Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals

Abstract Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether livi...

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Bibliographic Details
Published in:Molecular biology and evolution 2019-10, Vol.36 (10), p.2171-2183
Main Authors: Jiao, Hengwu, Zhang, Libiao, Xie, Huan-Wang, Simmons, Nancy B, Liu, Hui, Zhao, Huabin
Format: Article
Language:English
Subjects:
Animals
Biological Evolution
Chiroptera - genetics
Chiroptera - metabolism
Diet
Discoveries
Trehalase - genetics
Trehalase - metabolism
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Summary:Abstract Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.
ISSN:0737-4038
1537-1719
DOI:10.1093/molbev/msz127