Muscle nonshivering thermogenesis in a feral mammal

Abstract

While small mammals and neonates are able to maintain an optimal body temperature (Tb) independent of ambient conditions by producing heat via nonshivering thermogenesis (NST) in the brown adipose tissue (BAT), larger mammals and other mammals lacking BAT were long believed to rely primarily on shivering and behavioural adaptations. However, recently, a second mechanism of NST was found in skeletal muscle that could play an important role in thermoregulation of such species. Muscle NST is independent of muscle contractions and produces heat based on the activity of an ATPase pump in the sarcoplasmic reticulum (SERCA1a) and controlled by the protein sarcolipin. To evaluate whether muscle NST could indeed play an important role in thermoregulation in species lacking BAT, we investigated the thermogenic capacities of new-born wild boar piglets. During cold exposure over the first 5 days of life, total heat production was improved while shivering intensity decreased, indicating an increasing contribution of NST. Sampling skeletal muscle tissue for analyses of SERCA activity as well as gene expression of SERCA1a and sarcolipin, we found an age-related increase in all three variables as well as in Tb. Hence, the improved thermogenesis during the development of wild boars is not due to shivering but explained by the observed increase in SERCA activity. Our results suggest that muscle NST may be the primary mechanism of heat production during cold stress in large mammals lacking BAT, strengthening the hypothesis that muscle NST has likely played an important role in the evolution of endothermy.

Thermoregulation in the wild boar (Sus scrofa)

“…One might be tempted to think that in wild boars NST, in the absence of UCP1, plays no role. However, another type of NST, driven by the SERCA pump in muscles, enables juvenile wild boars to generate heat, while shivering is diminishing (Nowack et al 2019 ). This type of NST is also present in pigs, the domestic form of wild boar, and seems to be widespread even within adult mammals (Berthon et al 1994 ; Nowack et al 2017 ).…”

Thermoregulation in the wild boar (Sus scrofa)

“…One might be tempted to think that in wild boars NST, in the absence of UCP1, plays no role. However, another type of NST, driven by the SERCA pump in muscles, enables juvenile wild boars to generate heat, while shivering is diminishing (Nowack et al 2019 ). This type of NST is also present in pigs, the domestic form of wild boar, and seems to be widespread even within adult mammals (Berthon et al 1994 ; Nowack et al 2017 ).…”

Whole‐body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians

“…However, most of what is accepted about NST has been framed around studies on eutherian mammals with BAT. Little is known so far about the operational aspects of muscle NST, although it does seem to have a similar function in newborn wild boar piglets, which lack BAT (Nowack et al ., 2019). Whether SERCA‐based heat production was a more direct contributor to endothermy in its earliest phase is unexplored so far but given its multiple occurrences in fishes (see Section III), as it may be in the deep muscle tissue of the regionally endothermic opah (Franck et al ., 2019), that is possible.…”

“…However, studies from several different groups have provided evidence for a role of SLN in thermogenesis and muscle metabolism (Maurya et al ., 2018; Rotter et al ., 2018; Kaspari et al ., 2020; Nicolaisen et al ., 2020; Wang et al ., 2020). Also, the case for the muscle NST hypothesis has been strengthened considerably by recent experimental work on wild boar piglets ( Sus scrofa ), eutherian mammals that lack BAT (Nowack et al ., 2019). These authors monitored an age‐related replacement of ST by NST in wild piglets, which lack BAT, and found the transition to be accompanied by an increase in T b and coincident increase in SERCA activity and the expression of both SERCA and SLN.…”

How climate change and wildlife management affect population structure in wild boars

“…www.nature.com/scientificreports www.nature.com/scientificreports/ shown for new-born wild boars 24 . Nevertheless, the proportions of light juveniles and LAJ females generally increased under favourable conditions.…”

“…Consequently, a high summer survival of 95% was assumed for yearlings and adults. Further, smaller individuals are more susceptible to cold temperatures because of a lower body surface to volume ratio and the resulting higher energy demands for thermoregulation 23,24 . It therefore seems plausible that LJ have lower survival rates than HJ.…”

Thermoregulation in the wild boar (Sus scrofa)

“…One might be tempted to think that in wild boars NST, in the absence of UCP1, plays no role. However, another type of NST, driven by the SERCA pump in muscles, enables juvenile wild boars to generate heat, while shivering is diminishing (Nowack et al 2019 ). This type of NST is also present in pigs, the domestic form of wild boar, and seems to be widespread even within adult mammals (Berthon et al 1994 ; Nowack et al 2017 ).…”

Whole‐body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians

“…However, most of what is accepted about NST has been framed around studies on eutherian mammals with BAT. Little is known so far about the operational aspects of muscle NST, although it does seem to have a similar function in newborn wild boar piglets, which lack BAT (Nowack et al ., 2019). Whether SERCA‐based heat production was a more direct contributor to endothermy in its earliest phase is unexplored so far but given its multiple occurrences in fishes (see Section III), as it may be in the deep muscle tissue of the regionally endothermic opah (Franck et al ., 2019), that is possible.…”

“…However, studies from several different groups have provided evidence for a role of SLN in thermogenesis and muscle metabolism (Maurya et al ., 2018; Rotter et al ., 2018; Kaspari et al ., 2020; Nicolaisen et al ., 2020; Wang et al ., 2020). Also, the case for the muscle NST hypothesis has been strengthened considerably by recent experimental work on wild boar piglets ( Sus scrofa ), eutherian mammals that lack BAT (Nowack et al ., 2019). These authors monitored an age‐related replacement of ST by NST in wild piglets, which lack BAT, and found the transition to be accompanied by an increase in T b and coincident increase in SERCA activity and the expression of both SERCA and SLN.…”

How climate change and wildlife management affect population structure in wild boars

“…www.nature.com/scientificreports www.nature.com/scientificreports/ shown for new-born wild boars 24 . Nevertheless, the proportions of light juveniles and LAJ females generally increased under favourable conditions.…”

“…Consequently, a high summer survival of 95% was assumed for yearlings and adults. Further, smaller individuals are more susceptible to cold temperatures because of a lower body surface to volume ratio and the resulting higher energy demands for thermoregulation 23,24 . It therefore seems plausible that LJ have lower survival rates than HJ.…”

Thermoregulation in the wild boar (Sus scrofa)

“…One might be tempted to think that in wild boars NST, in the absence of UCP1, plays no role. However, another type of NST, driven by the SERCA pump in muscles, enables juvenile wild boars to generate heat, while shivering is diminishing (Nowack et al 2019 ). This type of NST is also present in pigs, the domestic form of wild boar, and seems to be widespread even within adult mammals (Berthon et al 1994 ; Nowack et al 2017 ).…”

Whole‐body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians

“…However, most of what is accepted about NST has been framed around studies on eutherian mammals with BAT. Little is known so far about the operational aspects of muscle NST, although it does seem to have a similar function in newborn wild boar piglets, which lack BAT (Nowack et al ., 2019). Whether SERCA‐based heat production was a more direct contributor to endothermy in its earliest phase is unexplored so far but given its multiple occurrences in fishes (see Section III), as it may be in the deep muscle tissue of the regionally endothermic opah (Franck et al ., 2019), that is possible.…”

“…However, studies from several different groups have provided evidence for a role of SLN in thermogenesis and muscle metabolism (Maurya et al ., 2018; Rotter et al ., 2018; Kaspari et al ., 2020; Nicolaisen et al ., 2020; Wang et al ., 2020). Also, the case for the muscle NST hypothesis has been strengthened considerably by recent experimental work on wild boar piglets ( Sus scrofa ), eutherian mammals that lack BAT (Nowack et al ., 2019). These authors monitored an age‐related replacement of ST by NST in wild piglets, which lack BAT, and found the transition to be accompanied by an increase in T b and coincident increase in SERCA activity and the expression of both SERCA and SLN.…”

How climate change and wildlife management affect population structure in wild boars

“…www.nature.com/scientificreports www.nature.com/scientificreports/ shown for new-born wild boars 24 . Nevertheless, the proportions of light juveniles and LAJ females generally increased under favourable conditions.…”

“…Consequently, a high summer survival of 95% was assumed for yearlings and adults. Further, smaller individuals are more susceptible to cold temperatures because of a lower body surface to volume ratio and the resulting higher energy demands for thermoregulation 23,24 . It therefore seems plausible that LJ have lower survival rates than HJ.…”