Energy Homeostasis in Monotremes

Abstract

In 1803, the French anatomist Étienne Geoffroy Saint-Hilaire decided that the newly described echidna and platypus should be placed in a separate order, the monotremes, intermediate between reptiles and mammals. The first physiological observations showed monotremes had low body temperatures and metabolic rates, and the consensus was that they were at a stage of physiological development intermediate between “higher mammals” and “lower vertebrates.” Subsequent studies demonstrated that platypuses and echidnas are capable of close thermoregulation in the cold although less so under hot conditions. Because the short-beaked echidna Tachyglossus aculeatus, may show very large daily variations in body temperature, as well as seasonal hibernation, it has been suggested that it may provide a useful model of protoendotherm physiology. Such analysis is complicated by the very significant differences in thermal relations between echidnas from different climates. In all areas female echidnas regulate Tb within 1°C during egg incubation. The lactation period is considered to be the most energetically expensive time for most female mammals but lactating echidnas showed no measurable difference in field metabolic rate from non-lactating females, while the lactation period is more than 200 days for Kangaroo Island echidnas but only 150 days in Tasmania. In areas with mild winters echidnas show reduced activity and shallow torpor in autumn and early winter, but in areas with cold winters echidnas enter true hibernation with Tb falling as low as 4.5°C. Monotremes do not possess brown adipose tissue and maximum rates of rewarming from hibernation in echidnas were only half those of marmots of the same mass. Although echidnas show very large seasonal variations in fat stores associated with hibernation there is no relationship between plasma leptin and adiposity. Leptin levels are lowest during post-reproductive fattening, supporting suggestions that in evolutionary terms the anorectic effects of leptin preceded the adiposity signal. BMR of platypuses is twice that of echidnas although maximum metabolism is similar. High levels of thyroid hormones in platypuses may be driving metabolism limited by low body temperature. Monotremes show a mosaic of plesiomorphic and derived features but can still inform our understanding of the evolution of endothermy.

Development and evolution of the metazoan heart

“…Not all mammals are considered endotherms. Echidna (monotremes) must probably be considered mesotherm with an elevated body temperature only during egg incubation …”

“…As endothermy evolved several times wide apart in paleontological history, this presents multiple entrees for research. Mammalian history is particularly interesting, as development of embryos relying on a placenta probably originated after the onset of endothermy. It is intriguing to note that the mesotherm egg‐laying Echidna maintains a constant body temperature during egg incubation, which is favorable for development of the embryo in the pouch. Investigations on the evolution of monotremes related to cardiac development could provide more insight in the origin of endothermy in mammals.…”

“…Echidna (monotremes) must probably be considered mesotherm with an elevated body temperature only during egg incubation. 202 In endotherm amniotes (mammals and birds), there is a connection between cardiac output, separation of low pulmonary and high systemic pressure by complete cardiac septation, and high rates of metabolism, which are often 5 to 10 times as high as in reptiles of the same size. Ectotherms usually exhibit a low metabolism combined with a cardiovascular system that lacks complete separation of systemic and pulmonary circulations.…”

Energetics meets sexual conflict: The phenology of hibernation in Tasmanian echidnas

“…Percentage of adult echidnas of each sex hibernating over the period 1997 and 2013 plotted against date (a) and (b) minimum and maximum soil temperatures at 20 cm recorded over the same period at a Bureau of Meteorology station approximately 4 km from the centre of the field site. Dashed line shows a temperature of 17°C, above which hibernation cannot be maintained (Nicol, ; Nicol & Andersen, ). Date from 14 males (24 immergence and 27 emergence dates) and 24 females (55 immergence and 49 emergence dates)…”

“…The short‐beaked echidna ( Tachyglossus aculeatus ) is the most widely distributed of the monotremes and occurs from the tropics of New Guinea to the cool temperate island of Tasmania (40.6–43.6°S). Echidnas eat ants, termites and other soil invertebrates (Griffiths, ; Sprent & Nicol, ) and have the lowest basal and maximal metabolic rates of all the mammals (Lovegrove, ; Nicol, ). Like other mammals with similar diets, they have a roaming male mating system (Clutton‐Brock, ; Nicol, Vanpé, Sprent, Morrow, & Andersen, ), and throughout Australia, mating occurs between June and October, with mating in Tasmania, if anything, being slightly earlier than in warmer regions (Morrow, Andersen, & Nicol, ).…”