Maternal effects are the influence of maternal phenotype and “the maternally provided environment” on the phenotype (i.e., expression of traits) of offspring (Bernardo, 1996; Wolf and Wade, 2009). Life history theory posits that females must balance their own needs and probability of survival with current and future reproductive events (Festa-Bianchet et al., 1998; Marshall and Uller, 2007). When resources are abundant, females often produce larger or more offspring by allocating more energy toward current reproduction (Haywood and Perrins, 1992; Bardsen et al., 2008). However, when resources are scarce, females often allocate less energy to current reproduction (e.g., produce smaller and fewer offspring) to maximize lifetime fitness (Smith and Fretwell, 1974; Einum and Fleming, 2000). Producing smaller offspring potentially decreases current maternal reproductive success in exchange for enhancing survival to a future reproductive bout. Therefore, maternal effects may have a positive or negative influence on the fitness potential of offspring (Kirkpatrick and Lande, 1989; Marshall and Uller, 2007; Freeman et al., 2013). Because of this maternal influence on fitness and production, effective conservation can only be achieved with an understanding maternal effects.

Identifying the life-history traits of offspring that are influenced by maternal effects can be difficult, as there are numerous mechanisms driving both life-history traits and maternal effects (Kirkpatrick and Lande, 1989; Benton et al., 2001). Maternal nutritional condition and subsequent energy allocation have been shown to influence offspring traits, including size at birth (Feiner et al., 2016), growth rate (Haywood and Perrins, 1992), survival (Duquette et al., 2014), age at first reproduction, and fecundity. Nonetheless, maternal effects may disappear after the period of maternal care (Gendreau et al., 2005) or be masked by the influence of environmental conditions in long-lived species (Hewison and Gaillard, 1999). Further, relatively little is known about the importance of maternal effects in large, long-lived species due to the difficulty of studying maternal-offspring relationships in free-ranging mammals. Therefore, determining the duration of maternal effects can be challenging but is critically important for understanding life-history, and can have important implications for conservation.

Ungulates provide a model system to study the duration of maternal effects because they are iteroparous and long-lived (Freeman et al., 2013). Short-term maternal effects, from birth to weaning and during early-life growth, exist in some ungulate species (Kojola, 1993; Wauters et al., 1995; Festa-Bianchet and Jorgenson, 1998). Long-lasting maternal effects may also be present. An intergenerational maternal effect exists on growth and size at maturity in white-tailed deer (Odocoileus virginianus; Monteith et al., 2009). Additionally, maternal effects last into adulthood for antler growth in elk (Cervus canadensis) and mule deer (Odocoileus hemionus), a sexually selected trait that influences fitness potential (Freeman et al., 2013). Despite some evidence for both short- and long-term maternal effects, maternal effects among offspring of ungulate species from early life through recruitment are not well understood.

Maternal effects can manifest both before and after parturition (Bernardo, 1996). However, there has been little differentiation between effects in utero or during rearing of offspring. Pre-parturition effects are primarily direct allocation of energy to the offspring that is in utero (Robbins and Robbins, 1979). Nevertheless, both direct and indirect maternal effects can influence offspring post-parturition. For example, direct effects include energy and nutrient allocation such as milk to nursing young and indirect effects include protection of young (Wolf and Wade, 2009), habitat selection, and maternal care other than nursing (Bernardo, 1996).

Here we focus on direct maternal effects in mule deer fawns. Our objective was to determine the importance of direct maternal effects on birth weight, growth rates, and survival of neonates through 18 months of life. More specifically, we examined the influence of nutritional condition of dams on birth weight, growth rates, and survival of offspring. We hypothesized that maternal nutritional condition would influence offspring both while in utero (birth weight) and throughout the lactation period (growth rate and survival). We predicted that greater maternal condition would be correlated with increased birth weight, growth, and survival of fawns. We predicted that greater maternal condition would lead to larger body sizes for fawns at 6 months of age and that larger fawns would have a greater likelihood of survival through their first winter to recruitment at 18 months of age.

Between March of 2018 and March of 2020 we captured and marked 89 female mule deer with GPS collars. Of these adults, 22 individuals were captured in two consecutive years and one individual was captured all 3 years for a total of 112 capture events. Average ingesta-free body fat (IFBF) for adult females was 6.06% in 2018, 4.34% in 2019, and 6.26% in 2020. Ultrasonography revealed that 106 of 112 (95%) captured animals were pregnant. We captured neonates from 61 collared adult females. In three fawning seasons we located 104 neonates and captured and collared all 98 individuals (6 were stillborn). Over the course of the study we observed 39 sets of twins, and 20 singletons. Of neonates captured, 49 were male and 49 were female. Parturition dates ranged from 28 May to 29 June. Mean date of parturition was June 8th, 14th, and 9th during 2018–2020, respectively. Between December of 2018 and December of 2020, we captured and collared 59 mule deer fawns at approximately 6 months of age. Of the 59 juveniles captured, 27 were individuals originally captured as neonates. Average weight was 30.5 kg in 2018 (SE = 1.2), 31.0 kg in 2019 (SE = 0.8), and 33.6 kg in 2020 (SE = 1.0).

We examined the influence of maternal IFBF on birth weight for 98 neonates. Explanatory variables associated with timing of parturition (mean, median, onset) were highly correlated (r > |0.50|) along with onset and hoof growth. Thus, we did not include these variables together in the same model, but did allow them to occur across models for evaluation. Out of 23 candidate models, the top model examining neonate birth weight accounted for 78.4% of the AICc weight compared to 15.4% for the second-ranked model (no competing models, ΔAICc<2; Table 1). The most supported model included influence of twin, sex, hoof growth, IFBF, and maternal age. As predicted, birth weight of neonates was positively related to IFBF. On average for females with the lowest IFBF, neonates weighed 3.0 kg at birth (SE = 0.1). For females with higher IFBF, neonates averaged 3.5 kg at birth (SE = 0.1; Figure 1). Presence of a twin was associated with lower birth weight. On average, neonates associated with a twin weighed 0.2 kg less than those that were singletons. Age was in the top model but confidence intervals around the estimate overlapped zero. Hoof growth was positively associated with birth weight, but of limited relevance. Measurement of hoof growth is used to determine age of neonate at capture, and older neonates would be heavier than those captured closer to parturition. Males were also associated with greater birth weight (Table 1).

Growth rate of neonates from birth to 6 months of age was related to nutritional condition of the dam. We had four competing models (ΔAICc<2) and averaged all models that carried >5% AICc weight. The averaged models had a cumulative weight of 65.3% (Table 1). Variables in supported models included maternal IFBF, birth weight, sex, and presence of a twin. Maternal IFBF during gestation was positively related to growth through the first 6 months of life. On average neonates from females with higher IFBF grew at a rate of 5.2 kg per month (SE = 0.2), while those from females with low IFBF grew at a rate of 4.4 kg per month (SE = 0.2; Figure 2).

Our top CPH model for neonate survival to 6 months accounted for 50% of the AICc weight (no competing models, ΔAICc<2.0) and included the influence of maternal IFBF, a variable time component of month one versus months 2–6, and whether the neonate was born before or after the peak of parturition (Table 1). Neonate survival to 6 months was positively influenced by maternal IFBF. Neonates born to females with higher IFBF had a higher likelihood of survival than neonates from females with lower IFBF (Figure 3). There was a lower likelihood of survival in month one compared to months two through six, especially for fawns born after peak parturition.

We also examined the influence of maternal IFBF on body size at 6 months for 59 individuals. The top model, with 43% of the AICc weight included maternal age and birth weight (Table 2). After accounting for the effect of maternal age and birth weight, the next ranked model, with 24% of the AICc weight, included maternal IFBF. While the effect was not as strong as at birth, juveniles from females with higher IFBF weighed an average of 4.1 kg more than juveniles from females with lower IFBF (SE = 1.3; Figure 4).

Our top CPH model for survival from six to 18 months accounted for 87% AICc weight. Our most supported model of survival included the influence of weight and year (Table 2). As predicted, larger fawns had a greater likelihood of survival. Deer fawns weighing 35 kg at 6 months of age had at least a 50% probability of survival (Figure 5). Year of birth was a random effect in our models that also influenced survival likely due to the variation in summer precipitation (i.e., food availability) and winter severity among years.

The study of maternal effects to determine phenotypic quality of offspring has become foundational for understanding life-history characteristics (Kirkpatrick and Lande, 1989; Bernardo, 1996). Until recently, technological constraints have limited the ability to monitor free-ranging ungulates and their offspring. Recent technological advancements, however, allow insight into the relationship between maternal nutritional condition and outcomes for offspring (Johnson et al., 2019). These advances have enabled the more precise study of mother-offspring relationships and the natural history of mule deer during early life. Nutritional condition of the dam has been linked to increased survival of neonatal mule deer to 140 days (Monteith et al., 2014). Here, for the first time, however, we connect the influence of maternal nutritional condition to indicators of health (including survival) in mule deer from birth to recruitment at 18 months of age. Consistent with other ungulates, nutritional condition influenced neonatal mule deer both before (e.g., birth weight of neonate mule deer) and after (e.g., growth rate and survival of neonate mule deer) parturition (Duquette et al., 2014; Feiner et al., 2016). Consistent with our prediction, increased nutritional condition of the dam was correlated with increased birth weight, growth rate, and survival of fawns to 6 months of age. Additionally, the effects of maternal nutritional condition lasted through early life and influenced juvenile body weight at 6 months of age and survival through recruitment at 18 months of life.

Mule deer experienced a pre-parturition direct effect of allocation of energy to offspring in utero, manifest as birth weight. Our findings indicate that nutritional condition of females (measured as IFBF) during gestation had a significant impact on birthweight of offspring. Fawns born to females in relatively good nutritional condition were approximately 40% heavier at birth, which could lead to greater potential fitness (Monteith et al., 2009). This finding is consistent with previous research (Hudson and Browman, 1959; Short, 1970; Heffelfinger et al., 2018). Moreover, birth weight is a strong predictor of growth and survival (Monteith et al., 2014).

Post-parturition direct effects were also present through the lactation period, as demonstrated by the influence of maternal nutritional condition on growth rates. There is likely a correlation between quality or quantity of milk and maternal nutritional condition during gestation. The amount and quality of milk produced by the mother is important for growth and development of young (Cook et al., 2004; Tollefson et al., 2010, 2011). Adult females in better condition likely produce more or higher quality milk, which in turn provides greater energy to nursing fawns and subsequent increased growth and survival rates. While there are many environmental factors that may also influence growth to 6 months, few investigators have been able to recapture free-ranging juveniles to monitor growth during the initial months of life.

We were able to clearly link maternal nutritional condition to survival of juvenile mule deer after parturition consistent with current understanding in this species (Monteith et al., 2014). This effect was present even after accounting for the influence of parturition timing or Julian date that the neonate was born. Fawns have a higher likelihood of survival if their mother is in good nutritional condition and if they are born at or before the mean date of parturition. Specifically, fawns from females in the best nutritional condition, born before peak parturition had a roughly 50% greater chance of survival than fawns from females in poor nutritional condition, born after peak parturition (Figure 3). There are likely two advantages associated with being born early—the animal becomes mobile before predators have developed a search image for neonates and the neonates have extra time to grow before the onset of winter. The effects of maternal nutritional condition on survival are consistent with evidence in other ungulate species that heavier females give birth earlier (Cameron et al., 1993; Keech et al., 2000).

Our results do not support the assertion that maternal effects weaken after maternal care ends (Gendreau et al., 2005). Maternal care lessens after weaning, which occurs during late summer and early fall for mule deer (Bowyer, 1991; Tollefson et al., 2011). Here, however, we found that maternal nutritional condition influenced offspring even after weaning, as fawns from mothers in better nutritional condition were heavier when recaptured in early winter at approximately 6 months of age (Figure 4). Further, the influence of maternal nutritional condition persists through the first 18 months of life because capture weight at 6 months of age strongly predicted survival to recruitment age at 18 months. Small sample sizes of recaptured individuals with known parentage prevented us from directly examining the influence of maternal nutritional condition on survival to 18 months. Nonetheless, our data demonstrate that weight at 6 months of age influenced survival to 18 months. Therefore, we infer a connection between maternal nutritional condition, mass of fawns at 6 months of age, and survival of fawns to 18 months of age.

Understanding the link between maternal effects and population dynamics is critical for the conservation and management of mule deer and other long-lived ungulates. For example, the reproductive potential of a population is not only influenced by pregnancy rate and litter size (Noyes et al., 2002; Souza et al., 2022), but also nutritional condition of the dams that influences the survival and expression of phenotypic traits in offspring. The phenotypic traits of young ungulates likely influence all aspects of life history, beyond just survival as we have demonstrated here, including susceptibility to predation (Murray, 2002) and disease (Beldomenico and Begon, 2010), and potential size and reproductive success (Keech et al., 2000; Freeman et al., 2013) as an adult. Therefore, monitoring and managing nutritional condition is fundamental to management and conservation of mule deer, and likely other ungulate populations.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

SL, BM, PF, KH, and RL conceived and designed the study. SL, BM, KH, and RL collected the field data. SL, MK, and RL conducted the statistical analysis. SL and BM wrote the manuscript with input from all authors. All authors contributed to the article and approved the submitted version.

This research was funded by Sportsmen for Fish and Wildlife, Utah Division of Wildlife Resources (Award #166154), and Brigham Young University.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.