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Title: Evolutionary responses of innate Immunity to adaptive immunity

Author
item WARD, A - University Of Maryland
item Rosenthal, Benjamin

Submitted to: Infection, Genetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2013
Publication Date: 1/8/2014
Citation: Ward, A.E., Rosenthal, B.M. 2014. Evolutionary responses of innate Immunity to adaptive immunity. Infection, Genetics and Evolution. 21:492-496.

Interpretive Summary: This manuscript considers how pathogen recognition systems have evolved in two kinds of animals: those (such as ourselves) that elaborate diverse repertoires of T cells in response to changing infectious stimuli, and those (such as marine invertebrates) that rely on pathogen recognition molecules inherited at birth. It further considers how the adaptive immunity in vertebrates (including humans and our livestock) relaxed or amplified the functional importance and molecular diversity of innate immune molecules of our own, and of those animals that rely entirely on such systems. Two evolutionary scenarios are considered, one involving the loss of diversity in our own systems governing innate pathogen recognition, and the other involving the gain of such diversity in those animals that lack our type of adaptive immunity. We suggest that those receptors may have lost the freedom to diversify when they became embedded in complex signaling pathways in vertebrates, but that diversity continues to confer an advantage for organisms lacking the means to generate non-self recognition receptors via somatic mutation. Thus, the development of adaptive immunity changed the role of PRRs in immunity as well as the selective forces on host receptors, deuterostomes, and pathogens. This information will be of interest to immunologists, microbiologists, and evolutionary biologists.

Technical Abstract: Innate immunity is present in all metazoans, whereas the evolutionarily more novel adaptive immunity is limited to jawed fishes and their descendants (gnathostomes). We observe that the organisms that possess adaptive immunity lack diversity in their innate pattern recognition receptors (PRRs), raising the question: did gnathostomes lose the diversity of their ancestors? Or might innate receptors have diversified in the lineage lacking adaptive immunity? We address this question by contextualizing PRRs in their distinct functional roles in organisms possessing or lacking adaptive immunity. In particular, limited PRR diversity in gnathostomes is accompanied by an expansion of the Jak/Stat signaling pathway, which would suggest that the development of adaptive immunity shifted the role of PRRs from the entirety of pathogen recognition to regulators of subsequent immune responses. As PRRs became essential upstream components of the increasingly complex Jak/Stat signaling cascade in organisms possessing adaptive immunity, it may have limited their freedom to diversify. By contrast, PRR diversity continues to confer an advantage for organisms lacking the means to generate non-self recognition receptors via somatic mutation. Extensive deuterostome PRR diversity may have been driven by gnathostome adaptive immunity inducing diversification of shared pathogens, which exerted strong diversifying selection on deuterostome PRRs. Thus, the development of adaptive immunity changed the role of PRRs in immunity as well as the selective forces on host receptors, deuterostomes, and pathogens.