Increased homeothermy during reproduction in a basal placental mammal

Abstract

Homeothermic endothermy, the maintenance of a high and stable body temperature (T b ) 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 T b to fluctuate with large variations between active and rest-phase T b . 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 T b 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 T b below the thermoneutral zone, accompanied by a decrease in T b 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.

A phenology of the evolution of endothermy in birds and mammals

“…Reversal into hibernation and daily torpor would have been highly adaptive when animals were not breeding, especially in predator-rich environments (Bieber et al, 2012;Lovegrove et al, 2014b). Some marsupials (Geiser, McAllan & Brigham, 2005), tenrecs (Stephenson & Racey, 1993a,b) and bats (Willis, Brigham & Geiser, 2006) become torpid during pregnancy, but the vast majority of mammals maximize endogenous heat production during pregnancy and lactation emphasizing the prevailing importance of parental care in the evolution of endothermy (Farmer, 2000;Levesque & Lovegrove, 2014).…”

Modelling mammalian energetics: the heterothermy problem

“…Conversely, in colder climates where most small-bodied species rest in thermally insulated burrows, diurnal activity can reduce overall energy expenditure by lowering the need for thermogenesis during the active period [13,62]. The relative energetic costs and benefits of a nocturnal or diurnal activity pattern have so far mostly been discussed in single species studies, or in hypotheses about the evolution of endothermy [40,61,[63][64][65]. Unfortunately, nocturnal and diurnal species, as well as those that do not fit clearly in either category, are usually lumped together in meta-analyses despite facing vastly different environmental conditions.…”

“…An extreme example can be found in basoendotherms. In these species, the thermoneutral zone (TNZ) can be difficult to distinguish as T b often closely tracks T a , which also blurs the lines between normothermy and torpor [63,[83][84][85]. What these basoendotherms demonstrate, is that by allowing T b to decrease along with T a they reduce the T b -T a gradient, which allows for lower rates of heat loss as well as a widening of the range of T a over which minimum rates of metabolism are measured.…”

“…But factors other than energy expenditure, such as low water availability (see above) or the reproductive status of an individual can also influence torpor use. While some species abandon torpor use during pregnancy and lactation [63,138,139], others will continue to use torpor to save energy during inclement conditions and even to delay parturition until a more favourable time [107,140,141]. When attempting to model how a species will respond to changes in climate, it is important to have an understanding of how often, and for how long, they will be able to employ torpor.…”

Improved homeothermy and hypothermia in African lions during gestation

“…Support for the PCM has been found in tenrecs, primitive eutherian mammals, which were more homeothermic during pregnancy than at other times [18]. Tighter regulation of T b during near-term gestation has also been demonstrated in echidnas (Tachyglossus aculeatus), bats (Eptesicus fuscus) and dunnarts (Sminthopsis macroura) [19], and more recently support for the PCM has been found in the remarkable discovery of reproductive endothermy in a small (approx.…”