Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.

Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments.

Experimental extra-pair copulations provide proof of concept for fertility insurance in a socially monogamous bird.

Extra-pair paternity is common among socially monogamous birds, but whether females benefit from having extra-pair copulations remains unresolved. In this study, I staged single extra-pair copulations in captive pairs of socially monogamous Japanese quail (Coturnix japonica) and used extra-pair males of a different colour to identify extra-pair fertilizations. This eliminated among-female variation in extra-pair copulations as a source of variation in extra-pair fertilizations and tested whether a single extra-pair copulation would insure against infertility of the social male. Overall, the probability of extra-pair fertilization was 0.46 for the first egg that was fertilized after extra-pair copulation, but this rapidly declined over consecutive eggs in the laying sequence. However, a single extra-pair copulation was effective in ensuring fertilization of the majority of a typical clutch in the few cases where the social male was completely infertile. Hence, my results show that variation in extra-pair paternity can be independent from variation in extra-pair copulation behaviour and that a single, strategically timed, extra-pair copulation can largely insure against social male infertility. Among-female variation in extra-pair fertilizations, and their declining probability over the laying sequence, as typical for many bird species, can thus, in principle, be parsimoniously explained by a uniform female fertility insurance strategy.

High individual repeatability of the migratory behaviour of a long-distance migratory seabird.

BACKGROUND: Understanding the evolution of migration requires knowledge of the patterns, sources, and consequences of variation in migratory behaviour, a need exacerbated by the fact that many migratory species show rapid population declines and require knowledge-based conservation measures. We therefore need detailed knowledge on the spatial and temporal distribution of individuals across their annual cycle, and quantify how the spatial and temporal components of migratory behaviour vary within and among individuals. METHODS: We tracked 138 migratory journeys undertaken by 64 adult common terns (Sterna hirundo) from a breeding colony in northwest Germany to identify the annual spatiotemporal distribution of these birds and to evaluate the individual repeatability of eleven traits describing their migratory behaviour. RESULTS: Birds left the breeding colony early September, then moved south along the East Atlantic Flyway. Wintering areas were reached mid-September and located at the west and south coasts of West Africa as well as the coasts of Namibia and South Africa. Birds left their wintering areas late March and reached the breeding colony mid-April. The timing, total duration and total distance of migration, as well as the location of individual wintering areas, were moderately to highly repeatable within individuals (repeatability indexes: 0.36-0.75, 0.65-0.66, 0.93-0.94, and 0.98-1.00, respectively), and repeatability estimates were not strongly affected by population-level inter-annual variation in migratory behaviour. CONCLUSIONS: We found large between-individual variation in common tern annual spatiotemporal distribution and strong individual repeatability of several aspects of their migratory behaviour.

Immunosenescence in the wild? A longitudinal study in a long-lived seabird.

Longitudinal studies of various vertebrate populations have demonstrated senescent declines in reproductive performance and survival probability to be almost ubiquitous. Longitudinal studies of potential underlying proximate mechanisms, however, are still scarce. Due to its critical function in the maintenance of health and viability, the immune system is among the potential (mediators of) proximate mechanisms that could underlie senescence. Here, we studied three innate immune parameters-haemagglutination titre, haemolysis titre and haptoglobin concentration-in a population of common terns (Sterna hirundo) known to undergo actuarial senescence. We repeatedly sampled birds of known sex and age across 11 years and used random regression models to (a) quantify how immune parameters vary among individuals and (b) describe within-individual age-specific changes in, and potential trade-offs between, immune parameters. Our models revealed no differences between males and females in haemagglutination titre and haptoglobin concentration, and very low among-individual variation in these parameters in general. Within individuals, haemagglutination titre increased with age, while haptoglobin concentration did not change. We found no indication for selective (dis)appearance in relation to haemagglutination titre or haptoglobin concentration, nor for the existence of a trade-off between them. Haemolysis was absent in the majority (76%) of samples. Common terns do not exhibit clear senescence in haemagglutination titre and haptoglobin concentration and show very little among-individual variation in these parameters in general. This may be explained by canalisation of the immune parameters or by the colonial breeding behaviour of our study species, but more longitudinal studies are needed to facilitate investigation of links between species' characteristics and immunosenescence in wild animals.

Telomere length is heritable and genetically correlated with lifespan in a wild bird.

Telomeres are protective caps at the end of eukaryotic chromosomes that shorten with age and in response to stressful or resource-demanding conditions. Their length predicts individual health and lifespan across a wide range of animals, but whether the observed positive association between telomere length and lifespan is environmentally induced, or set at conception due to a shared genetic basis, has not been tested in wild animals. We applied quantitative genetic "animal models" to longitudinal telomere measurements collected over a 10-year period from individuals of a wild seabird (common tern; Sterna hirundo) with known pedigree. We found no variation in telomere shortening with age among individuals at the phenotypic and genetic level, and only a small permanent environmental effect on adult telomere length. Instead, we found telomere length to be highly heritable and strongly positively genetically correlated with lifespan. Such heritable differences between individuals that are set at conception may present a hitherto underappreciated component of variation in somatic state.

How fitness consequences of early-life conditions vary with age in a long-lived seabird: A Bayesian multivariate analysis of age-specific reproductive values.

Evolutionary theory suggests that individuals can benefit from deferring the fitness cost of developing under poor conditions to later in life. Although empirical evidence for delayed fitness costs of poor developmental conditions is abundant, individuals that die prematurely have not often been incorporated when estimating fitness, such that age-specific fitness costs, and therefore the relative importance of delayed fitness costs are actually unknown. We developed a Bayesian statistical framework to estimate age-specific reproductive values in relation to developmental conditions. We applied it to data obtained from a long-term longitudinal study of common terns Sterna hirundo, using sibling rank to describe variation in developmental conditions. Common terns have a maximum of three chicks, and later hatching chicks acquire less food, grow more slowly and have a lower fledging probability than their earlier hatched siblings. We estimated fitness costs in adulthood to constitute c. 45% and 70% of the total fitness costs of hatching third and second, respectively, compared to hatching first. This was due to third-ranked hatchlings experiencing especially high pre-fledging mortality, while second-ranked hatchlings had lower reproductive success in adulthood. Both groups had slightly lower adult survival. There was, however, no evidence for sibling rank-specific rates of senescence. We additionally found years with low fledgling production to be associated with particularly strong pre-fledging selection on sibling rank, and with increased adult survival to the next breeding season. This suggests that adults reduce parental allocation to reproduction in poor years, which disproportionately impacts low-ranked offspring. Interpreting these results, we suggest that selection at the level of the individual offspring for delaying fitness costs is counteracted by selection for parental reduction in brood size when resources are limiting.

Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long-lived seabird.

Telomeres are protective caps at the end of chromosomes, and their length is positively correlated with individual health and lifespan across taxa. Longitudinal studies have provided mixed results regarding the within-individual repeatability of telomere length. While some studies suggest telomere length to be highly dynamic and sensitive to resource-demanding or stressful conditions, others suggest that between-individual differences are mostly present from birth and relatively little affected by the later environment. This dichotomy could arise from differences between species, but also from methodological issues. In our study, we used the highly reliable Terminal Restriction Fragment analysis method to measure telomeres over a 10-year period in adults of a long-lived seabird, the common tern (Sterna hirundo). Telomeres shortened with age within individuals. The individual repeatability of age-dependent telomere length was high (>0.53), and independent of the measurement interval (i.e., one vs. six years). A small (R2  = .01), but significant part of the between-individual variation in telomere length was, however, explained by the number of fledglings produced in the previous year, while reproduction in years prior to the previous year had no effect. We confirmed that age-dependent telomere length predicted an individual's remaining lifespan. Overall, our study suggests that the majority of between-individual variation in adult telomere length is consistent across adult life, and that a smaller part of the variation can be explained by dynamic factors, such as reproduction.

Age-Specific Offspring Mortality Economically Tracks Food Abundance in a Piscivorous Seabird.

Earlier offspring mortality before independence saves resources for kin, which should be more beneficial when food is short. Using 24 years of data on age-specific common tern (Sterna hirundo) chick mortality, best described by the Gompertz function, and estimates of energy consumption per age of mortality, we investigated how energy wasted on nonfledged chicks depends on brood size, hatching order, and annual abundance of herring (Clupea harengus), the main food source. We found mortality directly after hatching (Gompertz baseline mortality) to be high and to increase with decreasing herring abundance. Mortality declined with age at a rate relatively insensitive to herring abundance. The sensitivity of baseline mortality to herring abundance reduced energy wasted on nonfledged chicks when herring was in short supply. Among chicks that did not fledge, last-hatched chicks were less costly than earlier-hatched chicks because of their earlier mortality. However, per hatchling produced, the least energy was wasted on chicks without siblings because their baseline mortality was most sensitive to herring abundance. We suggest that earlier mortality of offspring when food is short facilitates economic adjustment of posthatching parental investment to food abundance but that such economic brood reduction may be constrained by sibling competition.

Contrasting heterozygosity-fitness correlations across life in a long-lived seabird.

Selection is a central force underlying evolutionary change and can vary in strength and direction, for example across time and space. The fitness consequences of individual genetic diversity have often been investigated by testing for multilocus heterozygosity-fitness correlations (HFCs), but few studies have been able to assess HFCs across life stages and in both sexes. Here, we test for HFCs using a 26-year longitudinal individual-based data set from a large population of a long-lived seabird (the common tern, Sterna hirundo), where 7,974 chicks and breeders of known age were genotyped at 15 microsatellite loci and sampled for life-history traits over the complete life cycle. Heterozygosity was not correlated with fledging or post-fledging prospecting probabilities, but was positively correlated with recruitment probability. For breeders, annual survival was not correlated with heterozygosity, but annual fledgling production was negatively correlated with heterozygosity in males and highest in intermediately heterozygous females. The contrasting HFCs among life stages and sexes indicate differential selective processes and emphasize the importance of assessing fitness consequences of traits over complete life histories.

Embryonic growth rate affects telomere attrition: an experiment in a wild bird.

High growth rate is associated with a short lifespan, but the physiological basis for this trade-off is not well known. Telomere length predicts individual lifespan and in this study we investigated whether embryonic growth rate, manipulated using incubation temperature, affects erythrocyte telomere length in a wild bird species, the common tern (Sterna hirundo). A 1°C lower incubation temperature decreased growth rate by 5%, without affecting size at hatching. The slower growth was associated with an average telomere length that was 147 base pairs longer at hatching. If carried through to adulthood, this effect would correspond with an approximately 3 year longer lifespan. Our results thus suggest that an effect of growth rate on lifespan may be mediated by telomere dynamics or a physiological process reflected by telomere length.

Reduced telomere length in offspring of old fathers in a long-lived seabird.

Evidence for transgenerational effects of senescence, whereby offspring from older parents have a reduced lifetime reproductive success, is increasing. Such effects could arise from compromised germline maintenance in old parents, potentially reflected in reduced telomere length in their offspring. We test the relationship between parental age and offspring early-life telomere length in a natural population of common terns and find a significant negative correlation between paternal age and offspring telomere length. Offspring telomere length is reduced by 35 base pairs for each additional year of paternal age. We find no correlation with maternal age. These results fit with the idea of compromised germline maintenance in males, whose germline stem cells require continued division.

Intraspecific Variation in and Environment-Dependent Resource Allocation to Embryonic Development Time in Common Terns.

Embryonic development time is thought to impact life histories through trade-offs against life-history traits later in life, yet the inference is based on interspecific comparative analyses only. It is largely unclear whether intraspecific variation in embryonic development time that is not caused by environmental differences occurs, which would be required to detect life-history trade-offs. Here we performed a classical common-garden experiment by incubating fresh eggs of free-living common terns (Sterna hirundo) in a controlled incubation environment at two different temperatures. Hatching success was high but was slightly lower at the lower temperature. While correcting for effects of year, incubation temperature, and laying order, we found significant variation in the incubation time embryos required until hatching and in their heart rate. Embryonic heart rate was significantly positively correlated within clutches, and a similar tendency was found for incubation time, suggesting that intrinsic differences in embryonic development rate between offspring of different parents exist. Incubation time and embryonic heart rate were strongly correlated: embryos with faster heart rates required shorter incubation time. However, after correction for heart rate, embryos still required more time for development at the lower incubation temperature. This suggests that processes other than development require a greater share of resources in a suboptimal environment and that relative resource allocation to development is, therefore, environment dependent. We conclude that there is opportunity to detect intraspecific life-history trade-offs with embryonic development time and that the resolution of trade-offs may differ between embryonic environments.

Early mortality saves energy: estimating the energetic cost of excess offspring in a seabird.

Offspring are often produced in excess as insurance against stochastic events or unpredictable resources. This strategy may result in high early-life mortality, yet age-specific mortality before offspring independence and its associated costs have rarely been quantified. In this study, we modelled age-specific survival from hatching to fledging using 24 years of data on hatching order (HO), growth and age of mortality of more than 15 000 common tern (Sterna hirundo) chicks. We found that mortality peaked directly after hatching, after which it declined rapidly. Mortality hazard was best described with the Gompertz function, and was higher with later HO, mainly due to differences in baseline mortality hazard, rather than age-dependent mortality. Based on allometric mass-metabolism relationships and detailed growth curves of starving chicks, we estimated that the average metabolizable energy intake of non-fledged chicks was only 8.7% of the metabolizable energy intake of successful chicks during the nestling phase. Although 54% of hatchlings did not fledge, our estimates suggest them to have consumed only 9.3% of the total energy consumption of all hatched chicks in the population before fledging. We suggest that rapid mortality of excess offspring is part of an adaptive brood reduction strategy to the benefit of the parents.

Male-biased sex allocation in ageing parents; a longitudinal study in a long-lived seabird.

Optimal sex allocation is frequency-dependent, but senescence may cause behaviour at old age to be suboptimal. We investigated whether sex allocation changes with parental age, using 16 years of data comprising more than 2500 molecularly sexed offspring of more than 600 known-age parents in common terns (Sterna hirundo), slightly sexually size-dimorphic seabirds. We decomposed parental age effects into within-individual change and sex allocation-associated selective (dis)appearance. Individual parents did not differ consistently in sex allocation, but offspring sex ratios at fledging changed from female- to male-biased as parents aged. Sex ratios at hatching were not related to parental age, suggesting sons to outperform daughters after hatching in broods of old parents. Our results call for the integration of sex allocation theory with theory on ageing and demography, as a change in sex allocation with age per se will cause the age structure of a population to affect the frequency-dependent benefits and the age-specific strength of selection on sex allocation.

Contrasting between- and within-individual trait effects on mortality risk in a long-lived seabird.

Individual life span is the most important determinant of lifetime reproductive success and fitness across taxa. Identifying the relationships between life-history traits and survival therefore is fundamental to understanding the evolution of a species' traits. Especially important in this respect is to separate the contributions of between- and within-individual trait effects, because only such an approach can identify markers of individual quality and expose within-individual processes such as aging or the occurrence of costs of reproduction. Here we report a rigorous cross-trait comparison in which we quantify effects of between- and within- individual variation in phenology, body mass, and reproductive performance on mortality risk in a long-lived seabird, the Common Tern Sterna hirundo. Between individuals, earlier arrival at the breeding colony, earlier egg-laying, greater body mass, and more successful reproduction are associated with a lower mortality risk, and are markers of individual quality. The standardized between-individual effects of arrival and laying date especially stand out, suggesting that phenology represents the best proxy for life span. In contrast, within individuals, earlier phenology, greater body mass, and more successful reproduction are associated with a higher mortality risk, as is a reduced probability of breeding. After correcting for changes in traits with age, within-individual effects of phenology, breeding probability, clutch size, and egg volume remain significantly associated with mortality risk, which reveals survival costs of early arrival and initial investment in reproduction, but suggests terminal effects in breeding probability. Overall, our study illustrates the usefulness of separating between- and within-individual trait effects on fitness measures to identify markers of individual quality and life-history trade-offs in natural populations.

Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird.

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.

Age-dependent trait variation: the relative contribution of within-individual change, selective appearance and disappearance in a long-lived seabird.

Within populations, the expression of phenotypic traits typically varies with age. Such age-dependent trait variation can be caused by within-individual change (improvement, senescence, terminal effects) and/or selective (dis)appearance of certain phenotypes among older age classes. In this study, we applied two methods (decomposition and mixed modelling) to attribute age-dependent variation in seven phenological and reproductive traits to within-individual change and selective (dis)appearance, in a long-lived seabird, the common tern (Sterna hirundo). At the population level, all traits, except the probability to breed, improved with age (i.e. phenology advanced and reproductive output increased). Both methods identified within-individual change as the main responsible process, and, within individuals, performance improved until age 6-13, before levelling off. In contrast, within individuals, breeding probability decreased to age 10, then levelled off. Effects of selective appearance and disappearance were small, but showed that longer-lived individuals had a higher breeding probability and bred earlier and that younger recruits performed better throughout life than older recruits in terms of both phenology and reproductive performance. In the year prior to death, individuals advanced reproduction, suggesting terminal investment. The decomposition method attributed more age-dependent trait variation to selective disappearance than the mixed-modelling method: 14-36% versus 0-8%, respectively, which we identify to be due to covariance between rates of within-individual change and selective (dis)appearance leading to biased results from the decomposition method. We conclude that the decomposition method is ideal for visualizing processes underlying population change in performance from one age class to the next, but that a mixed-modelling method is required to investigate the significance and relative contribution of age effects. Considerable variation in the contribution of the different age processes between the seven phenotypic traits studied, as well as notable differences between species in patterns of age-dependent trait expression, calls for better predictions regarding optimal allocation strategies with age.

Ecological causes of multilevel covariance between size and first-year survival in a wild bird population.

Estimates of selection in natural populations are frequent but our understanding of ecological causes of selection, and causes of variation in the direction, strength and form of selection is limited. Here, we apply a multilevel framework to partition effects of great tit fledging mass on first-year survival to hierarchical levels and quantify their ecological dependence using a data set spanning 51 years. We show that estimates of the effect of fledging mass on first-year survival decline threefold from year- to brood- to individual level, so that estimates of selection depend strongly on the level at which they are calculated. We identify variables related to summer and winter food availability as underlying higher-level effects of fledging mass on first-year survival and show experimentally that brood-level effects originate early in development. Further, we show that predation and conspecific density modulate individual-level effects of fledging mass on first-year survival. These analyses demonstrate how correlations between traits, fitness and environment influence estimates of selection and show how partitioning trait effects between levels of selection and environmental factors is a promising approach to identify potential agents of selection.

The contribution of an avian top predator to selection in prey species.

Natural selection can vary in magnitude, form and direction, yet the causes of selection, and of variation in selection, are poorly understood. We quantified the effect of a key predator (Eurasian sparrowhawks) on selection on fledging body mass in two bird species (blue tits and great tits). By partitioning selection into within- and between-brood components, we were able to separate individual from brood-level effects of fledging mass on predation probability and recruitment. In blue tits, selection on fledging mass by sparrowhawk predation was nonsignificant and could not explain selection to recruitment. In contrast, in great tits, sparrowhawk predation selected for increased fledging mass at the individual level and could explain 73% of individual-level selection on fledging mass to recruitment. Moreover, in great tits, individual-level selection on fledging mass was significantly stronger in years in which sparrowhawks were present compared to years when sparrowhawks were absent. Selection at the brood level was independent of sparrowhawk presence. These results provide compelling evidence that sparrowhawk predation acts as an important causal agent of selection on fledging mass in great tits but not in blue tits. Variation in predation pressure can therefore account for variation in selection, but specific patterns may not be easily generalized across species.