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The Glycogen Synthase 2 Gene (Gys2) Displays Parallel Evolution Between Old World and New World Fruit Bats

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Abstract

Frugivorous and nectarivorous bats rely largely on hepatic glycogenesis and glycogenolysis for postprandial blood glucose disposal and maintenance of glucose homeostasis during short time starvation, respectively. The glycogen synthase 2 encoded by the Gys2 gene plays a critical role in liver glycogen synthesis. To test whether the Gys2 gene has undergone adaptive evolution in bats with carbohydrate-rich diets in relation to their insect-eating sister taxa, we sequenced the coding region of the Gys2 gene in a number of bat species, including three Old World fruit bats (OWFBs) (Pteropodidae) and two New World fruit bats (NWFBs) (Phyllostomidae). Our results showed that the Gys2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to OWFBs and NWFBs. Our explicit convergence test showed that posterior probabilities of convergence between several branches of OWFBs, and the NWFBs were markedly higher than that of divergence. Three parallel amino acid substitutions (Q72H, K371Q, and E666D) were detected among branches of OWFBs and NWFBs. Tests for parallel evolution showed that two parallel substitutions (Q72H and E666D) were driven by natural selection, while the K371Q was more likely to be fixed randomly. Thus, our results suggested that the Gys2 gene has undergone parallel evolution on amino acid level between OWFBs and NWFBs in relation to their carbohydrate metabolism.

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Acknowledgments

The authors thank Yi-Hsuan Pan for technical advice on protein analyses and Ming Lei for help in convergent evolution analyses. This study was supported by the Foundation for Science and Technology Innovation of University Students from East China Normal University to YQ, the Chinese National Science Foundation (Grant No. 31172077) to SZ, and the Academic Scholarship for Ph.D. Candidate Granted by Ministry of Education of the P.R.China (MXRZZ2012008) to BS.

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  1. School of Life Science, East China Normal University, Shanghai, 200062, China

    Yamin Qian

  2. Institute of Molecular Ecology and Evolution, Institutes for Advanced Interdisciplinary Research, East China Normal University, Shanghai, 200062, China

    Tao Fang, Bin Shen & Shuyi Zhang

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  1. Yamin Qian
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Correspondence to Bin Shen or Shuyi Zhang.

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Fig. S1

Schematic representation of biochemical pathway of glycogen synthesis. Blood glucose is transported into cells via glucose transporter proteins and converted into glucose 6-phosphate by hexokinase 4. Then glucose 6-phosphate is converted into glucose 1-phosphate by phosphoglucomutase. And the glucose 1-phosphate is converted into UDP-glucose by UDP-glucose pyrophosphorylase. Finally, the UDP-glucose is used as glucosyl donor by glycogen synthase to form glycogen via formation of the α-1,4-glycosidic linkages (PDF 289 kb)

Fig. S2

Alignment of the amino acid sequences of the Gys2 gene from 22 mammals (only the variable sites are shown) (PDF 374 kb)

Fig. S3

Nonsynonymous amino acid substitutions mapped onto the species topology of 22 mammals. Branch lengths are not drawn to scale (PDF 365 kb)

Fig. S4

Species topology showing inferred evolutionary change along the Gys2 gene. Values on each branch are rates of non-synonymous substitution (d N) and synonymous substitution (d S) estimated by one-ratio model based on maximum-likelihood method using PAML CODEML package. Branch lengths are based on nucleotide substitutions per codon (PDF 312 kb)

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Qian, Y., Fang, T., Shen, B. et al. The Glycogen Synthase 2 Gene (Gys2) Displays Parallel Evolution Between Old World and New World Fruit Bats. J Mol Evol 78, 66–74 (2014). https://doi.org/10.1007/s00239-013-9600-1

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