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Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys

Abstract

Similar morphological or physiological changes occurring in multiple evolutionary lineages are not uncommon. Such parallel changes are believed to be adaptive, because a complex character is unlikely to originate more than once by chance. However, the occurrence of adaptive parallel amino acid substitutions is debated1,2,3. Here I propose four requirements for establishing adaptive parallel evolution at the protein sequence level and use these criteria to demonstrate such a case. I report that the gene encoding pancreatic ribonuclease was duplicated independently in Asian and African leaf-eating monkeys. Statistical analyses of DNA sequences, functional assays of reconstructed ancestral proteins and site-directed mutagenesis show that the new genes acquired enhanced digestive efficiencies through parallel amino acid replacements driven by darwinian selection. They also lost a non-digestive function independently, under a relaxed selective constraint. These results demonstrate that despite the overall stochasticity, even molecular evolution has a certain degree of repeatability and predictability under the pressures of natural selection.

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Figure 1: Sequence alignment of pancreatic RNases.
Figure 2: Phylogenetic relationships among colobine pancreatic RNase genes.
Figure 3: RNase activities against yeast tRNA at different pHs.
Figure 4: Parallel amino acid substitutions and parallel functional changes in guereza and douc langur pancreatic RNases.
Figure 5: Loss of the RNase activity against dsRNA in douc langur RNASE1B and guereza RNASE1β and RNASE1γ.

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Acknowledgements

I thank M. Bakewell, S. Cho, W. Grus, A. Rooney and D. Webb for comments. This work was supported by the US National Institutes of Health.

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Correspondence to Jianzhi Zhang.

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Supplementary information

Supplementary Fig. 1

The structures of the human and guereza pancreatic RNase genes. (PDF 17 kb)

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Zhang, J. Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys. Nat Genet 38, 819–823 (2006). https://doi.org/10.1038/ng1812

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