Parental age does not influence offspring telomeres during early life in common gulls (Larus canus).

Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre- and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.

Age-dependent expression of cancer-related genes in a long-lived seabird.

Studies of model animals like mice and rats have led to great advances in our understanding of the process of tumorigenesis, but this line of study has less to offer for understanding the mechanisms of cancer resistance. Increasing the diversity of nonmodel species from the perspective of molecular mechanisms of natural cancer resistance can lead to new insights into the evolution of protective mechanisms against neoplastic processes and to a wider understanding of natural cancer defense mechanisms. Such knowledge could then eventually be harnessed for the development of human cancer therapies. We suggest here that seabirds are promising, albeit currently completely ignored candidates for studying cancer defense mechanisms, as they have a longer maximum life span than expected from their body size and rates of energy metabolism and may have thus evolved mechanisms to limit neoplasia progression, especially at older ages. We here apply a novel, intraspecific approach of comparing old and young seabirds for improving our understanding of aging and neoplastic processes in natural settings. We used the long-lived common gulls (Larus canus) for studying the age-related pattern of expression of cancer-related genes, based on transcriptome analysis and databases of orthologues of human cancer genes. The analysis of differently expressed cancer-related genes between young and old gulls indicated that similarly to humans, age is potentially affecting cancer risk in this species. Out of eleven differentially expressed cancer-related genes between the groups, three were likely artifactually linked to cancer. The remaining eight were downregulated in old gulls compared to young ones. The downregulation of five of them could be interpreted as a mechanism suppressing neoplasia risk and three as increasing the risk. Based on these results, we suggest that old gulls differ from young ones both from the aspect of cancer susceptibility and tumor suppression at the genetic level.

Uropygial gland size: a marker of phenotypic quality that shows no senescence in a long-lived seabird.

Studies of senescence in the wild have traditionally focused on traits like survival or fecundity. Although efforts to measure other salient phenotypic traits and markers of relevant physiological processes are rapidly increasing, traits related to self-maintenance remain understudied in the context of aging. Uropygial or preen gland is a holocrine gland, exclusive to birds, directly linked to self-maintenance of the quality of plumage. We measured the size of uropygial glands of common gulls (Larus canus) in a cross sectional manner in order to test whether it shows the similar age-related decline as reproductive traits previously recorded in this species. Gulls with larger glands started breeding earlier in the season, indicating that gland size is a marker of individual phenotypic quality. We found a senescent decline in the onset of breeding and the size of white wing patches, a sexually dimorphic ornamental trait, while in contrast, preen gland increased with advancing age. This finding supports the view of life-history theory that in long-lived species whose lifetime reproductive success depends heavily on lifespan, self-maintenance is prioritized over reproduction. Altogether our results support the concept that senescence in the wild can be asynchronous for traits related to maintenance versus reproduction.

Age-specific patterns of maternal investment in common gull egg yolk.

While the general patterns of age-specific changes in reproductive success are quite well established in long-lived animals, we still do not know if allocation patterns of maternally transmitted compounds are related to maternal age. We measured the levels of yolk testosterone, carotenoids and vitamins A and E in a population of known-aged common gulls (Larus canus) and found an age-specific pattern in yolk lutein and vitamin A concentrations. Middle-aged mothers allocated more of these substances to yolk compared to young and old mothers. These results can be explained through differences in age-specific foraging, absorption or deposition patterns of carotenoids and vitamins into yolk. If these molecules play a role in antioxidant defence and immune modulation, our results suggest a possible physiological pathway underlying the age-specific changes in reproductive success of long-lived birds in the wild.

Variation in the Markers of Nutritional and Oxidative State in a Long-Lived Seabird: Associations with Age and Longevity.

Age-related declines in life-history traits have been widely observed in free-living animals. Several theories link senescence to oxidative stress. The aim of this study was to measure several widely used markers of oxidative and nutritional state in a long-lived seabird, the common gull (Larus canus), in order to assess the suitability of these markers for describing deterioration in physiological condition associated with chronological age and survival. Associations with longevity and individual consistency of these parameters over the years (repeatability) were also assessed. Senescence in fitness parameters was observed during the study period: in females, laying date and clutch mass were related to bird age in a curvilinear manner, with middle-aged birds breeding earlier and laying heavier eggs. The only parameter associated with aging processes was glutathione concentration in erythrocytes, which was lower in female birds with longer life spans. Of indexes of nutritional state, plasma triglyceride concentration showed a between-individual increase with age, suggesting selective mortality of birds with low levels. Additionally, total plasma protein levels of individual males increased with age. The mostly negative results of this study hint that the commonly used parameters of physiological condition and oxidative state used in this study do not adequately reflect an individual's long-term health condition. Alternatively, it is possible that in common gulls, senescence occurs in reproductive mechanisms but not in mechanisms responsible for maintaining an organism's redox balance, consistent with the idea that different aspects of an organism's physiological condition age at different rates. Significant interannual repeatability was detected in three plasma constituents-carotenoids, uric acid, and total protein-all of which can possibly be linked to variation in dietary habits.

Skin pentosidine and telomere length do not covary with age in a long-lived seabird.

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.

"Hidden" reproductive conflict between mates in a wild bird population.

Environmental conditions experienced by a female prior to reproducing may be influenced by her mate. Part of such an indirect effect of a male on his partner's reproduction may be genetic (indirect genetic effect). However, a female's direct and a male's indirect genetic effects need not align. We analyzed 10,652 records of seasonal timing of laying, an important reproductive trait in many organisms, of 1864 male and 1916 female common gulls Larus canus collected during 37 years. We show that there is both a direct (female) and an indirect (male) genetic effect (explaining 14.5% and 4.8% of the REML estimated variance in laying date, respectively), but these are significantly negatively correlated (-0.53+/-0.22 SE), indicating that genes for early laying in females are associated with genes for a delaying male effect on his partner's laying date (and vice versa). There is strong selection for laying early in this population, and these sexually antagonistic genetic effects may contribute in maintaining the variation in laying date. Our findings provide an empirical demonstration of a hitherto largely unstudied level of conflict between mates, with important ramifications for our understanding of evolutionary dynamics and mate choice in nature.

Exploring plasticity in the wild: laying date-temperature reaction norms in the common gull Larus canus.

Exploration of causal components of plasticity is important for insight into evolutionary dynamics and an organism's ability to respond to climate change. Among individuals, variation in plasticity can be due to genotype-environment interaction (GxE) or a result from environmental effects associated with an individual. We investigated plasticity for laying date in the common gulls Larus canus, using data collected in Estonia during 37 years (n=11624 records on 2262 females, with 472 relatives). We used a sliding window approach to find the period in spring during which mean temperature best explained the annual mean laying date. Then, considering the spring temperature as a quantitative description of the environment, we used pedigree information and a random regression animal model to determine the variation in plasticity for the laying date-temperature relationship. We found that individuals differ in the plasticity of laying date (such that there is increased variation among individuals for the laying date in warmer springs), and that approximately 11% of variation in the laying date is heritable, but we found no statistical support for GxE. Plasticity in this species is not constrained by warmer springs.

Reproductive success in presenescent common gulls (Larus canus): the importance of the last year of life.

Survival selection against individuals of inferior quality (measured as breeding success) has been proposed to account for the increase in average reproductive success with advancing age in presenescent birds. This so-called selection hypothesis relies on quality-dependent survival. In the present breeding performance study of common gulls, Larus canus, this assumption was not verified. In particular, omitting the last breeding year from the analysis resulted in the disappearance of the correlation between breeding success and survival. A positive correlation in the full dataset was thus solely based on the poor breeding success of ultimate breeders. Indeed, presenescent individuals were shown to have a specifically low breeding success in their terminal breeding event. The poor success of ultimate breeders thus reflects an abruptly declined condition rather than the birds' overall quality. A comparison of the survival of poor and good performers, involving last-time breeders, thus needs not to be a proper test of the selection hypothesis. Longitudinal analysis revealed a steady increase of individual breeding success until the tenth breeding year. The results suggest that an increase of breeding success with age often found in cross-sectional analyses is primarily a result of age-related improvements of competence and/or increased reproductive effort.