Direct and indirect effects of early-life environment on lifetime fitness of bighorn ewes

Pigeon, Gabriel; Pelletier, Fanie

doi:10.1098/rspb.2017.1935

Cited by 27 publications

(37 citation statements)

References 54 publications

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“…At Ram Mountain, early primiparity did not reduce longevity and was positively associated with lifetime reproductive success (Martin & Festa‐Bianchet, ). High density at birth reduced both longevity and lifetime reproductive success, particularly when density during adulthood was also high (Pigeon & Pelletier, ). In mountain goats (Panagakis, Hamel, & Côté, ), heavier and dominant females tended to attain primiparity earlier and had higher reproductive success early in life.…”

Section: Detecting Costs Of Reproduction Despite Individual Heterogenmentioning

confidence: 99%

“…As density increased, ewes allocated fewer resources to reproduction and more to growth or maintenance. Those changes in allocation led to the somewhat paradoxical result of heavier adult mass at high density for ewes born at intermediate or high density (Pigeon & Pelletier, ). This conservative reproductive tactic has important consequences for population dynamics, because females delay primiparity and reduce maternal care when resources are scarce, leading to lower recruitment (Festa‐Bianchet, Jorgenson, Bérubé, Portier, & Wishart, ; Martin & Festa‐Bianchet, ).…”

Section: The Conservative Reproductive Tactic Of Female Capital Breedmentioning

confidence: 99%

“…This conservative reproductive tactic has important consequences for population dynamics, because females delay primiparity and reduce maternal care when resources are scarce, leading to lower recruitment (Festa‐Bianchet, Jorgenson, Bérubé, Portier, & Wishart, ; Martin & Festa‐Bianchet, ). Fitness costs in bighorn sheep were mostly expressed through reduced lamb survival, as 92% of ewes aged 3 years and older lactated (Pigeon & Pelletier, ). In mountain goats, multiparous females skipped reproduction in about 22% of years, and fitness costs included reproductive pauses (Hamel, Côté, & Festa‐Blanchet, ).…”

Section: The Conservative Reproductive Tactic Of Female Capital Breedmentioning

confidence: 99%

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Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

Festa‐Bianchet

Côté

Hamel

et al. 2019

Journal of Animal Ecology

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Fitness costs of reproduction are expected when resources are limited. Costs drive the evolution of life‐history strategies and can affect population dynamics if females change their allocation of resources to reproduction. We studied fitness costs of reproduction in mountain ungulates in Alberta, Canada. We monitored two populations of bighorn sheep (Ovis canadensis) for 44 and 30 years, and one of mountain goats (Oreamnos americanus) for 30 years. Both species are highly iteroparous. Heterogeneity in individual reproductive potential makes fitness costs of reproduction difficult to detect and quantify without manipulations. In capital breeders, individual differences can be partly accounted for by considering body mass and other correlates of reproductive potential. Long‐term monitoring can reveal costs that only manifest under stressful conditions such as disease or resource scarcity. Despite individual differences in reproductive potential, we detected fitness costs of reproduction in females. Costs, in terms of mass gain and survival, are almost entirely born by subsequent offspring, as mothers prioritize their own maintenance and survival. Costs are greater for primiparous females, decrease with increasing body mass and increase as resource availability declines, and sons are costlier than daughters. Costs may increase for senescent females that appear to reduce allocation to reproduction. In bighorn sheep, costs mostly involve reduced mass gain and lower survival of subsequent offspring. In mountain goats, costs include reductions in mass gain, subsequent fecundity and juvenile survival. In males, fitness costs derive mostly from attempts to reproduce rather than from siring success and likely depend upon individual competitiveness. In the absence of selective harvests, dominant males may enjoy high fitness and possibly lower costs compared to subordinates. The conservative reproductive tactic of mountain ungulate females likely explains why density dependence mostly involves later primiparity and lower recruitment, but rarely affects adult survival. Future research will seek to better account for heterogeneity in reproductive potential, assess cumulative reproductive costs and investigate the potential effects of fathers on maternal allocation tactics.

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Section: Detecting Costs Of Reproduction Despite Individual Heterogenmentioning

confidence: 99%

Section: The Conservative Reproductive Tactic Of Female Capital Breedmentioning

confidence: 99%

Section: The Conservative Reproductive Tactic Of Female Capital Breedmentioning

confidence: 99%

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Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

Festa‐Bianchet

Côté

Hamel

et al. 2019

Journal of Animal Ecology

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“…We take advantage of a detailed long‐term monitoring of wild bighorn sheep ( Ovis canadensis ) to evaluate whether and how early environment influences adult mortality in females and males. In this population, the effects of population density in the year of birth on life span of females have been described (Pigeon, Festa‐Bianchet, & Pelletier, ; Pigeon & Pelletier, ). However, a comparison of the effects of early environment (sensu Lindström, ) on adult mortality in either sex has not been made.…”

Section: Introductionmentioning

confidence: 99%

Trophy hunting mediates sex‐specific associations between early‐life environmental conditions and adult mortality in bighorn sheep

Douhard

Festa‐Bianchet

Landes

et al. 2019

Journal of Animal Ecology

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Environmental conditions during early development, from conception to sexual maturity, can have lasting consequences on fitness components. Although adult life span often accounts for much of the variation in fitness in long‐lived animals, we know little about how early environment affects adult life span in the wild, and even less about whether these effects differ between the sexes. Using data collected over 45 years from wild bighorn sheep (Ovis canadensis), we investigated the effects of early environment on adult mortality in both sexes, distinguishing between natural and anthropogenic sources of mortality. We used the average body mass of yearlings (at about 15 months of age) as a yearly index of environmental quality. We first examined sex differences in natural mortality responses to early environment by censoring harvested males in the year they were shot. We then investigated sex differences in the effects of early environment on overall mortality (natural and hunting mortality combined). Finally, we used path analysis to separate the direct influence of early environment from indirect influences, mediated by age at first reproduction, adult mass and horn length. As early environmental conditions improved, natural adult mortality decreased in both sexes, although for males the effect was not statistically supported. Sex differences in the effects of early environment on adult mortality were detected only when natural and hunting mortality were pooled. Males that experienced favourable early environment had longer horns as adults and died earlier because of trophy hunting, which does not mimic natural mortality. Females that experienced favourable early environment started to reproduce earlier and early primiparity was associated with reduced mortality, suggesting a silver‐spoon effect. Our results show that early conditions affect males and females differently because of trophy hunting. These findings highlight the importance of considering natural and anthropogenic environmental factors across different life stages to understand sex differences in mortality.

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“…For example, in humans, low early life socioeconomic status predicts increased risk of coronary heart disease (2–4), stroke (2, 5, 6), type II diabetes (7), poor perceived health (8), and all-cause mortality (9, 10) in adulthood. Similarly, numerous studies of wild mammals (11–14) and birds (15–17) find that adult fecundity is reduced in animals that experienced adverse early life environments, and a few have also found an effect of early life adversity on adult survival (13–15, 18).…”

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confidence: 99%

Title: Intergenerational effects of early adversity on survival in wild baboons

Zipple

Archie

Tung

et al. 2019

Preprint

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In humans and nonhuman animals, early life adversity can affect an individual's 12 health, survival, and fertility for many years after the adverse experience. However, 13 whether early life adversity also imposes intergenerational effects on the exposed 14 individual's offspring is not well understood. Here, we fill this gap by leveraging 15 prospective, longitudinal data on a wild, long-lived primate. We find that juveniles whose 16 mothers experienced early life adversity exhibit high mortality before age 4, and this effect 17 is independent of the juvenile's own experience of early adversity. Furthermore, our results 18 point towards a strong role for classic parental effects in driving these effects: mothers that 19 experienced early life adversity displayed reduced viability in adulthood, which in turn led 20 to reductions in offspring survival. Importantly, these mothers' juvenile offspring often 21 preceded them in death by 1 to 2 years, indicating that, for high adversity mothers, the 22 quality of maternal care declines near the end of life. While we cannot exclude direct effects 23 of a parent's environment on offspring quality (e.g., transgenerational epigenetic changes), 24 our results are most consistent with a classic parental effect, in which the environment 25 experienced by a parent affects its future phenotype and therefore its offspring's 26 phenotype. Together, our findings demonstrate that adversity experienced by individuals 27 in one generation can have strong effects on the survival of offspring in the next generation, 28 even if those offspring did not themselves experience early adversity. 29 An individual's health, survival, and fertility can be profoundly shaped by its early life 30 environment (1). For example, in humans, low early life socioeconomic status predicts increased 31 risk of coronary heart disease (2-4), stroke (2, 5, 6), type II diabetes (7), poor perceived health 32 (8), and all-cause mortality (9, 10) in adulthood. Similarly, numerous studies of wild mammals 33 (11-14) and birds (15-17) find that adult fecundity is reduced in animals that experienced 34 adverse early life environments, and a few have also found an effect of early life adversity on 35 adult survival (13)(14)(15) 18). 36 If the effects of early adversity extend to the descendants of exposed individuals, the 37 epidemiological and evolutionary impact of these effects would be further amplified. However, 38 evidence from humans for intergenerational effects that result directly from the early life 39 experience of the parent is mixed, as studies have produced somewhat contradictory results (19-40 22). For example, a study of the Överkalix population in Sweden identified strong, contrasting 41 effects of grandparents' exposure to early-life food scarcity on grand-offspring survival, 42 depending on small differences in the age at which the grandparent was exposed to scarcity (22). 43Similarly, two studies of the same population exposed in utero to the Dutch hunger winter (a 44 well-studied famine th...

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Direct and indirect effects of early-life environment on lifetime fitness of bighorn ewes

Cited by 27 publications

References 54 publications

Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

Trophy hunting mediates sex‐specific associations between early‐life environmental conditions and adult mortality in bighorn sheep

Title: Intergenerational effects of early adversity on survival in wild baboons

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