article-7 - LETTERS 2006 Nature Publishing Group

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Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys Jianzhi Zhang 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 debated 1–3 . 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 efFciencies 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. I propose that four requirements should be fulFlled to demonstrate adaptive parallel evolution at the protein sequence level. ±irst, similar changes in protein function occur in independent evolutionary lineages. Second, parallel amino acid substitutions are observed in these proteins. Third, the parallel substitutions are not attributable to chance alone and therefore must have been driven by a common selective pressure. ±ourth, the parallel substitutions are responsible for the parallel functional changes. Although more than a dozen cases of molecular parallel evolution have been reported 1,4–7 , almost all of them satisfy only the Frst and/or second requirements. Below I describe the parallel evolution of colobine pancreatic ribonucleases (RNases), which satisFes all four criteria. Colobines are a subfamily of Old World monkeys and are separated into Asian and African clades, which diverged from each other B 13 million years (Myr) ago 8 . Colobines are different from most other primates in that their primary diet consists of leaves rather than insects or fruits 9 . Because mammals do not possess enzymes to degrade cellulose, a main component of leaves, colobines adopt a ruminant- like alimentary system 9 . That is, they use symbiotic bacteria in their foregut to ferment leaves and then recover nutrients by digesting the bacteria 9 . Because rapidly growing bacteria have the highest ratio of RNA nitrogen to total nitrogen of all cells, a higher-than-usual amount of RNase is required in foregut-fermenters to quickly degrade RNA so that the nitrogen can be recycled efFciently 10 .I n d e e d , ruminants and colobines have considerably higher concentrations of pancreatic RNase than other mammals do 10,11 . In addition, it is
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This note was uploaded on 04/22/2009 for the course EEB 318 taught by Professor Cutter during the Spring '09 term at University of Toronto- Toronto.

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article-7 - LETTERS 2006 Nature Publishing Group

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