Modeling heterothermic fitness landscapes in a marsupial hibernator using changes in body composition

Abstract

Hibernation is an adaptive strategy that allows animals to enter a hypometabolic state, conserving energy and enhancing their fitness by surviving harsh environmental conditions. However, addressing the adaptive value of hibernation, at the individual level and in natural populations, has been challenging. Here, we applied a non-invasive technique, body composition analysis by quantitative magnetic resonance (qMR), to calculate energy savings by hibernation in a population of hibernating marsupials (Dromiciops gliroides). Using outdoor enclosures installed in a temperate rainforest, and measuring qMR periodically, we determined the amount of fat and lean mass consumed during a whole hibernation cycle. With this information, we estimated the daily energy expenditure of hibernation (DEEH) at the individual level and related to previous fat accumulation. Using model selection approaches and phenotypic selection analysis, we calculated linear (directional, β), quadratic (stabilizing or disruptive, γ) and correlational (ρ) coefficients for DEEH and fat accumulation. We found significant, negative directional selection for DEEH (βDEEH = − 0.58 ± 0.09), a positive value for fat accumulation (βFAT = 0.34 ± 0.07), and positive correlational selection between both traits (ρDEEH × FAT = 0.24 ± 0.07). Then, individuals maximizing previous fat accumulation and minimizing DEEH were promoted by selection, which is visualized by a bi-variate selection surface estimated by generalized additive models. At the comparative level, results fall within the isometric allometry known for hibernation metabolic rate in mammals. Thus, by a combination of a non-invasive technique for body composition analysis and semi-natural enclosures, we were characterized the heterothermic fitness landscape in a semi-natural population of hibernators.

Climate change and population persistence in a hibernating marsupial

“…During hibernation, animals reduce their metabolic rate by up to 95% and do not ingest food, thus relying completely on accumulated fat [45,46]. Indeed, a hibernating Dromiciops consumes about 0.09 g of fat per day [29]. Thus, it would need to accumulate about 13.5 g of fat to survive 150 days of hibernation.…”

“…These projections have a resolution of 500 m and every 1000 m of elevation bands, which we downloaded as raster layers and used with a resolution of 2.5 min (about 5 km per side). Given that projections for mean temperatures for different climate change scenarios are tabulated monthly, we assumed that during the 4-month period where Dromiciops is known to be at deep-torpor, from May to August [29,44], animals rely 100% on their fat stores. Thus, we also assumed that animals will survive the winter if the fat content is enough for these 120 days (using the energy consumption provided by equations (2.7) and (2.8)) or will die if fat is not enough.…”

“…Thus, we also assumed that animals will survive the winter if the fat content is enough for these 120 days (using the energy consumption provided by equations (2.7) and (2.8)) or will die if fat is not enough. In other words, there is a time period of 120 days during which animals do not ingest any food and should fully rely on their fat stores to cover their energy needs [29,34,53]. Then, we assumed that whenever this 120-day threshold is surpassed, the population will persist and on the contrary, if the threshold is not reached, the population will decline.…”

“…A unique ecosystem in southern South America is the temperate rainforest, a phylogenetically conserved biome of Gondwanan origin [27,28] and the home to the microbiotheriid marsupial 'monito del monte' (body mass range: 25-35 g), which comprises two species: Dromiciops bozinovici at the northern part (distributional range: 35-39° S) and D. gliroides at the southern part of its distribution (range: 39-43° S) [29][30][31]. The monito del monte is recognized as one of the two South American true hibernators (see [32,33]).…”

“…The monito del monte is recognized as one of the two South American true hibernators (see [32,33]). It experiences multi-day torpor events of up to 12 days, a whole hibernation cycle of about 150 days and a metabolic reduction during torpor of over 95% compared to normothermia [29,34,35]. Also, these arboreal marsupials play important ecological roles in the temperate rainforest as unique seed dispersers of over 80% of plant species of this biome [36].…”