects were stronger (more negative), the existence and magnitude of paternal effects is particularly noteworthy, given thoroughbred sires have no involvement in parental care. Our results also suggest that the selective disappearance of both sires and dams is ongoing. These findings could potentially be used to optimize thoroughbred racehorse breeding decisions, and more generally, add to the increasing body of evidence that both maternal and paternal age affect a range of offspring characteristics.

Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment.

AbstractIn many species, parental age at reproduction can influence offspring performance and life span, but the direction of these effects and the traits affected vary among studies. Data on parental age effects are still scarce in noncaptive populations, especially insects, despite species such as fruit flies being models in laboratory-based aging research. We performed a biologically relevant experimental manipulation of maternal and paternal age at reproduction of antler flies (Protopiophila litigata) in the laboratory and tracked the adult life span and reproductive success of their male offspring released in the wild. Increased paternal, but not maternal, age somewhat increased sons' adult life span, while parental ages did not influence sons' mating rate or reproductive senescence. Our results indicate that while parental age effects do exist in an insect in the field, they may be beneficial in such a short-lived animal, in contrast to results from most wild vertebrates and laboratory invertebrates.

Distinguishing within- from between-individual effects: How to use the within-individual centring method for quadratic patterns.

Any average pattern observed at the population level (cross-sectional analysis) may confound two different types of processes: some processes that occur among individuals and others that occur within individuals. Separating within- from among-individual processes is critical for our understanding of ecological and evolutionary dynamics. The within-individual centring method allows distinguishing within- from among-individual processes and this method has been widely used in ecology to investigate both linear and quadratic patterns. Here we show that two alternative equations could be used for the investigation of quadratic within-individual patterns. We explain the different assumptions and constraints of both equations. Reviewing the literature, we found that mainly one of these two equations has been used in studies investigating quadratic patterns. Yet this equation might not be the most appropriate in all circumstances leading to bias and imprecision. We show that these two alternative equations make different assumptions about the shape of the within-individual pattern. One equation assumes that the within-individual effect is related to an absolute process whereas the other assumes the effect arises from an individual relative process. The choice of using one equation instead of the other should depend upon the biological process investigated. Using simulations, we showed that a mismatch between the assumptions made by the equation used to analyse the data and the biological process investigated might led to flawed inference affecting output of model selection and accuracy of estimates. We stress that the equation used should be chosen carefully. We provide step by step guidelines for choosing an equation when studying quadratic pattern with the within-individual centring approach. We encourage the use of the within-individual centring method, promoting its relevant application for nonlinear relationships.

Live long and prosper: durable benefits of early-life care in banded mongooses.

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Divergent patterns of telomere shortening in tropical compared to temperate stonechats.

Telomeres have emerged as important biomarkers of health and senescence as they predict chances of survival in various species. Tropical birds live in more benign environments with lower extrinsic mortality and higher juvenile and adult survival than temperate birds. Therefore, telomere biology may play a more important role in tropical compared to temperate birds. We measured mean telomere length of male stonechats (Saxicola spp.) at four age classes from tropical African and temperate European breeding regions. Tropical and temperate stonechats had similarly long telomeres as nestlings. However, while in tropical stonechats pre-breeding first-years had longer telomeres than nestlings, in temperate stonechats pre-breeding first-years had shorter telomeres than nestlings. During their first breeding season, telomere length was again similar between tropical and temperate stonechats. These patterns may indicate differential survival of high-quality juveniles in tropical environments. Alternatively, more favorable environmental conditions, that is, extended parental care, may enable tropical juveniles to minimize telomere shortening. As suggested by previous studies, our results imply that variation in life history and life span may be reflected in different patterns of telomere shortening rather than telomere length. Our data provide first evidence that distinct selective pressures in tropical and temperate environments may be reflected in diverging patterns of telomere loss in birds.

Disentangling Pre- and Postnatal Maternal Age Effects on Offspring Performance in an Insect with Elaborate Maternal Care.

Maternal effect senescence has attracted much recent scientific interest. However, the age-related effects of pre- and postnatal maternal age are often conflated, as these naturally originate from the same individual. Additionally, many maternal effect senescence studies fail to account for potential biases associated with selective disappearance. Here we use a cross-fostered laboratory population of a burying beetle, Nicrophorus vespilloides, to examine both the effects of female pre- and postnatal maternal age on offspring life-history traits and the postcare outcomes of mothers while accounting for selective disappearance of postnatal caregivers. Neither pre- nor postnatal maternal age affected offspring longevity or larval weight at hatching, and postnatal age had no effect on postcare maternal outcomes except to confirm the presence of actuarial senescence. There was weak evidence for concave relationships between two larval traits (dispersal weight and survival) and the age of egg producers. Selective disappearance of caregivers had no clear effect on any of the measured offspring traits. Contrary to predictions from evolutionary theory, maternal effect senescence and reproductive effort increases do not always manifest, and current theory may be insufficient to account for the true diversity of aging patterns relating to maternal care.

Contrasting drivers of reproductive ageing in albatrosses.

Age-related variation in reproductive performance is ubiquitous in wild vertebrate populations and has important consequences for population and evolutionary dynamics. The ageing trajectory is shaped by both within-individual processes, such as improvement and senescence, and the among-individual effects of selective appearance and disappearance. To date, few studies have compared the role of these different drivers among species or populations. In this study, we use nearly 40 years of longitudinal monitoring data to contrast the within- and among-individual processes contributing to the reproductive ageing patterns in three albatross species (two biennial and one annual breeder) and test whether these can be explained by differences in life histories. Early-life performance in all species increased with age and was predominantly influenced by within-individual improvements. However, reproductive senescence was detected in only two of the species. In the species exhibiting senescent declines, we also detected a terminal improvement in breeding success. This is suggestive of a trade-off between reproduction and survival, which was supported by evidence of selective disappearance of good breeders. We demonstrate that comparisons of closely related species which differ in specific aspects of their life history can shed light on the ecological and evolutionary forces shaping variation in ageing patterns.

Stabilizing survival selection on presenescent expression of a sexual ornament followed by a terminal decline.

Senescence is a decrease in functional capacity, increasing mortality rate with age. Sexual signals indicate functional capacity, because costs of ornamentation ensure signal honesty, and are therefore expected to senesce, tracking physiological deterioration and mortality. For sexual traits, mixed associations with age and positive associations with life expectancy have been reported. However, whether these associations are caused by selective disappearance and/or within-individual senescence of sexual signals, respectively, is not known. We previously reported that zebra finches with redder bills had greater life expectancy, based on a single bill colour measurement per individual. We here extend this analysis using longitudinal data and show that this finding is attributable to terminal declines in bill redness in the year before death, with no detectable change in presenescent redness. Additionally, there was a quadratic relationship between presenescent bill colouration and survival: individuals with intermediate bill redness have maximum survival prospects. This may reflect that redder individuals overinvest in colouration and/or associated physiological changes, while below-average bill redness probably reflects poorer phenotypic quality. Together, this pattern suggests that bill colouration is defended against physiological deterioration, because of mate attraction benefits, or that physiological deterioration is not a gradual process, but accelerates sharply prior to death. We discuss these possibilities in the context of the reliability theory of ageing and sexual selection.

Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird.

Telomeres, DNA-protein structures at chromosome ends, shorten with age, and telomere length has been linked to age-related diseases and survival. In vitro studies revealed that the shortest telomeres trigger cell senescence, but whether the shortest telomeres are also the best biomarker of ageing is not known. We measured telomeres in erythrocytes of wild common terns Sterna hirundo using terminal restriction fragment analysis. This yields a distribution of telomere lengths for each sample, and we investigated how different telomere subpopulations (percentiles) varied in their relation to age and fitness proxies. Longer telomeres within a genome lost more base pairs with age and were better predictors of survival than shorter telomeres. Likewise, fitness proxies such as arrival date at the breeding grounds and reproductive success were best predicted by telomere length at the higher percentiles. Our finding that longer telomeres within a genome predict fitness components better than the shorter telomeres indicates that they are a more informative ageing biomarker. This finding contrasts with the fact that cell senescence is triggered by the shortest telomeres. We suggest that this paradox arises, because longer telomeres lose more base pairs per unit time and thus better reflect the various forms of stress that accelerate telomere shortening, and that telomeres primarily function as biomarker because their shortening reflects cumulative effects of various stressors rather than reflecting telomere-induced cell senescence.