| Abstract |
The nutrition of wild animals affects their ability to survive, reproduce, and ultimately persist in unpredictable environments. Nutrition interacts with the life history of animals across different scales (Smiley, LaSharr, et al., 2022), from long-term and cross-generational effects that dictate phenotype and reproductive success (Michel et al., 2016), to influences of their current environment on survival (Parker et al., 2009). For large mammals, nutrition underpins much of what they do. Particularly in temperate environments with harsh conditions and severe limitation of resources for extended periods, animals rely heavily on energy stored as fat during winter when resources are scarce (Mautz, 1978; Parker et al., 2009). In seasonal environments, the pattern of fat accumulation and depletion is closely synchronized to their environment and availability of resources (Smiley, Wagler, et al., 2022). Nevertheless, to survive when severe environmental conditions result in an unanticipated but necessary depletion in fat reserves, animals that persist are faced with severe consequences for reproduction that can span years or even generations. The environmental, physiological, and nutritional state of a mother has a lifetime effect on her offspring (Bernardo, 1996), and for ungulates, the nutrition of the mother during gestation can have an important and often underappreciated effect on the lifetime phenotype, behavior, and success of her offspring (Michel et al., 2016). The link between maternal nutrition and offspring performance may have important consequences for how populations or species respond to changing environments. Research in captive settings has shown, even with animals that are closely related (i.e., have similar genetic makeups), maternal condition can have serious lifetime implications for an animal's offspring; mothers in poor condition give birth to sons that exhibit stunted growth compared with sons born to mothers in good condition (Monteith et al., 2009). Yet, identifying the role of maternal effects in wild animals can be difficult. It requires information on the nutritional legacy of a mother in combination with information on current environmental conditions (Benton et al., 2001). Garnering data necessary to disentangle the effects of current nutritional state, environment, and maternal effects requires repeated sampling of mothers and their offspring through time. Long-term, individual-based research is expensive, and logistically challenging, but can provide intricate data to test complex questions and theories. Through a long-term research project, we observed how the nutritional legacy of a harsh winter before an animal's birth potentially influenced the growth and development of a male mule deer (Odocoileus hemionus) born in the wild. As part of a research project that was focused on disentangling the mechanisms of population performance of mule deer, in December 2013 in Wyoming, USA, we captured 70 adult females and fitted them with GPS collars (ATS, Iridium and Vectronic Aerospace, Vertex Plus). Each spring and autumn following that initial capture until December 2021, we recaptured each individual. From 2015 to 2021, we captured newborns of collared females and fit them with expandable VHF or GPS collars (ATS and Vectronic Aerospace). We recaptured all surviving juveniles (both males and females) as adults each spring and autumn following their survival to adulthood. At each capture event for adults, we measured nutritional condition (i.e., percent body fat) and each spring we measured pregnancy and fetal rates of female deer via ultrasonography (see Aikens et al., 2021 for detailed methodology). At each autumn capture, we measured antler size of male deer using standard approaches including measurements of beam lengths, tine lengths, and antler circumferences (Monteith et al., 2014). This long-term, individual-based study has allowed us to begin to elucidate the cross-generational roles of nutrition in a wild population. Mule deer in this population inhabit the Salt and Wyoming Ranges of Wyoming, and each year migrate from low-elevation (~1800 m) winter ranges dominated by sagebrush steppe to high-elevation (~2300–27,500 m) summer ranges, comprised of tall forb, mixed-mountain shrub, aspen, and conifer communities. Peak parturition occurred in mid-June, after migration to summer ranges (Aikens et al., 2021). Overwinter survival was heavily dependent on stored fat accumulated over summer, and winter conditions could be harsh. To assess how winter weather influenced the nutrition of a female mule deer and the subsequent fitness of her offspring, we evaluated the condition of a collared deer (deer 096) and her collared, male offspring (deer MFFO) born after a severe winter and the next 4.5 years of his life. During the winter of 2016–2017, animals in this population encountered harsher conditions than they had experienced in nearly 30 years (snowfall that winter was 236.2 cm, the third greatest annual snowfall recorded for the state; Smiley, LaSharr, et al., 2022), with prolonged periods of subzero temperatures and more extreme snow conditions than average. Indeed, average body fat of animals when captured between 8 March and 10 March 2017 was 2.3% (average during normal winters 4.6%), and although deer 096 (7 years old) was in better shape than many of her counterparts with 4.1% body fat (Figure 1), this population faced an additional 2 months of extremely harsh winter conditions. Animals were pushed to their physiological limits and many succumbed to overwinter mortality; survival of collared females was 70% and survival of collared juveniles (<1 year old) was 0%. After this particularly harsh winter, survival of offspring born in the spring of 2017 was low: 29% of juvenile mule deer born that summer were stillborn or succumbed to malnutrition early (stillbirth/malnutrition ranged from 3% to 18% in other years), further exemplifying the nutritional stress experienced by female deer. On 1 June 2017, deer 096 gave birth to two offspring, one male (MFFO) and one female. Despite the harsh winter that depleted the majority of fat reserves of animals in this population, deer 096 carried two fetuses to term and was successful in her reproductive efforts, likely a product of her higher than average fat levels for the population in spring of 2017. Recruitment of two offspring was something that was not achieved by most mule deer during that summer. Indeed, MFFO was the only male from his cohort that we had collared as an adult; despite capture efforts of random, adult males on the landscape we have not captured a male born during the summer of 2017 on MFFO's winter range. Yet, despite deer 096's success in recruiting two offspring into the population, the legacy of the harsh winter that preceded his birth probably followed MFFO for the remainder of his life. Over the 4.5 years that followed his birth, we recaptured him at 2.5 and 3.5 years of age and measured his antlers and nutritional condition; additionally when he was harvested as a 4.5 year old, we measured his antlers following harvest. MFFO never achieved antler growth that was comparable with average males in his age class in the population (Figure 2). Indeed, each year his antlers appeared more similar to the age class below him than to his actual age class. Compared with other males in this population, MFFO's antlers were 30% smaller than the average 2.5 year old, 33% smaller than the average 3.5 year old, and 20% smaller than the average 4.5 year old in each respective year of his life (Figure 3). Moreover, the amount of fat he had in the autumn was often similar or higher (7% and 9.7% at 2.5 and 3.5 years of age, respectively), compared with other mature males (i.e., 6.4%). Even though his nutritional condition demonstrated that he had access to high-quality food, he was probably unable to achieve his full phenotypic potential. Although there is the potential that expression of genetic potential for antler size was below average for MFFO, we suspect his stunted trajectory of antler growth was in large part a response to his mother's condition when he was in utero and a consequence of a life-lasting maternal effect on growth. The effect of maternal condition on offspring phenotype has been investigated using an individual-based approach in captive settings (Michel et al., 2016; Monteith et al., 2009), and has been evaluated at the population level in wild systems (Monteith et al., 2017). Yet, an investigation of maternal condition on offspring using an individual-based approach has yet to be achieved in wild populations. Long-term, individual-based research provides the opportunity to better understand wild populations and the mechanisms that drive their trajectories. Although MFFO is only a single individual, his striking growth pattern and size may well be driven by the lasting, deleterious effects of the 2016–2017 winter. Moreover, the trajectory of MFFO's growth and the connection to extreme environmental conditions and maternal nutrition has provided a unique opportunity to communicate complex concepts of nutrition and maternal effects to nonscientific audiences. There is an inherent value in the connection to individual animals that accompanies individual-based, long-term research; it can provide tangible examples that allow scientists to demonstrate intricate ecological theory to the public in an understandable manner (Jakopak et al., 2019). Storytelling is an effective and engaging way to allow nonscientific audiences to process, understand, and retain scientific information (Joubert et al., 2019). The story of MFFO's life and growth provides an example of the potential lifetime consequences that a mother's nutrition might have for her offspring in a wild population, regardless of the short-term environments and resources they experience. As populations of large herbivores are exposed to increasingly extreme conditions, changes to nutrition might have unanticipated consequences for animal phenotypes. We thank B. Wagler, R. Smiley, E. Moberg, E. Monfort, and T. Faber for assistance with data collection on the Wyoming Range Mule Deer project during the summer of 2017. The Wyoming Range Mule Deer study was supported by the Wyoming Game and Fish Department, Wyoming Game and Fish Commission, Bureau of Land Management, Muley Fanatic Foundation (including Southwest, Kemmerer, Upper Green, and Blue Ridge Chapters), Boone and Crockett Club, Wyoming Wildlife and Natural Resources Trust, Knobloch Family Foundation, Wyoming Animal Damage Management Board, Wyoming Governor's Big Game License Coalition, Bowhunters of Wyoming, Wyoming Outfitters and Guides Association, Pope and Young Club, the United States Forest Service, and United States Fish and Wildlife Service. We thank the multiple landowners that kindly offered access to their property for this research. The authors declare no conflict of interest. Nutritional condition data (LaSharr, 2022) are available in Dryad at https://doi.org/10.5061/dryad.0rxwdbs3b. |
, Rhiannon P. Jakopak 
