Not that hot after all: no limits to heat dissipation in lactating mice selected for high or low BMR

Sadowska, Julita; Gębczyński, Andrzej K.; Lewoc, Małgorzata; Konarzewski, Marek

doi:10.1242/jeb.204669

Cited by 17 publications

(18 citation statements)

References 45 publications

(55 reference statements)

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“…In the present study, food intake, digestive energy intake, milk energy output or litter mass did not differ between F1 female adults that previously weaned at 32.5 and 21°C when they were lactating at 21°C. Consistent with these data, Swiss mice artificially selected for either high or low basal metabolic rate, which had had fur from the dorsal body surface removed to increase their thermal conductance and facilitate heat dissipation, did not benefit from increasing their thermal conductance at peak lactation (Sadowska et al, 2019). This is also consistent with previous data which indicate at 21°C that this strain is probably not limited by the capacity for heat dissipation (Wen et al, 2017).…”

Section: Discussionsupporting

confidence: 90%

Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

Bao

Chen

Hambly

et al. 2020

Journal of Experimental Biology

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Exposure to high temperatures (heatwaves) is rapidly emerging as an important issue of climate change, in particular for female mammals during lactation. High temperatures adversely affect the ability to dissipate heat, which has negative effects on reproductive output. The cumulative effects on growth of F1 offspring after weaning, and future reproductive performance of offspring, remain uncertain. In this study, F1 mice weaned from mothers lactating at 21 and 32.5°C were housed at 21°C from day 19 until day 56 of age, during which food intake and body mass were measured. The F1 adult females that were weaned at the two temperatures were bred and then exposed to 32.5°C during lactation. Energy intake and milk output, and litter size and mass, were determined. The F1 adults weaned at 32.5°C consumed less food and had lower body mass than their counterparts weaned at 21°C. Several visceral organs or reproductive tissues were significantly lower in mass in F1 weaned at 32.5°C than at 21°C. The exposure to 32.5°C significantly decreased energy intake, milk output and litter mass in F1 adult females during lactation. The F1 adult females weaned at 32.5°C produced less milk and raised lighter pups than those previously weaned at 21°C. The data suggest that transient exposure to hot temperatures during lactation has longlasting impacts on offspring, including stunted growth and decreases in future reproductive performance when adult. This indicates that the offspring of females previously experiencing hot temperatures have a significant fitness disadvantage.

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Section: Discussionsupporting

confidence: 90%

Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

Bao

Chen

Hambly

et al. 2020

Journal of Experimental Biology

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“…Nestling‐feeding blue tits ( Cyanistes caeruleus ) with removed ventral plumage sired larger nestlings, maintained lower temperature and lost less body mass (Nord, Nilsson, & Portugal, 2018). However, other studies on reproducing mammals did not support HDL predictions (Zhao, Chi, & Cao, 2010; Sadowska et al ., 2019), thus casting doubt on its generality. Furthermore, reproducing mammals or birds do not lose fur or feathers, which is likely because of the risk of death if the temperature suddenly drops, which would on average decrease their lifetime reproductive success.…”

Section: Mechanistic Explanation Of Hypoallometric Mr Scalingmentioning

confidence: 99%

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

2020

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Despite many decades of research, the allometric scaling of metabolic rates (MRs) remains poorly understood. Here, we argue that scaling exponents of these allometries do not themselves mirror one universal law of nature but instead statistically approximate the non‐linearity of the relationship between MR and body mass. This ‘statistical’ view must be replaced with the life‐history perspective that ‘allows’ organisms to evolve myriad different life strategies with distinct physiological features. We posit that the hypoallometric allometry of MRs (mass scaling with an exponent smaller than 1) is an indirect outcome of the selective pressure of ecological mortality on allocation ‘decisions’ that divide resources among growth, reproduction, and the basic metabolic costs of repair and maintenance reflected in the standard or basal metabolic rate (SMR or BMR), which are customarily subjected to allometric analyses. Those ‘decisions’ form a wealth of life‐history variation that can be defined based on the axis dictated by ecological mortality and the axis governed by the efficiency of energy use. We link this variation as well as hypoallometric scaling to the mechanistic determinants of MR, such as metabolically inert component proportions, internal organ relative size and activity, cell size and cell membrane composition, and muscle contributions to dramatic metabolic shifts between the resting and active states. The multitude of mechanisms determining MR leads us to conclude that the quest for a single‐cause explanation of the mass scaling of MRs is futile. We argue that an explanation based on the theory of life‐history evolution is the best way forward.

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“…Explanations of the limits on female lactation performance are disputed. The 'central limitation' hypothesis suggests that the limits are imposed by the uptake capacity of the energy-supplying machinery (such as the alimentary tract and associated organs) (Perrigo, 1987;Diamond, 1992, 1994;Koteja, 1996;Thurber et al, 2019;Sadowska et al, 2019). More recent evidence in small mammals tends to support the 'peripheral limitation' or 'heat dissipation limitation' (HDL) theories.…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, surgically removing half of the mammary glands in Swiss mice had an impact on pup growth (Hammond et al, 1996), which also supports the idea that the mammary gland imposes the limit on milk production capacity at room temperature in this strain. Another study in artificially selected Swiss mice (high and low basal metabolic rate lines) showed that the lactation performance of both lines did not benefit from increasing their thermal conductance at peak lactation by fur removal (Sadowska et al, 2019). This also suggested that the limit was not imposed by heat dissipation capacity, but rather by the spare capacity of the alimentary tract and other organs to respond to such sudden energy demand (Sadowska et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Limits to Sustained Energy Intake XXXI: Effect of Graded Levels of Dietary Fat on Lactation Performance in Swiss Mice

Huang

Mendoza

Hambly

et al. 2020

Journal of Experimental Biology

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The heat dissipation limit theory predicts that lactating female mice consuming diets with lower specific dynamic action (SDA) should have enhanced lactation performance. Dietary fat has lower SDA than other macronutrients. Here we tested the effects of graded dietary fat levels on lactating Swiss mice. We fed females five diets varying in fat content from 8.3 to 66.6%. Offspring of mothers fed diets of 41.7% fat and above were heavier and fatter at weaning compared with those of 8.3 and 25% fat diets. Mice on dietary fat contents of 41.7% and above had greater metabolizable energy intake at peak

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Not that hot after all: no limits to heat dissipation in lactating mice selected for high or low BMR

Cited by 17 publications

References 45 publications

Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective

Limits to Sustained Energy Intake XXXI: Effect of Graded Levels of Dietary Fat on Lactation Performance in Swiss Mice

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