Understanding variation in metabolic rate Pettersen, Amanda K; Marshall, Dustin J; White, Craig R
Journal of experimental biology,
01/2018, Volume:
221, Issue:
Pt 1
Journal Article
Peer reviewed
Open access
Metabolic rate reflects an organism's capacity for growth, maintenance and reproduction, and is likely to be a target of selection. Physiologists have long sought to understand the causes and ...consequences of within-individual to among-species variation in metabolic rates - how metabolic rates relate to performance and how they should evolve. Traditionally, this has been viewed from a mechanistic perspective, relying primarily on hypothesis-driven approaches. A more agnostic, but ultimately more powerful tool for understanding the dynamics of phenotypic variation is through use of the breeder's equation, because variation in metabolic rate is likely to be a consequence of underlying microevolutionary processes. Here we show that metabolic rates are often significantly heritable, and are therefore free to evolve under selection. We note, however, that 'metabolic rate' is not a single trait: in addition to the obvious differences between metabolic levels (e.g. basal, resting, free-living, maximal), metabolic rate changes through ontogeny and in response to a range of extrinsic factors, and is therefore subject to multivariate constraint and selection. We emphasize three key advantages of studying metabolic rate within a quantitative genetics framework: its formalism, and its predictive and comparative power. We make several recommendations when applying a quantitative genetics framework: (i) measuring selection based on actual fitness, rather than proxies for fitness; (ii) considering the genetic covariances between metabolic rates throughout ontogeny; and (iii) estimating genetic covariances between metabolic rates and other traits. A quantitative genetics framework provides the means for quantifying the evolutionary potential of metabolic rate and why variance in metabolic rates within populations might be maintained.
Environmental temperature is a key driver of variation in developmental physiological rates in reptiles. Cooler temperatures extend development time and can increase the amount of energy required to ...achieve hatching success, which can pose fitness consequences later in life. Yet, for locally-adapted populations, genetic variation can oppose environmental variation across ecological gradients, known as countergradient variation (CnGV). Biologists often seek to understand the presence of phenotypic variation, yet the absence of such variation across environmental gradients can also reveal insights into the mechanisms underlying local adaptation. While evidence for genetic variation opposing environmental variation in physiological rates has been summarized in other taxa, the generality of CnGV variation in reptiles is yet unknown. Here I present a summary of studies measuring development time and metabolic rates in locally-adapted populations across thermal clines for 15 species of reptiles across 8 families. CnGV in development time is found to be common, while no clear pattern emerges for the thermal sensitivity of metabolic rates across locally-adapted populations. CnGV in development time may be an adaptive response in order to decrease the costly development in cool climates, however, empirical work is needed to disentangle plastic from genetic responses, and to uncover potentially general mechanisms of local thermal adaptation in reptiles.
Metabolic rates are linked to key life-history traits that are thought to set the pace of life and affect fitness, yet the role that parents may have in shaping the metabolism of their offspring to ...enhance survival remains unclear. Here, we investigated the effect of temperature (24°C or 30°C) and feeding frequency experienced by parent zebrafish (
) on offspring phenotypes and early survival at different developmental temperatures (24°C or 30°C). We found that embryo size was larger, but survival lower, in offspring from the parental low food treatment. Parents exposed to the warmer temperature and lower food treatment also produced offspring with lower standard metabolic rates-aligning with selection on embryo metabolic rates. Lower metabolic rates were correlated with reduced developmental and growth rates, suggesting selection for a slow pace of life. Our results show that intergenerational phenotypic plasticity on offspring size and metabolic rate can be adaptive when parent and offspring temperatures are matched: the direction of selection on embryo size and metabolism aligned with intergenerational plasticity towards lower metabolism at higher temperatures, particularly in offspring from low-condition parents. These findings provide evidence for adaptive parental effects, but only when parental and offspring environments match. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.
Offspring size is a key functional trait that can affect all phases of the life history, from birth to reproduction, and is common to all the Metazoa. Despite its ubiquity, reviews of this trait tend ...to be taxon‐specific. We explored the causes and consequences of offspring size variation across plants, invertebrates and vertebrates.
We find that offspring size shows clear latitudinal patterns among species: fish, amphibians, invertebrates and birds show a positive covariation in offspring size with latitude; plants and turtles show a negative covariation with latitude. We highlight the developmental window hypothesis as an explanation for why plants and turtles show negative covariance with latitude. Meanwhile, we find evidence for stronger, positive selection on offspring size at higher latitudes for most animals.
Offspring size also varies at all scales of organization, from populations through to broods from the same female. We explore the reasons for this variation and suspect that much of this variation is adaptive, but in many cases, there are too few tests to generalize.
We show that larger offspring lose relatively less energy during development to independence such that larger offspring may have greater net energy budgets than smaller offspring. Larger offspring therefore enter the independent phase with relatively more energy reserves than smaller offspring. This may explain why larger offspring tend to outperform smaller offspring but more work on how offspring size affects energy acquisition is needed.
While life‐history theorists have been fascinated by offspring size for over a century, key knowledge gaps remain. One important next step is to estimate the true energy costs of producing offspring of different sizes and numbers.
A plain language summary is available for this article.
Plain Language Summary
Abstract
Quantifying how variable temperature regimes affect energy expenditure during development is crucial for understanding how future thermal regimes may impact early life survival and ...population persistence.
Developmental cost theory (DCT) suggests that there is an optimal temperature (T
opt
) that minimises energy expenditure during development (the ‘cost of development‘). Exposure to fluctuating temperatures around an average of T
opt
is anticipated to increase either development time or metabolic rate. As a result, embryos will rapidly deplete yolk reserves, and consequently hatch at a smaller size or with less residual yolk to support postnatal survival and growth.
Here, we studied total embryonic energy expenditure (development time and rate of CO
2
production) and conversion of yolk into tissue in common wall lizards (
Podarcis muralis
) under three incubation treatments anticipated, based on DCT, to increase the cost of development: no variance (T
opt
constant, 24°C), low variance (22°C–26°C) and high variance (18°C–30°C).
As predicted, we found that increasing variance around T
opt
increased the cost of development, despite reducing time to hatching. As a consequence, embryos on average hatched with 59% lower residual yolk reserves under high variance versus the constant incubation temperature treatment.
Our results highlight how the relative temperature sensitivities of development time and metabolic rate determine the cost of development, which in turn may predict the ability of egg‐laying ectotherms to persist in variable environments. We show that DCT can provide a mechanistic framework for understanding the widespread, but often seemingly idiosyncratic, effects of fluctuating incubation temperatures on hatchling tissue and residual yolk mass.
Read the free
Plain Language Summary
for this article on the Journal blog.
Metabolic rate reflects the ‘pace of life’ in every organism. Metabolic rate is related to an organism's capacity for essential maintenance, growth and reproduction—all of which interact to affect ...fitness. Although thousands of measurements of metabolic rate have been made, the microevolutionary forces that shape metabolic rate remain poorly resolved. The relationship between metabolic rate and components of fitness are often inconsistent, possibly because these fitness components incompletely map to actual fitness and often negatively covary with each other. Here we measure metabolic rate across ontogeny and monitor its effects on actual fitness (lifetime reproductive output) for a marine bryozoan in the field. We also measure key components of fitness throughout the entire life history including growth rate, longevity and age at the onset of reproduction. We found that correlational selection favours individuals with higher metabolic rates in one stage and lower metabolic rates in the other—individuals with similar metabolic rates in each developmental stage displayed the lowest fitness. Furthermore, individuals with the lowest metabolic rates lived for longer and reproduced more, but they also grew more slowly and took longer to reproduce initially. That metabolic rate is related to the pace of the life history in nature has long been suggested by macroevolutionary patterns but this study reveals the microevolutionary processes that probably generated these patterns.
Size at the start of life reflects the initial per offspring parental investment - including both the embryo and the nutrients supplied to it. Initial offspring size can vary substantially both ...within and among species. Within species, increasing offspring size can enhance growth, reproduction, competitive ability, and reduce susceptibility to predation and starvation later in life, that can ultimately increase fitness. Previous work has suggested that the fitness benefits of larger offspring size may be driven by energy expenditure during development - or how offspring metabolic rate scales with offspring size. Despite the importance of early life energy expenditure in shaping later life fitness trajectories, consideration of among-species scaling of metabolic rate at the time of birth as a potential source of general metabolic scaling patterns has been overlooked by theory. Here we review the patterns and processes of energy expenditure at the start of life when mortality is often greatest. We compile existing data on metabolic rate and offspring size for 191 ectotherm species spanning eight phyla and use phylogenetically-controlled methods to quantify among-species scaling patterns. Across a 109-fold mass range, we find that offspring metabolic rate scales hypometrically with size, with an overall scaling exponent of 0.66. This exponent varies across ontogenetic stage and feeding activity, but is consistently hypometric, including across environmental temperatures. Despite differences in parental investment, life history and habitat, large-offspring species use relatively less energy as a proportion of size, compared with small-offspring species. Greater residual energy can be used to fuel the next stages of life, particularly in low resource environments. Based on available evidence, we conclude that, while large knowledge gaps remain, the evolution of offspring size is likely shaped by context-dependent selection acting on correlated traits, including metabolic rates maintaining hypometric scaling, that operates within broader physical constraints.
Preserving biodiversity over time is a pressing challenge for conservation science. A key goal of marine protected areas (MPAs) is to maintain stability in species composition, via reduced turnover, ...to support ecosystem function. Yet, this stability is rarely measured directly under different levels of protection. Rather, evaluations of MPA efficacy generally consist of static measures of abundance, species richness, and biomass, and rare measures of turnover are limited to short‐term studies involving pairwise (beta diversity) comparisons. Zeta diversity is a recently developed metric of turnover that allows for measurement of compositional similarity across multiple assemblages and thus provides more comprehensive estimates of turnover. We evaluated the effectiveness of MPAs at preserving fish zeta diversity across a network of marine reserves over 10 years in Batemans Marine Park, Australia. Snorkel transect surveys were conducted across multiple replicated and spatially interspersed sites to record fish species occurrence through time. Protection provided by MPAs conferred greater stability in fish species turnover. Marine protected areas had significantly shallower decline in zeta diversity compared with partially protected and unprotected areas. The retention of harvested species was four to six times greater in MPAs compared with partially protected and unprotected areas, and the stabilizing effects of protection were observable within 4 years of park implementation. Conversely, partial protection offered little to no improvement in stability, compared with unprotected areas. These findings support the efficacy of MPAs for preserving temporal fish diversity stability. The implementation of MPAs helps stabilize fish diversity and may, therefore, support biodiversity resilience under ongoing environmental change.
Impactos de las Áreas Protegidas Marinas sobre la Estabilidad Temporal de la Diversidad de Especies de Peces
Resumen
A medida que avanza el tiempo, la conservación de la biodiversidad es un reto apremiante para las ciencias de la conservación. Un objetivo importante de las áreas marinas protegidas (AMP) es mantener la estabilidad de la composición de especies, por medio de rotaciones reducidas, para así ayudar a la función del ecosistema. Sin embargo, esta estabilidad casi no se mide directamente bajo diferentes niveles de protección. En su lugar, las evaluaciones de eficiencia de las AMP generalmente consisten en medidas estáticas de abundancia, riqueza de especies y biomasa, y las pocas medidas de la rotación están limitadas a los estudios a corto plazo que involucran comparaciones por pares (diversidad beta). La diversidad zeta es una medida recientemente desarrollada de la rotación, la cual permite la medición de las similitudes en la composición en múltiples ensamblajes, proporcionando así estimaciones más completas de la rotación. Evaluamos la efectividad que tienen las AMP en la conservación de la diversidad zeta de los peces en una red de reservas marinas durante diez años en el Parque Marino Bateman, Australia. Se realizaron censos en transecto con snorkel en varios sitios replicados e intercalados espacialmente para registrar la presencia de especies de peces a lo largo del tiempo. La protección proporcionada por las AMP otorgó una mayor estabilidad en la rotación de especies de peces. Las áreas marinas protegidas tuvieron una declinación significativamente más baja de la diversidad zeta que las áreas parcialmente protegidas o desprotegidas. La retención de especies pescadas fue 4–6 veces mayor en las AMP que en las áreas desprotegidas o parcialmente protegidas, y los efectos estabilizadores de la protección fueron observables a partir de cuatro años de la implementación del parque. De manera opuesta, la protección parcial ofreció poca o ninguna estabilidad, comparada con las áreas desprotegidas. Estos descubrimientos respaldan la eficiencia que tienen las AMP en la conservación de la estabilidad temporal de la diversidad de especies de peces. La implementación de las AMP ayuda a estabilizar la diversidad de peces y por lo tanto puede fomentar la resiliencia de la biodiversidad frente al cambio ambiental en curso.
摘要海洋保护区对鱼类物种多样性时间稳定性的影响
【摘要】对生物多样性的长期保护是保护科学面临的一项紧迫挑战。海洋保护区 (MPAs) 的一个关键目标是通过降低周转率来维持物种组成稳定, 以支持生态系统功能。然而, 很少有研究直接测量不同保护级别的海洋中的物种稳定性。相反, 海洋保护区的有效性评估则通常包括对丰度、物种丰富度和生物量的静态测量, 少有的周转率量度也仅限于涉及成对 (beta 多样性) 比较的短期研究。 Zeta 多样性是近期发展起来的周转率指标, 它可以测量多个群集的物种组成相似性, 从而提供更全面的周转率估计。本研究利用澳大利亚贝特曼海岸公园超过十年的海洋保护区网络, 估计了海洋保护区在保护鱼类 zeta 多样性方面的有效性。我们通过在空间上分散的多个位点进行重复的浮潜样带调查, 记录了不同时期鱼类物种的出现情况。结果发现, 海洋保护区提供的保护使鱼类物种周转更加稳定。相比于部分保护区和未保护位点, 海洋保护区 zeta 多样性下降明显更为缓和, 且对渔获物种的保留率高出 4‐6 倍, 这种保护带来的稳定性成效可以在建立海岸公园的四年内观测到。相反, 部分保护区与未受保护位点相比, 在稳定性方面几乎没有改善。这些发现支持了海洋保护区在保护鱼类多样性时间稳定性方面的有效性。海洋保护区的建立有助于稳定鱼类多样性, 因此可以支持持续环境变化背景下的生物多样性恢复力。【翻译: 胡怡思; 审校: 聂永刚】
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