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

Abstract

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.

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

“…This increase suggests that the (tagged) population as a whole departs and arrives substantially earlier or later in some years, while the phenological ranking of individual birds remains largely the same. A possible mechanism underlying this inter-annual population variation in autumn migration could be annual variation in breeding success, which indeed is substantial in the study population [ 126 ]. In years with poor herring abundance, common terns show strong brood reduction [ 127 , 128 ].…”

Sex-specific changes in autosomal methylation rate in ageing common terns

“…Interestingly, male and female terns from our study population do not differ in the onset or rate of senescence in survival or breeding probabilities (Zhang et al 2015b;Vedder et al 2021b), such that sex-specificity in the ageing process is only found in how parental age affects the quality of the offspring that recruit back into the population (with maternal age negatively affecting the reproductive performance of daughters and paternal age negatively affecting survival of sons (Bouwhuis et al 2015)). As such, we did not necessarily expect sex differences in the age-specificity of the birds' autosomal methylation level.…”

The quantitative genetics of fitness in a wild seabird

“…We fitted random intercepts for individual identity linked to the pairwise relatedness matrix, individual identity not linked to the pedigree (to account for permanent environmental effects) and year of observation (to account for temporal variation across years). As fixed effects, we modeled the trait intercept and age (continuous trait ranging from 1 to 23 years), as AAS is known to linearly decrease with age (Zhang et al 2015;Vedder et al 2021) (but see Supporting Information, Table S3, for results of the same animal model without age effects).…”

“…A better understanding of the genetic architecture of fitness will also provide added benefits, as, for instance, it would allow a deeper understanding of the genetic underpinnings of complex traits such as fitness, which might be subjected to different pleiotropic effects (Mackay 2001). For instance, antagonistic pleiotropy is often assumed to underlie the negative phenotypic correlation between the two main components of lifetime fitness: survival and reproductive success (also observed in the terns: Vedder et al 2021).…”