Extreme physiological plasticity in a hibernating basoendothermic mammal, Tenrec ecaudatus

Abstract

Physiological plasticity allows organisms to respond to diverse conditions. However, can being too plastic actually be detrimental? Malagasy common tenrecs, , have many plesiomorphic traits and may represent a basal placental mammal. We established a laboratory population of and found extreme plasticity in thermoregulation and metabolism, a novel hibernation form, variable annual timing, and remarkable growth and reproductive biology. For instance, tenrec body temperature ( ) may approximate ambient temperature to as low as 12°C even when tenrecs are fully active. Conversely, tenrecs can hibernate with of 28°C. During the active season, oxygen consumption may vary 25-fold with little or no change in During the austral winter, tenrecs are consistently torpid but the depth of torpor may vary. A righting assay revealed that contributes to but does not dictate activity status. Homeostatic processes are not always linked, e.g. a hibernating tenrec experienced a ∼34% decrease in heart rate while maintaining constant body temperature and oxygen consumption rates. Tenrec growth rates vary but young may grow ∼40-fold in the 5 weeks until weaning and may possess indeterminate growth as adults. Despite all of this profound plasticity, tenrecs are surprisingly intolerant of extremes in ambient temperature (<8 or >34°C). We contend that while plasticity may confer numerous energetic advantages in consistently moderate environments, environmental extremes may have limited the success and distribution of plastic basal mammals.

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

“…In contrast to those tenrec species highlighted above that use some form of heterothermic response during most of the year, other species, such as the tailless tenrec, Tenrec ecaudatus, are generally believed to only hibernate seasonally (Nicoll, 1986). Although based on more recent studies, it is highly likely that they can also use short bouts of torpor outside of the regular hibernation period (Lovegrove et al, 2014b;Treat et al, 2018).…”

Waking the sleeping dragon: gene expression profiling reveals adaptive strategies of the hibernating reptile Pogona vitticeps

“…'brumation' [10]. However, there is large variation in physiology even between hibernating mammals, notably in tenrec [11], implying that hibernation is not one specific physiological state. As such, herein 'hibernation' will be used to describe the state of reptilian winter dormancy.…”

Hans Bluntschli in Berne: Researching reproduction in hedgehog tenrecs (Afrosoricida, Tenrecidae)

“…Starting with Hubrecht, embryologists focused on insectivores because they were perceived to be primitive and could cast light on the basic mammalian condition (Hubrecht, ). Tenrecs continue to be viewed in this light (Treat et al, ). They have a low encephalisation index (Mack et al, ; Stankowich & Stensrud, ), a cloaca (Riedelsheimer, Unterburger, Kuenzle, & Welsch, ) and highly variable body temperature (Treat et al, ).…”

“…Bluntschli is often cited (e.g., Treat et al, ) for his observation that Tenrec can have a litter of up to 32 young and he mentions finding as many as 40 blastocysts in the uterus (Bluntschli, ). This is the upper end of the range as a later study found a mean of 9.7 implantations (Nicoll & Racey, ).…”