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Infection risk and extensive parental care govern the molecular evolution of Toll-like receptors in birds.

By Zhechun Zhang, Dan Liang, Guoling Chen, Fasheng Zou, Fumin Lei, Lu Dong, Michael Griesser, Yang Liu

Posted 02 Dec 2019
bioRxiv DOI: 10.1101/860114

The arms race between pathogens and the immune system of their hosts is a critical evolutionary force that affects the ecology and life history of organisms. An increased infection risk selects for adaptations in immune genes that encode receptors involved in pathogen recognition and the initiation of innate immune responses, including Toll-like receptor (TLR) genes. Although recent studies assessed the evolution of major histocompatibility complex (MHC) genes, the ecological and evolutionary processes that drive the evolution of immune genes across major phylogenetic lineages remain unstudied. Moreover, trade-offs between immune responses and other energy-demanding vital functions may limit the resource allocation into costly immune functions, and therefore affect the evolution of immune genes. Here we assess the evolutionary patterns of six TLR genes across 121 bird species, covering 95% of extant orders that represent diverse ecologies and life histories. Selection analyses revealed that all six TLR genes show strong signs of purifying selection, while few sites underwent episodic positive selection. Comparative phylogenetic analyses showed that the intensity of positive selection of TLR genes is associated with long-distance migration, extensive parental care (i.e., altricality and prolonged parent-offspring association), and a large body size (a proxy of increased longevity). Together, these results suggest that the evolution of immune genes is characterized by episodic positive selection, and is shaped by an increased inflection risk and extensive parental care that buffers the costs of immune functions.

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