Ancestral and developmental cold alter brown adipose tissue function and adult thermal acclimation in Peromyscus

Abstract

Small, non-hibernating endotherms increase their thermogenic capacity to survive seasonal cold, through adult phenotypic flexibility. In mammals, this response is primarily driven by remodeling of brown adipose tissue (BAT), which matures postnatally in altricial species. In many regions, ambient temperatures can vary dramatically throughout the breeding season. We used second-generation lab-born Peromyscus leucopus, cold exposed during two critical developmental windows, to test the hypothesis that adult phenotypic flexibility to cold is influenced by rearing temperature. We found that cold exposure during the postnatal period (14 °C, birth to 30 days) accelerated BAT maturation and permanently remodeled this tissue. As adults, these mice had increased BAT activity and thermogenic capacity relative to controls. However, they also had a blunted acclimation response when subsequently cold exposed as adults (5 °C for 6 weeks). Mice born to cold-exposed mothers (14 °C, entire pregnancy) also showed limited capacity for flexibility as adults, demonstrating that maternal cold stress programs the offspring thermal acclimation response. In contrast, for P. maniculatus adapted to the cold high alpine, BAT maturation rate was unaffected by rearing temperature. However, both postnatal and prenatal cold exposure limited the thermal acclimation response in these cold specialists. Our results suggest a complex interaction between developmental and adult environment, influenced strongly by ancestry, drives thermogenic capacity in the wild.

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Acknowledgments

CER and GBM designed the study and wrote the manuscript. CER performed research and analyzed data. Funding was provided by a National Science and Engineering Research Council of Canada (NSERC) Discovery grant awarded to G.B.M. and an NSERC Doctoral Canadian graduate scholarship awarded to C.E.R. We wish to thank Rob Rhem for his help with PET/CT imaging.

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Robertson, C., McClelland, G.B. Ancestral and developmental cold alter brown adipose tissue function and adult thermal acclimation in Peromyscus. J Comp Physiol B 191, 589–601 (2021). https://doi.org/10.1007/s00360-021-01355-z

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Keywords

  • Developmental plasticity
  • Thermogenic capacity
  • Non-shivering thermogenesis
  • High altitude
  • Phenotypic flexibility
  • Endothermy