Journal
SCIENCE ADVANCES
Volume 3, Issue 7, Pages -Publisher
AMER ASSOC ADVANCEMENT SCIENCE
DOI: 10.1126/sciadv.1602878
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Funding
- Natural Sciences and Engineering Research Council of Canada (NSERC) [238838, 418503]
- NSERC Discovery Accelerator Supplement [412336]
- Canada Research Chairs program [950-223744]
- German Center for Diabetes Research (DZD)
- NSF [DEB-1457735]
- University of Manitoba Undergraduate Research Award
- University of Manitoba Graduate Fellowship
- Manitoba Graduate Fellowship
- Natural Environment Research Council
- University of York
- NSERC Alexander Graham Bell Canada Graduate Scholarship-Doctoral Program
- Direct For Biological Sciences [1457735] Funding Source: National Science Foundation
- Division Of Environmental Biology [1457735] Funding Source: National Science Foundation
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Mitochondrial uncoupling protein 1 (UCP1) is essential for nonshivering thermogenesis in brown adipose tissue and is widely accepted to have played a key thermoregulatory role in small-bodied and neonatal placental mammals that enabled the exploitation of cold environments. We map ucp1 sequences from 133 mammals onto a species tree constructed from a similar to 51-kb sequence alignment and show that inactivating mutations have occurred in at least 8 of the 18 traditional placental orders, thereby challenging the physiological importance of UCP1 across Placentalia. Selection and timetree analyses further reveal that ucp1 inactivations temporally correspond with strong secondary reductions in metabolic intensity in xenarthrans and pangolins, or in six other lineages coincided with a similar to 30 million-year episode of global cooling in the Paleogene that promoted sharp increases in body mass and cladogenesis evident in the fossil record. Our findings also demonstrate that members of various lineages (for example, cetaceans, horses, woolly mammoths, Steller's sea cows) evolved extreme cold hardiness in the absence of UCP1-mediated thermogenesis. Finally, we identify ucp1 inactivation as a historical contingency that is linked to the current low species diversity of clades lacking functional UCP1, thus providing the first evidence for species selection related to the presence or absence of a single gene product.
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