Eutherian mammals exhibit a greater capacity for cold acclimation than marsupials and birds: a comparative analysis

The ability to enhance heat production in response to prolonged cold exposure (cold acclimation capacity) is a key physiological adaptation in some endotherms, such as eutherian mammals, owing to a specialized mechanism of adaptive non-shivering thermogenesis in brown adipose tissue, mediated by uncoupling protein 1, which seems to be absent in marsupials and birds. Phenotypically, it is unclear whether these endotherms lack cold acclimation capacity or whether they have other facultative heat production mechanisms. To test for differences in thermal acclimation capacity, we analyzed published studies measuring maximum metabolic rates following cold acclimation. Using generalized linear models, phylogenetic generalized least squares and meta-analyses, we compared placentals, marsupials and birds. The results consistently indicated that placental mammals exhibit significantly greater cold acclimation capacity than marsupials and birds. Meta-analysis revealed maximum rate of oxygen consumption responses as being 101.8% higher in placentals than those in birds and 301.2% higher than those in marsupials. Our findings suggesting superior thermogenic plasticity in placental mammals reflect unique evolutionary adaptations, permitting these animals to thrive in seasonally cold environments, which is especially important when migration capacity is limited. Birds, however, with lesser migratory restrictions, would have prioritized the insulating capacity of feathers as an evolutionary solution to the cold. Marsupials, without the innovation of adaptive thermogenesis, would have a geographical distribution restricted to non-extreme areas.