Insights into Dietary Switch in Cetaceans: Evidence from Molecular Evolution of Proteinases and Lipases

Abstract

Fossil evidence suggests that cetaceans evolved from artiodactylans. Thus, there was a major dietary change from herbivorous to carnivorous during their transition from a terrestrial to an aquatic environment. However, the molecular evolutionary mechanisms underlying this dietary switch have not been well investigated. Evidence of positive selection of digestive proteinases and lipases of cetaceans was detected: (1) For the four pancreatic proteinase families (carboxypeptidase, trypsin, chymotrypsin, and elastase) examined in this study, each family included only a single intact gene (e.g., CPA1, PRSS1, CTRC, and CELA3B) that had no ORF-disrupted or premature stop codons, whereas other members of each family had become pseudogenized. Further selective pressure analysis showed that three genes (PRSS1, CTRC, and CELA3B) were subjected to significant positive selection in cetaceans. (2) For digestive proteinases from the stomach, PGA was identified to be under positive selection. (3) Intense positive selection was also detected for the lipase gene PLRP2 in cetaceans. In addition, parallel /convergent amino acid substitutions between cetaceans and carnivores, two groups of mammals that have evolved similar feeding habits, were identified in 10 of the 12 functional genes. Although pseudogenization resulted in each family of pancreatic proteinases only retaining one intact gene copy in cetacean genomes, positive selection might have driven pancreatic proteinases, stomach proteinases, and lipases to adaptively evolve a stronger ability to digest a relatively higher proportion of proteins and lipids from animal foods. This study can provide some novel insights into the molecular mechanism of cetacean dietary changes during their transition from land to sea.

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Acknowledgements

This research was financially supported by the National Natural Science Foundation of China (NSFC) Grant No. 31872219 and 31370401, and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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WR, GY, SX, GL and LL contributed to the study conception and design. Material preparation, data collection, analysis and experiment were performed by GL, HW, JB and XD. The first draft of the manuscript was written by GL. GY and WR revised previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Wenhua Ren.

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Handling editor: Peter Chi.

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Li, G., Wei, H., Bi, J. et al. Insights into Dietary Switch in Cetaceans: Evidence from Molecular Evolution of Proteinases and Lipases. J Mol Evol 88, 521–535 (2020). https://doi.org/10.1007/s00239-020-09952-2

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Keywords

  • Cetaceans
  • Proteinase
  • Lipase
  • Positive selection
  • Dietary switch