Importance of adipocyte browning in the evolution of endothermy

Jastroch, Martin; Seebacher, Frank

doi:10.1098/rstb.2019.0134

Cited by 17 publications

(15 citation statements)

References 96 publications

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“…Water loss, however, could be avoided if T b is regulated slightly above ambient, and the outward flow of heat is varied by insulation, therefore, a switch to a diurnal activity pattern in some species would have necessitated higher T b s (Crompton et al, 1978), which in turn were only made possible with the evolution of the scrotum (Lovegrove, 2019). The evolution of endothermy in mammals is an emergent property of the evolution of various characteristics that aid in either heat production (e.g., thermogenesis, UCP1) and heat dissipation (e.g., insulation, external scrotums) and happened to a different degree across the mammalian lineage (Lovegrove, 2012(Lovegrove, , 2019Seebacher, 2018;Jastroch and Seebacher, 2020). By studying the added level of variability in many thermoregulatory traits, torpor use in particular, observed in species in the tropics and subtropics can help shed further light on how endothermy evolved in mammals.…”

Section: Tropical Origins Of Heterothermy and Endothermy In Mammalsmentioning

confidence: 99%

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

Nowack

Levesque

Reher³

et al. 2020

Front. Ecol. Evol.

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Mammalian heterotherms, species that employ short or long periods of torpor, are found in many different climatic regions. Although the underlying physiological mechanisms of heterothermy in species from lower latitudes (i.e., the tropics and southern hemisphere) appear analogous to those of temperate and arctic heterotherms, the ultimate triggers and resulting patterns of energy expenditure and body temperature are often noticeably different. Phenotypic flexibility in the patterns of thermoregulation in non-Holarctic species can be extensive (depending on body condition, environmental parameters and species competition) and the factors responsible for inducing heterothermy are more variable in non-Holarctic species. As well as being a regular adaptation to seasonality, heterothermy can also be employed as a response to unpredictability in environmental parameters and as a response to emergency situations. Non-Holarctic heterotherms also challenge the notion that regular inter-bout arousals during hibernation are obligatory and suggest all that is necessary to maintain proper functioning during hibernation is an occasional passive return to-or maintenance of-a relatively high body temperature. The study of non-Holarctic heterotherms has led to the conclusion that heterothermy must be defined on the basis of mechanistic, physiological parameters, and not solely by body temperature; yet we are still limited in our abilities to record such mechanistic parameters in the field. It is now believed that homeothermy in mammals evolved in hot climates via an ancestral heterothermic state. Similar to extant warm-climate heterotherms, early mammals could have relied mainly on passive body temperature regulation with a capacity for short-to longer-term up-regulation of metabolism when needed. Hibernation, as seen in temperate and arctic species may then be a derived state of this ancestral heterothermy, and the study of torpor in warm climates can provide potential models for the energetics of early mammals.

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Section: Tropical Origins Of Heterothermy and Endothermy In Mammalsmentioning

confidence: 99%

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

Nowack

Levesque

Reher³

et al. 2020

Front. Ecol. Evol.

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“…It has been shown that various physiological factors, including exercise, diet and the immune system, can cause the browning of white adipose tissue through epigenetic mechanisms [29]. In the first contribution of this section, Jastroch & Seebacher [5] review the molecular mechanisms underlying the browning of white adipocytes, and their potential contribution to endogenous heat production in the evolution of endothermy. Bal & Periasamy [6] review another mechanism of non-shivering thermogenesis: inhibition of Ca 2+ transport, but not ATP hydrolysis, of sarco-endoplasmic reticulum calcium ATPase (SERCA) by sarcolipin, resulting in a futile pump activity that generates heat.…”

Section: Thermometabolismmentioning

confidence: 99%

“…'Vertebrate palaeophysiology' will promote a better understanding of how organism-environment interactions have evolved in terms of energy budgets, predator-prey relationships and sensitivity to environmental change. The research areas covered by this theme issue include: phospho-calcic metabolism [2], acid-base homeostasis [3,4], thermometabolism [4][5][6][7][8][9], respiratory physiology [10], skeletal growth [11], palaeopathophysiology [12,13], genome size and metabolic rate [14], and a concluding historical perspective [15]. Sometimes, the two components ( physiological mechanism and palaeobiological inference) are proposed in separate papers (for instance, three contributions devoted to mechanisms of thermogenesis mechanisms [5][6][7] and three papers dealing with the thermometabolic inferences in extinct taxa [4,8,9]).…”

Section: Introductionmentioning

confidence: 99%

Vertebrate palaeophysiology

Cubo

Huttenlocker

2020

Phil. Trans. R. Soc. B

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Physiology is a functional branch of the biological sciences, searching for general rules by which explanatory hypotheses are tested using experimental procedures, whereas palaeontology is a historical science dealing with the study of unique events where conclusions are drawn from congruence among independent lines of evidence. Vertebrate palaeophysiology bridges these disciplines by using experimental data obtained from extant organisms to infer physiological traits of extinct ones and to reconstruct how they evolved. The goal of this theme issue is to understand functional innovations imprinted on modern vertebrate clades, and how to infer (or ‘retrodict’) physiological capacities in their ancient relatives a posteriori. As such, the present collection of papers deals with different aspects of a rapidly growing field to understand innovations in: phospho-calcic metabolism, acid–base homeostasis, thermometabolism, respiratory physiology, skeletal growth, palaeopathophysiology, genome size and metabolic rate, and it concludes with a historical perspective. Sometimes, the two components (physiological mechanism and palaeobiological inference) are proposed in separate papers. Other times, the two components are integrated in a single paper. In all cases, the approach was comparative, framed in a phylogenetic context, and included rigorous statistical methods that account for evolutionary patterns and processes. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

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“…Endothermy has evolved many times in vertebrates, and proceeds by varied mechanisms ( Jastroch and Seebacher, 2020 ; Legendre and Davesne, 2020 ). Thermogenic adipoctyes, and the presence of brown adipose tissue depots, are unique to placental mammals.…”

Section: Discussionmentioning

confidence: 99%

HOXA5 Participates in Brown Adipose Tissue and Epaxial Skeletal Muscle Patterning and in Brown Adipocyte Differentiation

Holzman

Ryckman

Finkelstein

et al. 2021

Front. Cell Dev. Biol.

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Brown adipose tissue (BAT) plays critical thermogenic, metabolic and endocrine roles in mammals, and aberrant BAT function is associated with metabolic disorders including obesity and diabetes. The major BAT depots are clustered at the neck and forelimb levels, and arise largely within the dermomyotome of somites, from a common progenitor with skeletal muscle. However, many aspects of BAT embryonic development are not well understood. Hoxa5 patterns other tissues at the cervical and brachial levels, including skeletal, neural and respiratory structures. Here, we show that Hoxa5 also positively regulates BAT development, while negatively regulating formation of epaxial skeletal muscle. HOXA5 protein is expressed in embryonic preadipocytes and adipocytes as early as embryonic day 12.5. Hoxa5 null mutant embryos and rare, surviving adults show subtly reduced iBAT and sBAT formation, as well as aberrant marker expression, lower adipocyte density and altered lipid droplet morphology. Conversely, the epaxial muscles that arise from a common dermomyotome progenitor are expanded in Hoxa5 mutants. Conditional deletion of Hoxa5 with Myf5/Cre can reproduce both BAT and epaxial muscle phenotypes, indicating that HOXA5 is necessary within Myf5-positive cells for proper BAT and epaxial muscle development. However, recombinase-based lineage tracing shows that Hoxa5 does not act cell-autonomously to repress skeletal muscle fate. Interestingly, Hoxa5-dependent regulation of adipose-associated transcripts is conserved in lung and diaphragm, suggesting a shared molecular role for Hoxa5 in multiple tissues. Together, these findings establish a role for Hoxa5 in embryonic BAT development.

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Importance of adipocyte browning in the evolution of endothermy

Cited by 17 publications

References 96 publications

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

Vertebrate palaeophysiology

HOXA5 Participates in Brown Adipose Tissue and Epaxial Skeletal Muscle Patterning and in Brown Adipocyte Differentiation

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