A Functional Nexus between Photoperiod Acclimation, Torpor Expression and Somatic Fatty Acid Composition in a Heterothermic Mammal

Fritz Geiser,Martin Klingenspor,Bronwyn M Mcallan,R Mark Brigham

doi:10.1371/journal.pone.0063803

Abstract

The seasonal changes in thermal physiology and torpor expression of many heterothermic mammals are controlled by photoperiod. As function at low body temperatures during torpor requires changes of tissue lipid composition, we tested for the first time whether and how fatty acids are affected by photoperiod acclimation in hamsters, Phodopus sungorus, a strongly photoperiodic species. We also examined changes in fatty acid composition in relation to those in morphology and thermal biology. Hamsters in short photoperiod had smaller reproductive organs and most had a reduced body mass in comparison to those in long photoperiod. Pelage colour of hamsters under short photoperiod was almost white while that of long photoperiod hamsters was grey-brown and black. Short photoperiod acclimation resulted in regular (28% of days) torpor use, whereas all hamsters in long photoperiod remained normothermic. The composition of total fatty acids differed between acclimation groups for brown adipose tissue (5 of 8 fatty acids), heart muscle (4 of 7 fatty acids) and leg muscle (3 of 11 fatty acids). Importantly, 54% of all fatty acids detected were correlated (r2 = 0.60 to 0.87) with the minimum surface temperature of individuals, but the responses of tissues differed. While some of the compositional changes of fatty acids were consistent with a ‘homeoviscous’ response, this was not the case for all, including the sums of saturated and unsaturated fatty acids, which did not differ between acclimation groups. Our data identify a possible nexus between photoperiod acclimation, morphology, reproductive biology, thermal biology and fatty acid composition. They suggest that some of the changes in thermal physiology are linked to the composition of tissue and organ fatty acids.

Highlights

Some textbooks still describe mammals as generically ‘homeothermic’ endotherms, e.g. [1], many species belonging to more than half of mammalian orders are, ‘heterothermic’ endotherms and use torpor for energy conservation [2,3,4,5]
Morphology and Torpor Use Body mass changed with season and photoperiod acclimation
Body mass change was significantly different between sexes, with males generally heavier than females at the end of the experiments, body masses did not differ at the beginning of the experiments (Sex, p = 0.02; Sex 6 Initial vs Final p,0.05; Table 1)

Summary

Introduction

Some textbooks still describe mammals as generically ‘homeothermic’ endotherms, e.g. [1], many species belonging to more than half of mammalian orders are, ‘heterothermic’ endotherms and use torpor for energy conservation [2,3,4,5]. Seasonal expression of torpor is affected by essential polyunsaturated dietary fatty acids, which have been shown to enhance the occurrence, duration and depth of torpor [8,9,10,11,12,13,14,15]. Data from these studies suggest that the observed diet-induced changes in the composition of tissue and cellular membrane fatty acids, which either occurred alongside, or caused the changes in thermal physiology, were to a large extent due to dietary uptake. The available evidence on compositional changes of tissue fatty acids induced by photoperiod acclimation is essentially restricted to leg muscle of deer mice (Peromyscus maniculatus), which, like other members of the genus, are not strongly seasonal in their use of torpor [18,19,20]

Methods

Results

Conclusion