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Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder.

ABSTRACT: Judicious management of energy can be invaluable for animal survival and reproductive success. Capital breeding mammals typically transfer energy to their young at extremely high rates while undergoing prolonged fasting, making lactation a tremendously energy demanding period. Effective management of the competing demands of the mother's energy needs and those of her offspring is presumably fundamental to maximizing lifetime reproductive success. How does the mother maximize her chances of successfully rearing her pup, by ensuring that both her pup and herself have sufficient energy during this 'energetic fast'? While energy management models were first discussed in the 1990s, application of this analytical technique is still very much in its infancy. Recent work suggests that a broad range of species exhibits 'energy compensation'; during periods when they expend more energy on activity, their bodies partially compensate by reducing background (basal) metabolic rate as an adaptation to limit overall energy expenditure. However, the value of energy management models in understanding animal ecology is presently unclear. We investigate whether energy management models provide insights into the breeding strategy of phocid seals. Not only do we expect lactating seals to display energy compensation because of their breeding strategy of high energy transfer while fasting, but we anticipate that mothers exhibiting a lack of energy compensation are less likely to rear offspring successfully. On the Isle of May in Scotland, we collected heart rate data as a proxy for energy expenditure in 52 known individual grey seal (Halichoerus grypus) mothers, repeatedly across 3 years of breeding. We provide evidence that grey seal mothers typically exhibit energy compensation during lactation by downregulating their background metabolic rate to limit daily energy expenditure during periods when other energy costs are relatively high. However, individuals that fail to energy compensate during the lactation period are more likely to end lactation earlier than expected. Our study is the first to demonstrate the importance of energy compensation to an animal's reproductive expenditure. Moreover, our multi-seasonal data indicate that environmental stressors may reduce the capacity of some individuals to follow the energy compensation strategy.

SUBMITTER: Shuert CR

PROVIDER: S-EPMC7693042 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder.

Shuert Courtney R CR Halsey Lewis G LG Pomeroy Patrick P PP Twiss Sean D SD

The Journal of animal ecology 20200907 11

Judicious management of energy can be invaluable for animal survival and reproductive success. Capital breeding mammals typically transfer energy to their young at extremely high rates while undergoing prolonged fasting, making lactation a tremendously energy demanding period. Effective management of the competing demands of the mother's energy needs and those of her offspring is presumably fundamental to maximizing lifetime reproductive success. How does the mother maximize her chances of succe ...[more]

PMID: 32895978

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Project description:Alternative migratory strategies can coexist within animal populations and species. Anthropogenic impacts can shift the fitness balance between these strategies leading to changes in migratory behaviors. Yet some of the mechanisms that drive such changes remain poorly understood. Here we investigate the phenotypic differences, and the energetic, behavioral, and fitness trade-offs associated with four different movement strategies (long-distance and short-distance migration, and regional and local residency) in a population of white storks (Ciconia ciconia) that has shifted its migratory behavior over the last decades, from fully long-distance migration toward year-round residency. To do this, we tracked 75 adult storks fitted with GPS/GSM loggers with tri-axial acceleration sensors over 5 years, and estimated individual displacement, behavior, and overall dynamic body acceleration, a proxy for activity-related energy expenditure. Additionally, we monitored nesting colonies to assess individual survival and breeding success. We found that long-distance migrants traveled thousands of kilometers more throughout the year, spent more energy, and >10% less time resting compared with short-distance migrants and residents. Long-distance migrants also spent on average more energy per unit of time while foraging, and less energy per unit of time while soaring. Migratory individuals also occupied their nests later than resident ones, later occupation led to later laying dates and a lower number of fledglings. However, we did not find significant differences in survival probability. Finally, we found phenotypic differences in the migratory probability, as smaller sized individuals were more likely to migrate, and they might be incurring higher energetic and fitness costs than larger ones. Our results shed light on the shifting migratory strategies in a partially migratory population and highlight the nuances of anthropogenic impacts on species behavior, fitness, and evolutionary dynamics.

Project description:Trade-offs between life history traits are expected to occur due to the limited amount of resources that organisms can obtain and share among biological functions, but are of least concern for selection responses in nutrient-rich or benign environments. In domestic animals, selection limits have not yet been reached despite strong selection for higher meat, milk or egg yields. Yet, negative genetic correlations between productivity traits and health or fertility traits have often been reported, supporting the view that trade-offs do occur in the context of nonlimiting resources. The importance of allocation mechanisms in limiting genetic changes can thus be questioned when animals are mostly constrained by their time to acquire and process energy rather than by feed availability. Selection for high productivity traits early in life should promote a fast metabolism with less energy allocated to self-maintenance (contributing to soma preservation and repair). Consequently, the capacity to breed shortly after an intensive period of production or to remain healthy should be compromised. We assessed those predictions in mammalian and avian livestock and related laboratory model species. First, we surveyed studies that compared energy allocation to maintenance between breeds or lines of contrasting productivity but found little support for the occurrence of an energy allocation trade-off. Second, selection experiments for lower feed intake per unit of product (i.e. higher feed efficiency) generally resulted in reduced allocation to maintenance, but this did not entail fitness costs in terms of survival or future reproduction. These findings indicate that the consequences of a particular selection in domestic animals are much more difficult to predict than one could anticipate from the energy allocation framework alone. Future developments to predict the contribution of time constraints and trade-offs to selection limits will be insightful to breed livestock in increasingly challenging environments.

Project description:Background: Some individuals appear prone to multiple adverse outcomes, including poor health, school dropout, risky behavior and early reproduction. This clustering remains poorly understood. Drawing on evolutionary life history theory, we hypothesized that maternal investment in early life would predict the developmental trajectory and adult phenotype of female offspring. Specifically, we predicted that daughters receiving low investment would prioritize the life history functions of "reproduction" and "defense" over "growth" and "maintenance," increasing the risk of several adverse outcomes. Methods: We investigated 2,091 mother-daughter dyads from a birth cohort in Pelotas, Brazil. We combined data on maternal height, body mass index, income, and education into a composite index of "maternal capital." Daughter outcomes included reproductive status at 18 years, growth, adult anthropometry, body composition, cardio-metabolic risk, educational attainment, work status, and risky behavior. We tested whether daughters' early reproduction (<18 years) and exposure to low maternal capital were associated with adverse outcomes, and whether this accounted for the clustering of adverse outcomes within individuals. Results: Daughters reproducing early were shorter, more centrally adipose, had less education and demonstrated more risky behavior compared to those not reproducing. Low maternal capital was associated with greater likelihood of the daughter reproducing early, smoking and having committed violent crime. High maternal capital was positively associated with the daughter's birth weight and adult size, and the likelihood of being in school. Associations of maternal capital with cardio-metabolic risk were inconsistent. Daughters reproducing early comprised 14.8% of the population, but accounted for 18% of obesity; 20% of violent crime, low birth weight and short stature; 32% of current smoking; and 52% of school dropout. Exposure to low maternal capital contributed similarly to the clustering of adverse outcomes among daughters. Outcomes were worst among daughters characterized by both low maternal capital and early reproduction. Conclusion: Consistent with life history theory, daughters exposed to low maternal capital demonstrate "future discounting" in behavior and physiology, prioritizing early reproduction over growth, education, and health. Trade-offs associated with low maternal capital and early reproduction contribute to clustering of adverse outcomes. Our approach provides new insight into inter-generational cycles of disadvantage.

Dataset Information

Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder.

Publications

Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder.

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