Increased homeothermy during reproduction in a basal placental mammal

Abstract

Homeothermic endothermy, the maintenance of a high and stable body temperature (Tb) using heat produced by elevated metabolism, is energetically expensive. There is increasing evidence that the earliest endotherms were heterotherms that, rather than maintaining strict homeothermy, allowed Tb to fluctuate with large variations between active and rest-phase Tb. The high level of homeothermy observed in modern mammals is therefore likely to have evolved from an ancestral heterothermic state. One of the hypotheses for the evolution of endothermy is that homeothermy allows for greater energetic output during reproduction (parental care model). We tested this hypothesis by measuring metabolic rates over a range of ambient temperatures in both reproductive and non-reproductive greater hedgehog tenrecs (Setifer setosus), a physiologically primitive mammal from Madagascar. Tenrecs have some of the lowest metabolic rates and highest levels of Tb variability of any mammal and are therefore good models of the ancestral eutherian state. During pregnancy and lactation, there was an increase in metabolism and Tb below the thermoneutral zone, accompanied by a decrease in Tb variability. The lower critical limit of the thermoneutral zone was estimated at ~25°C. However, whereas increases in resting metabolism were substantial below 20°C (up to 150% higher during reproduction), daytime rest-phase ambient temperatures at the study site rarely reached equivalent low levels. Thus, S. setosus provide an example for how relatively low-cost increases in homeothermy could have led to substantial increases in fitness by allowing for the faster production of young. The mechanisms necessary for increases in thermogenesis during reproduction would have further benefited the development of homeothermy in mammals.