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Deterioration in nutritional condition with aging could reduce reproductive success but coincides with declines in residual reproductive potential, thus invoking opposing expectations for late-life reproduction. Yet, the mechanisms regulating energy accrual and allocation to reproduction and survival throughout the lifetime of long-lived, iteroparous animals have remained elusive owing to variation in energetic costs across their extended reproductive cycle (from conception to juvenile independence). Using 10 years of repeated measures of both nutrition (i.e., body fat and food availability) and reproductive allocation across the reproductive cycle of 232 free-ranging, adult, female mule deer, we revealed that nutrition is a critical piece in understanding patterns of reproductive senescence and terminal investment. From conception to weaning, age-related patterns of reproduction were influenced by both body fat and environmental conditions. Reproductive senescence was clear across the entire reproductive cycle, although allocation to offspring was partly mediated by nutrition. Terminal investment, however, was most evident towards the end of the annual reproductive cycle and unveiled only when considering nutritional condition and food availability; during years with poor resource availability, older mothers raised larger juveniles (i.e., 6-months old). Our work evokes nutrition as a lurking variable in end-of-life reproductive tactics for long-lived animals, while demonstrating the necessity of accounting for energy when considering patterns of reproductive senescence and terminal investment in wild animals.

For many species, behavioral modification is an effective strategy to mitigate negative effects of harsh and unpredictable environmental conditions. When behavioral modifications are not sufficient to mitigate extreme environmental conditions, intrinsic factors may be the primary determinant of survival. We investigated how movement behavior, and internal (i.e., nutrition and age) and external (i.e., food availability and snow depth) states affect survival over winter of a long‐lived and highly faithful species (mule deer; Odocoileus hemionus). We first tested whether animals changed their behavior during winter based on internal and external states; we subsequently investigated how behavior and state interacted to influence survival in the face of extraordinary winter conditions. Movement behavior changed minimally as a function of age and nutrition; yet, movement behavior affected survival—animals that exhibited more restricted movements were more likely to succumb to mortality overwinter than animals with less restricted movements. Additionally, nutrition and cumulative snow depth had a strong effect on survival: animals that were exposed to deep snow and began winter with low fat were much less likely to survive. Behavior was an effective tool in securing survival during mild or moderate winters, but nutrition ultimately underpinned survival during harsh winters.

Nutrition underpins survival and reproduction in animal populations; reliable nutritional biomarkers are therefore requisites to understanding environmental drivers of population dynamics. Biomarkers vary in scope of inference and sensitivity, making it important to know what and when to measure to properly quantify biological responses. We evaluated the repeatability of three nutritional biomarkers in a large, iteroparous mammal to evaluate the level of intrinsic and extrinsic contributions to those traits. During a long-term, individual-based study in a highly variable environment, we measured body fat, body mass, and lean mass of mule deer (Odocoileus hemionus) each autumn and spring. Lean mass was the most repeatable biomarker (0.72 autumn; 0.61 spring), followed by body mass (0.64 autumn; 0.53 spring), and then body fat (0.22 autumn; 0.01 spring). High repeatability in body and lean mass likely reflects primary structural composition, which is conserved across seasons. Low repeatability of body fat supports that it is the primary labile source of energy that is largely a product of environmental contributions of the previous season. Based on the disparate levels in repeatability among nutritional biomarkers, we contend that body and lean mass are better indicators of nutritional legacies (e.g., maternal effects), whereas body fat is a direct and sensitive reflection of recent nutritional gains and losses.

Context Natural selection favors species with strong fidelity to seasonal ranges where resources are predictable across space and time. Extreme disturbance events may negate the fitness benefits of faithfulness—with consequences for population distributions. Objectives We hypothesized that extreme events fragment population distributions through two mechanisms: (1) reductions in fidelity or (2) elevated mortality. We tested the relative contributions of these mechanisms to population dynamics of mule deer ( Odocoileus hemionus )—a long-lived mammal—with long-term, individual-based information before and after disturbance occurred. Methods We evaluated our hypotheses in response to disturbance during winter using a unique dataset of the movement and fate of adult females from a migratory population of mule deer over 8 years in western Wyoming, USA. First, we calculated fidelity of individuals between progressive winters and identified vacant space between population-level ranges to represent gaps in the population distribution. We then assessed: (1) how internal state and disturbance conditions affected fidelity, (2) how internal state, disturbance conditions, and fidelity affected survival, and (3) how survival and fidelity affected creation of gaps in population distribution. Results Disturbance weakened fidelity, but fidelity did not affect survival. Nutritional condition and age affected survival. Weakened fidelity did not change population distribution; rather, nutritional condition underpinned population dynamics, meaning that behavior alone may not prevent the creation of gaps in distribution following extreme disturbances. Conclusions Extreme events may render behavioral plasticity incapable of mitigating mortality risk, and the environmental conditions that animals experience during the months, seasons, or even years before an event may regulate population-level organization in its aftermath.