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

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.

Brown adipose tissue: physiological function and evolutionary significance

“…The NST-capacity values were determined as the difference between the maximum VO 2 after noradrenaline injection and the basal metabolic rate (BMR) (the resting metabolic rate (RMR) in some cases) further claimed the absence of BAT in 37 other marsupial and one monotreme (prototherian) species. In addition to these morphological findings, in vivo studies found equivocal responses of typical noradrenaline-stimulated metabolic rate (Nicol 1978;Smith and Dawson 1984;Loudon et al 1985;Dawson and Olson 1988;Ye et al 1996;Nicol et al 1997;Clements et al 1998;Rose et al 1998Rose et al , 1999Opazo et al 1999;Polymeropoulos et al 2012). At this historical stage, only one study has reported on molecular hints for BAT in marsupials by immunological detection of UCP1 using heterologous eutherian antibodies (Hope et al 1997).…”

“…The South American marsupial Monodelphis domestica expresses UCP1 mRNA at the juvenile stage (G), whereas adult Australian fat-tailed dunnarts possesses "brownish" adipose tissue (H, Jastroch et al 2008). However, noradrenalineinduced thermogenesis appears to be non-adaptive (Polymeropoulos et al 2012) and thermogenic functionality of marsupial UCP1 has not been demonstrated so far. In Afrotheria, BAT is thermogenically active and adaptive to ambient temperatures in elephant shrews (D, Oelkrug et al 2012) and lesser hedgehog tenrecs (F, Oelkrug et al 2013).…”

“…Martin Jastroch). Furthermore, the classical adaptive increase of noradrenaline-stimulated thermogenesis in response to cold acclimatization is missing (Polymeropoulos et al 2012). So far, there is no report on UCP1 expression of monotremes (prototherian) species although UCP1 gene traces can be found in the platypus genome (pers.…”

Skeletal muscle mass and composition during mammalian hibernation

“…This process occurs through both non-shivering and shivering thermogenesis (Choi et al, 2001;Lee et al, 2010), and is characterized by high energy expenditure that approaches the upper limits for sustained aerobic metabolism (Geiser, 2004;Heldmaier et al, 2004;Peterson et al, 1990). Marsupial hibernators are unique in the sense that many species do not exhibit a robust non-shivering thermogenic response (Cortes et al, 2014;Opazo et al, 1999;Polymeropoulos et al, 2012), and as such they may be more reliant on shivering thermogenesis during arousal. Because of their much larger body mass and thermal inertia, bears display several differences in hibernation characteristics from those of small mammal hibernators.…”

Uncoupling protein 1 controls reactive oxygen species in brown adipose tissue

“…Even in marsupials, members of endothermic mammals that split about 130-150 million years ago from eutherians, the role of UCP1 in adipose tissue is unclear. The molecular phylogeny groups marsupial UCP1 close to ectothermic UCP1 orthologs (29), and classical adaptive thermogenic responses are missing in marsupials despite cold induction of UCP1 (30). From the perspective of UCP1's evolutionary history starting in ectotherms, there should be more than thermogenesis, particularly in archetypal UCP1, and there is accumulating evidence that the UCP1-dependent effects on ROS regulation may have contributed to shape the integration of UCP1 into the high thermogenic capacity of eutherian BAT.…”