Sandra Hamel

Individual variation in reproductive costs of reproduction: high-quality females always do better

1. Although life-history theory predicts substantial costs of reproduction, individuals often show positive correlations among life-history traits, rather than trade-offs. The apparent absence of reproductive costs may result from heterogeneity in individual quality. 2. Using detailed longitudinal data from three contrasted ungulate populations (mountain goats, Oreamnos americanus; bighorn sheep, Ovis canadensis; and roe deer, Capreolus capreolus), we assessed how individual quality affects the probability of detecting a cost of current reproduction on future reproduction for females. We used a composite measure of individual quality based on variations in longevity (all species), success in the last breeding opportunity before death (goats and sheep), adult mass (all species), and social rank (goats only). 3. In all species, high-quality females consistently had a higher probability of reproduction, irrespective of previous reproductive status. In mountain goats, we detected a cost of reproduction only after accounting for differences in individual quality. Only low-quality female goats were less likely to reproduce following years of breeding than of nonbreeding. Offspring survival was lower in bighorn ewes following years of successful breeding than after years when no lamb was produced, but only for low-quality females, suggesting that a cost of reproduction only occurred for low-quality females. 4. Because costs of reproduction differ among females, studies of life-history evolution must account for heterogeneity in individual quality.

Individual quality, early‐life conditions, and reproductive success in contrasted populations of large herbivores

Variations among individuals in phenotypic quality and fitness often confound analyses of life-history strategies assessed at the population level. We used detailed long-term data from three populations of large herbivores with generation times ranging from four to nine years to quantify heterogeneity in individual quality among females, and to assess its influence on mean annual reproductive success over the lifetime (MRS). We also determined how environmental conditions in early life shaped individual quality and tested A. Lomnickis hypothesis that variance in individual quality should increase when environmental conditions deteriorate. Using multivariate analyses (PCA), we identified one (in sheep and deer) or two (in goats) covariations among life-history traits (longevity, success in the last breeding opportunity, adult mass, and social rank) as indexes of individual quality that positively influenced MRS of females. Individual quality was reduced by unfavorable weather, low resource availability, and high population density in the year of birth. Early-life conditions accounted for 35-55% of variation in individual quality. In roe deer, we found greater variance in individual quality for cohorts born under unfavorable conditions as opposed to favorable ones, but the opposite was found in bighorn sheep and mountain goats. Our results demonstrate that heterogeneity in female quality can originate from environmental conditions in early life and can markedly influence the fitness of females in species located at different positions along the slow-fast continuum of life-history strategies.

Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations

Fitness costs of reproduction play a key role in understanding the evolution of reproductive tactics. Nevertheless, the detection and the intensity of costs of reproduction vary according to which life-history traits and species are studied. We propose an evolutionary model demonstrating that the chance of detecting a cost of reproduction should be lower when the fitness component studied has a low rather than high variance. Consequently, the fitness component that is affected the most by costs of reproduction should vary with life speed. Since long-lived species have developed a strategy that avoids jeopardizing their survival and short-lived species favour current reproduction, variance in survival is smaller and variance in reproduction higher in long-lived vs. short-lived species. We review empirical studies of costs of reproduction in free-ranging mammals, comparing evidence of costs reported among species and focal traits. In support of our model, more studies reported evidence of reproductive costs of reproduction in ungulates than in rodents, whereas survival costs of reproduction were more frequent in rodents than in ungulates. The life-history model we propose is expected to apply to any species, and hence provides a better understanding of life-history variation, which should be relevant to all evolutionary ecologists.

Maternal characteristics and environment affect the costs of reproduction in female mountain goats

Reproduction should reduce resources available for somatic investment and result in fundamental trade-offs among life-history traits. Using 18 years of longitudinal data from marked mountain goats (Oreamnos americanus), we assessed whether reproductive status affected female survival and future reproduction when accounting for parity, age, individual quality, population density, and environmental conditions. Reproduction reduced the probability of parturition and offspring survival in the following year. Female survival, however, was independent of previous reproduction, suggesting that females favored their own survival over that of their offspring. The lower probability of parturition in females that had a kid the previous year was only detected at high population density and among young and prime-aged females, suggesting that fitness costs of reproduction can be masked by variations in resource availability and individual characteristics. Primiparous females were less likely than multiparous females to reproduce in the subsequent year. Offspring survival was reduced at high density and after severe winters. Environmental conditions mainly influenced offspring survival, whereas female survival and fecundity were principally modulated by female characteristics. Our study highlights how different intrinsic and environmental factors can affect the probability of future reproduction and also underlines the value of long-term monitoring of known individuals.

Trade-offs in activity budget in an alpine ungulate: contrasting lactating and nonlactating females

Optimal time allocation to foraging behaviour may be constrained by intrinsic and extrinsic factors forcing animals to adopt compromises to meet their daily energetic needs. Our goal was to assess the influence of individual characteristics and extrinsic factors on the activity budget of marked adult female mountain goats, Oreamnos americanus. As lactation entails important energetic costs, we specifically aimed at contrasting activity budgets of lactating and nonlactating females. We determined female activity budgets using 10-min interval scan sampling between 2002 and 2005. Lactating females, females raising sons and females that were subordinate for their age spent more time foraging than nonlactating females, females raising daughters and dominant females, respectively. Although foraging is typically incompatible with scanning, increased time spent foraging was mainly performed at the expense of time spent lying rather than time spent in vigilance. Lactating females also increased time spent ruminating while lying compared with nonlactating females. All females traded lying time for increased foraging and ruminating times in early and late summer. Females spent less time foraging on warm days, and foraged more at dusk than during the rest of the day. Age and body mass did not influence female activity budgets. Our results indicate that lactating females partly compensated for the costs of lactation by trading lying for foraging time, and reorganized lying time to increase the proportion of time spent ruminating. This study emphasizes the fundamental behavioural trade-offs that female mammals must face to meet their daily energetic requirements and allows a better understanding of how these compromises vary through the lactation period.

Habitat use patterns in relation to escape terrain: are alpine ungulate females trading off better foraging sites for safety?

Predation risk often forces prey to trade off good foraging sites for safety, and compromises are expected to be greater in females with vulnerable offspring than in barren females. To determine whether adult females of large herbivores traded off forage for safety, we assessed habitat use and estimated vegetation abundance and quality in relation to distance to escape terrain in marked mountain goats (Oreamnos americanus de Blainville, 1816). We found that all females spent more time foraging near escape terrain than away from them. Females with young foraged on average 20 m closer to escape terrain than barren females in June, a time when offspring were particularly vulnerable to predation. Plant biomass did not vary with distance to escape terrain in June, but was lower closer than away from escape terrain during all other months. The abundance of forbs and shrubs increased with distance to escape terrain, but their quality did not vary. For grasses and sedges, plant digestible content decreased closer...

Population Dynamics and Harvest Potential of Mountain Goat Herds in Alberta

Abstract The understanding of population dynamics is a central issue for managing large mammals. Modeling has allowed population ecologists to increase their knowledge about complex systems and better predict population responses to diverse perturbations. Mountain goats (Oreamnos americanus) appear sensitive to harvest, but the relative influence of survival and reproductive rates on their population dynamics are not well understood. Using longitudinal data on age- and sex-specific survival and reproduction from a marked mountain goat population in Alberta, Canada, we built a stage-class matrix model to predict short-term numerical changes for 11 other goat populations in Alberta for which the only data available were from annual aerial surveys. Overall, the model provided an acceptable fit to changes in population size for 8 of 12 populations. Temporal trends in population size were underestimated in 2 populations and overestimated in another 2, suggesting that these populations had different vital rates than those of the intensively studied population. Sensitivity analyses revealed that the survival of mature females (aged 5 yr and older) had the greatest elasticity for population growth. Modeled management scenarios indicated that nonselective yearly harvest rates above 1% of goats aged 2 years and older were not sustainable over the short-term for some populations. The simulations also revealed that small (n = 25) and medium-size (n = 50) populations, which correspond to most goat populations in Alberta, had high extinction risk (18 to 82% over 40 years), even in the absence of harvest. Our results confirm that mountain goat populations are very sensitive to harvest, indicate that wildlife managers should prevent female harvest, and suggest that although a high demand for goat hunting exists in Alberta, most populations in this province—and probably small populations elsewhere—cannot withstand exploitation.

Maternal allocation in bison: co‐occurrence of senescence, cost of reproduction, and individual quality

Parental allocation strategies are of profound interest in life history because they directly impact offspring fitness and therefore are highly valuable for understanding population dynamics and informing management decisions. Yet, numerous questions about reproductive allocation patterns for wild populations of large mammals remain unanswered because of the challenges for measuring allocation in the wild. Using a nine-year longitudinal data set on life-history traits of mother-calf bison pairs, we identified sources of variation in relative maternal allocation (calf mass ratio on mother mass) and assessed the occurrence of reproductive costs associated with differential maternal allocation. We found that heavy mothers provided a lower allocation but still produced heavier calves than light mothers. Older females produced lighter calves and tended to decrease allocation as they aged, supporting the occurrence of reproductive senescence. Mothers that had produced a calf the previous year produced lighter calves and allocated less than mothers that did not lactate the previous year, revealing reproductive costs. However, greater maternal allocation did not reduce the probability of breeding in successive years, and the amount of allocation provided by a mother was positively correlated among the offspring she produced, illustrating individual heterogeneity. Although life-history studies are usually classified as either supporting costs of reproduction or individual quality, our study demonstrates that these contrasting evolutionary forces can shape variation within a single trait. Our work illustrates that many processes can coevolve within a population, emphasizing the need to integrate multiple concepts to better understand the evolution of life-history traits. With regard to management of bison herds, if the goal of culling programs is to select for animals with the best performance, this research suggests that managers should account for the condition and previous reproductive status of mothers when taking culling decisions on juvenile bison.

Assessing variation in life‐history tactics within a population using mixture regression models: a practical guide for evolutionary ecologists

Mixed models are now well‐established methods in ecology and evolution because they allow accounting for and quantifying within‐ and between‐individual variation. However, the required normal distribution of the random effects can often be violated by the presence of clusters among subjects, which leads to multi‐modal distributions. In such cases, using what is known as mixture regression models might offer a more appropriate approach. These models are widely used in psychology, sociology, and medicine to describe the diversity of trajectories occurring within a population over time (e.g. psychological development, growth). In ecology and evolution, however, these models are seldom used even though understanding changes in individual trajectories is an active area of research in life‐history studies. Our aim is to demonstrate the value of using mixture models to describe variation in individual life‐history tactics within a population, and hence to promote the use of these models by ecologists and evolutionary ecologists. We first ran a set of simulations to determine whether and when a mixture model allows teasing apart latent clustering, and to contrast the precision and accuracy of estimates obtained from mixture models versus mixed models under a wide range of ecological contexts. We then used empirical data from long‐term studies of large mammals to illustrate the potential of using mixture models for assessing within‐population variation in life‐history tactics. Mixture models performed well in most cases, except for variables following a Bernoulli distribution and when sample size was small. The four selection criteria we evaluated [Akaike information criterion (AIC), Bayesian information criterion (BIC), and two bootstrap methods] performed similarly well, selecting the right number of clusters in most ecological situations. We then showed that the normality of random effects implicitly assumed by evolutionary ecologists when using mixed models was often violated in life‐history data. Mixed models were quite robust to this violation in the sense that fixed effects were unbiased at the population level. However, fixed effects at the cluster level and random effects were better estimated using mixture models. Our empirical analyses demonstrated that using mixture models facilitates the identification of the diversity of growth and reproductive tactics occurring within a population. Therefore, using this modelling framework allows testing for the presence of clusters and, when clusters occur, provides reliable estimates of fixed and random effects for each cluster of the population. In the presence or expectation of clusters, using mixture models offers a suitable extension of mixed models, particularly when evolutionary ecologists aim at identifying how ecological and evolutionary processes change within a population. Mixture regression models therefore provide a valuable addition to the statistical toolbox of evolutionary ecologists. As these models are complex and have their own limitations, we provide recommendations to guide future users.

When relative allocation depends on total resource acquisition: implication for the analysis of trade-offs.

A central tenet of evolutionary biology states that life‐history traits are linked via trade‐offs, as classically exemplified by the van Noordwijk and de Jong model. This model, however, assumes that the relative resource allocation to a biological function varies independently of the total resource acquisition. Based on current empirical evidence, we first explored the dependency between the total resource acquisition and the relative resource allocation to reproduction and showed that such dependency is the rule rather than the exception. We then derived the expression of the covariance between traits when the assumption of independence is relaxed and used simulations to quantify the importance of such dependency on the detection of trade‐offs between current reproduction and future survival. We found that the dependency between the total energy acquisition and the relative allocation to reproduction can influence the probability to detect trade‐offs between survival and reproduction. As a general rule, a negative dependency between the total energy acquisition and the relative allocation to reproduction should lead to a higher probability of detecting a trade‐off in species with a fast pace of life, whereas a positive dependency should lead to a higher probability of detecting a trade‐off in species with a slow pace of life. In addition to confirming the importance of resource variation to reveal trade‐offs, our finding demonstrates that the covariance between resource allocation and resource acquisition is generally not null and also plays a fundamental role in the detection of trade‐offs.