Tenrecs: freaks we can all learn from

Abstract

Tenrecs, hedgehog-like mammals more closely related to elephants than hedgehogs, are freaks of nature when it comes to body temperature regulation. Most mammals that vary their body temperature (heterotherms) are not active at low body temperatures and instead become torpid – a state where their metabolic rate is reduced and they either become immobile, as in an extreme form of sleep, or very lethargic. Tenrecs, on the other hand, can remain active with body temperatures as low as ∼14°C and they can become torpid at relatively warm ambient and body temperatures of 28°C. A group of researchers, led by Frank van Breukelen at the University of Nevada, USA, and Jane Khudyakov at the University of the Pacific, USA, sought to further understand the underlying physiology behind the common tenrec's (Tenrec ecaudatus) extraordinary abilities by looking at the proteins expressed in the animal's liver.van Breukelen and his colleagues kept the tenrecs either at a cool (12°C) or warm (28°C) temperature in their captive colony at the University of Nevada Las Vegas, USA. Then, the researchers collected liver samples from three tenrecs that remained active in the warm conditions with a body temperature of 33.5°C and three that had slipped into torpor with body temperatures ∼27.7°C. Of the tenrecs housed at the cool temperature, the researchers took samples from three tenrecs that had become torpid with body temperatures of 12.8°C, three active tenrecs with cool body temperatures (14.5°C) and three active tenrecs with warm 30.2°C body temperatures. In this way, the researchers were able to not only compare active and torpid animals, but also body temperature with activity state. This experimental design is almost impossible to do with most other hibernators, as most mammals are not able to be active at such low body temperatures or become torpid at such high body temperatures.Of the 768 liver proteins that the team could identify, 51% were different between the torpid and active animals, which is almost unheard of; hibernating ground squirrels change the expression of only 15.5% of their proteins when they switch off for their long winter slumber. These differences in protein abundance were mostly connected to protein turnover, coordinating the processes that build proteins (anabolism) and those that break them down (catabolism). Additionally, they found nine proteins that were present more in the chillier temperatures, which may identify part of the liver's response to cold. 72.2% of the proteins that were upregulated in the cold tenrecs that remained active, compared with the warm active animals, were also upregulated in the tenrecs that had slipped into torpor at 28°C. This suggests that being at a cooler environmental temperature and being active at a low body temperature may hinder the animals’ ability to maintain a stable set of proteins. Overall, many of the 768 proteins identified overlapped with proteins found in other hibernating species, suggesting that even across distantly related species, the core metabolic pathways dealing with torpor are conserved.By researching the common tenrec – one of the most heterothermic mammal species, which retains many of the same physical characteristics as the first mammal – we can get a better understanding of how the ability to maintain a stable body temperature, homeothermy, may have evolved from heterothermy. van Breukelen and his colleagues predict that the evolution of homeothermy likely came about from the better coordination of protein destruction and production, resulting in a more balanced set of proteins matched to the thermal sensitivities of metabolic pathways.