Low Heritability but Significant Early Environmental Effects on Resting Metabolic Rate in a Wild Passerine

McFarlane, S. Eryn; Ålund, Murielle; Sirkiä, Päivi M.; Qvarnström, Anna

doi:10.1086/715842

Cited by 7 publications

(6 citation statements)

References 62 publications

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“…Indeed, our study demonstrates that both genetic inheritance (but also complementary mechanisms, such as parental effects before the cross-fostering) and the rearing environment contribute to variation in offspring mitochondrial traits, but with a larger contribution from the rearing environment. Similar results about lower contribution of familial background have been found for resting metabolic rate in collared flycatcher nestlings (Ficedula albicollis) (McFarlane et al, 2021). While the underlying mechanisms of modulation of mitochondria by early-life environmental conditions are unknown, recent research points out that mitochondrial function can respond to environmental cues through changes in gene expression and mitochondrial DNA methylation (Sharma et al, 2019;Wallace, 2016).…”

Section: Correlative Approachsupporting

confidence: 69%

Early-life environmental effects on mitochondrial aerobic metabolism: an experimental brood size manipulation in wild great tits

Cossin-Sevrin

Stier

Hukkanen

et al. 2023

Preprint

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Parental care (including postnatal provisioning) is a major component of the offspring early-life environment. In avian species, the number of chicks in the nest and subsequent sibling competition for food are known to affect chick growth, leading in some cases to long-lasting effects for the offspring. Because of its central role in converting energy, variation in the offspring mitochondrial metabolism could be an important pathway underlying variation in growth patterns. Here, we performed a brood size manipulation in great tits (Parus major) to unravel its impact on offspring mitochondrial metabolism and reactive oxygen species (ROS) production in red blood cells. We investigated the effects of brood size on chicks growth and survival, and tested for long-lasting effects on juvenile mitochondrial metabolism and phenotype. As expected, chicks raised in reduced broods had a higher body mass compared to enlarged and control groups. However, mitochondrial metabolism and ROS production were not significantly affected by the treatment either at chick or juvenile stages. Chicks in very small broods were smaller in size and had higher mitochondrial metabolic rates. The nest of rearing has a significant effect on nestling mitochondrial metabolism, yet variation in mitochondrial metabolism at the early-life stages are not associated with survival chances. The contribution of the rearing environment in determining offspring mitochondrial metabolism emphasizes the plasticity of mitochondrial metabolism in changing environments. Further studies would be needed to closely investigate what are the major environmental cues affecting the offspring mitochondrial metabolism during the growth period.

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Section: Correlative Approachsupporting

confidence: 69%

Early-life environmental effects on mitochondrial aerobic metabolism: an experimental brood size manipulation in wild great tits

Cossin-Sevrin

Stier

Hukkanen

et al. 2023

Preprint

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“…Mixed evidence shows that metabolism is sometimes under selection (e.g. [13][14][15]) and is somewhat heritable [16][17][18] and repeatable [19,20], suggesting that the fitness consequences of slow and fast metabolic rates are context-dependent [21,22]. It is unresolved whether metabolism has evolved as a driver or simply a by-product of the pace of life.…”

Section: Introductionmentioning

confidence: 99%

Intergenerational plasticity aligns with temperature-dependent selection on offspring metabolic rates

Pettersen,

Metcalfe,

Seebacher

2024

Phil. Trans. R. Soc. B

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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 ( Danio rerio ) 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’.

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“…This, in turn, can explain why RMR or BMR typically has high heritability (e.g. Nilsson et al, 2009; but see McFarlane et al, 2021) and is subjected to differential selection depending on environmental context (Nilsson and Nilsson, 2016). Thus, understanding the proximal drivers of variation in metabolic rate in natural populations is essential to better understand how environmental conditions shape metabolic phenotypes.…”

Section: Introductionmentioning

confidence: 99%

Permeabilization status affects the relationship between basal metabolic rate and mitochondrial respiration in great tit blood cells

Thoral

Garcia-Diaz

Persson

et al. 2023

Preprint

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Although mitochondrial respiration is believed to explain a substantial part of the variation in whole-animal basal (BMR) or resting metabolic rate (RMR), few studies have addressed the relationship between organismal and cellular metabolism and how this may vary in environments where individual demands for energy differ. We investigated the relationship between whole-individual metabolic rate, measured in temperatures ranging thermoneutrality to far below thermoneutrality, and mitochondrial respiration of intact or permeabilized blood cells in two separate studies on wild great tits (Parus major L.). Our results show that, in permeabilized cells, there are significant positive relationships between BMR or RMR and several mitochondrial traits, including phosphorylating respiration rate through both complexes I and II (i.e., OXPHOS respiration). However, surprisingly, the LEAK respiration (i.e., basal respiration that mainly counteract for proton leakage) was not related to BMR or RMR. When measurements were performed using intact blood cells, BMR was positively related to ROUTINE respiration (i.e., mitochondrial respiration on endogenous substrates) in one of the two studies, but no other mitochondrial traits could explain variation in BMR or RMR in any thermal environment. These studies seem to show that the level of activation of mitochondrial metabolism as well as the permeabilization status of blood cells play a primary role on the extent to which blood metabolism might explain variations in the whole-individual metabolic rate.

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Low Heritability but Significant Early Environmental Effects on Resting Metabolic Rate in a Wild Passerine

Cited by 7 publications

References 62 publications

Early-life environmental effects on mitochondrial aerobic metabolism: an experimental brood size manipulation in wild great tits

Early-life environmental effects on mitochondrial aerobic metabolism: an experimental brood size manipulation in wild great tits

Intergenerational plasticity aligns with temperature-dependent selection on offspring metabolic rates

Permeabilization status affects the relationship between basal metabolic rate and mitochondrial respiration in great tit blood cells

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