Divergent Selection of Pattern Recognition Receptors in Mammals with Different Ecological Characteristics
Pattern recognition receptors (PRRs) are specialized receptors that represent a key component of the host innate immune system. Whether molecular evolutionary history of different PRR classes have involved different genetic mechanisms underlying diverse pathogen environment in mammals, and whether distinct ecology of mammals may have imposed divergent selective pressures on the evolution of the PRRs, remained unknown. To test these hypotheses, we investigated the characterization of 20 genes belonging to four PRR classes in mammals. Evidence of positive selection was found in most (17 of 20) PRR genes examined, and most positively selected sites (84%) undergoing radical changes were found to fall in important functional regions, consistent with the co-evolutionary dynamics between the hosts and their microbial counterparts. We found different evolutionary patterns in different PRR classes, with the highest level of positive selection in C-type lectin receptor (CLR) family, suggesting that the capability of CLRs in response to a wide variety of ligands might explain their malleability to selection pressures. Tests using branch models that partitioned the data along habitat and social behavior found significant evidence of divergent selective pressures of PRRs among mammalian groups. Interestingly, species-specific evolution was detected on RIG-I-like helicase genes (RLRs) in cetaceans, suggesting that RLRs might play a critical role in the defense against widespread marine RNA viruses during their divergence and radiation into marine habitats. This study provides a comprehensive look at the evolutionary patterns and implications of mammalian PRRs, and highlights the importance of ecological influences in molecular adaptation.
KeywordsInnate immunity Pattern recognition receptors (PPRs) Host–pathogen interaction Adaptive evolution Positive selection
We thank Mr. Xinrong Xu for help with collecting samples for many years. We also thank members of the Jiangsu Key Laboratory for Biodiversity and Biotechnology, Nanjing Normal University, for their contributions to this paper.
This work was funded by the Key Project of the National Natural Science Foundation of China (NSFC) (Grant No. 31630071 to G.Y. and Grant No. 31570379; 31772448 to S.X.), the National Science Fund for Distinguished Young Scholars (Grant No. 31325025 to G.Y.), the National Key Program of Research and Development, Ministry of Science and Technology (Grant No. 2016YFC0503200 to G.Y. and S.X.), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) to G.Y. and S.X., and the Natural Science Foundation of Jiangsu Province of China (Grant No. BK20141449) to S.X., and the Cultivation Plan for Excellent Doctorial Dissertations of Nanjing Normal University (NNU) to R.T.
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Conflict of interest
The authors declare that they have no conflict interests.
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