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Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata)

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Abstract

The presence of nonshivering thermogenesis in marsupials is controversially debated. Survival of small eutherian species in cold environments is crucially dependent on uncoupling protein 1 (UCP1)-mediated, adaptive nonshivering thermogenesis that is executed in brown adipose tissue. In a small dasyurid marsupial species, the fat-tailed dunnart (Sminthopsis crassicaudata), an orthologue of UCP1 has been recently identified which is upregulated during cold exposure resembling adaptive molecular adjustments of eutherian brown adipose tissue. Here, we tested for a thermogenic function of marsupial brown adipose tissue and UCP1 by evaluating the capacity of nonshivering thermogenesis in cold-acclimated dunnarts. In response to an optimal dosage of noradrenaline, cold-acclimated dunnarts (12°C) showed no additional recruitment of noradrenaline-induced maximal thermogenic capacity in comparison to warm-acclimated dunnarts (24°C). While no differences in body temperature were observed between the acclimation groups, basal metabolic rate was significantly elevated after cold acclimation. Therefore, we suggest that adaptive nonshivering thermogenesis does not occur in this marsupial species despite the cold recruitment of oxidative capacity and UCP1 in the interscapular fat deposit. In conclusion, the ancient UCP orthologue in marsupials does not contribute to the classical nonshivering thermogenesis, and may exhibit a different physiological role.

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Abbreviations

BAT:

Brown adipose tissue

BMR:

Basal metabolic rate

CA:

Cold acclimated

FADH:

Flavin adenine dinucleotide

FFA:

Free fatty acid

NA:

Noradrenaline

NADH:

Nicotinamide adenine dinucleotide

NST:

Nonshivering thermogenesis

RMR:

Resting metabolic rate

RQ:

Respiratory quotient

T a :

Ambient temperature

T b :

Body temperature

UCP:

Uncoupling protein

\( \dot{V}{\text{O}}_{ 2} \) :

Rate of oxygen consumption

WA:

Warm acclimated

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Acknowledgments

This research was supported by the German Academic Exchange Service (DAAD). ETP is supported by a scholarship of the Commonwealth Scientific and Industrial Research Organisation (CSIRO), Information and Communication Technologies (ICT Centre); MJ is supported by a German Research Foundation (DFG) fellowship (JA1884/2).

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Authors and Affiliations

  1. School of Zoology, University of Tasmania, Hobart, 7001, Australia

    E. T. Polymeropoulos & P. B. Frappell

  2. Buck Institute for Research on Aging, 8001 Redwood Blvd, Novato, CA, 94945, USA

    M. Jastroch

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  1. E. T. Polymeropoulos
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  2. M. Jastroch
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  3. P. B. Frappell
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Correspondence to E. T. Polymeropoulos.

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Communicated by G. Heldmaier.

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Polymeropoulos, E.T., Jastroch, M. & Frappell, P.B. Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). J Comp Physiol B 182, 393–401 (2012). https://doi.org/10.1007/s00360-011-0623-x

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