Signatures of balancing selection in toll-like receptor (TLRs) genes – novel insights from a free-living rodent

Agnieszka Kloch (Corresponding Author), Marius A. Wenzel, Dominik R. Laetsch, Olek Michalski, Anna Bajer, Jerzy M. Behnke, Renata Welc-Falȩciak, Stuart B. Piertney

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Abstract

Selective pressure from pathogens is considered a key selective force driving the evolution of components of the immune system. Since single components of the immune system may interact with many pathogens, and single pathogens may be recognized by multiple components of the immune system, gaining a better understanding of the mechanisms of parasite-driven selection requires the study of multiple genes and pathogens. Toll-like receptors (TLRs) are a large gene family that code for antigen-presenting components of the innate immune response. In the present paper we characterize polymorphism and signatures of selection in seven TLRs in free-living bank voles Myodes glareolus. We report the first evidence of balancing selection in several TLR genes, supported by positive values of Fu and Li's D∗in TLR2 and TLR5, and positive values of Tajima's D in LRR regions within TLR1 and TLR2. We further found significant associations between amino-acid alleles of TLR1 and TLR5 and susceptibility to infection with the blood pathogen Bartonella. Interestingly, selection patterns in TLRs presenting virus-derived motifs (TLR7 and TLR9) differed considerably from those interacting with bacterial PAMPs. In contrast to the highly variable TLRs presenting bacterial motifs, TLR7 and TLR9 had low polymorphism and displayed signatures of directional selection. These findings suggest different functional responses across the TLR gene family and highlight the complexity of parasite-driven selection.

Original languageEnglish
Article number8361
JournalScientific Reports
Volume8
DOIs
Publication statusPublished - 30 May 2018

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Toll-Like Receptors
Rodentia
Genes
Immune System
Arvicolinae
Parasites
Bartonella
Innate Immunity
Alleles
Viruses
Antigens
Amino Acids
Infection

ASJC Scopus subject areas

  • General

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Signatures of balancing selection in toll-like receptor (TLRs) genes – novel insights from a free-living rodent. / Kloch, Agnieszka (Corresponding Author); Wenzel, Marius A.; Laetsch, Dominik R.; Michalski, Olek; Bajer, Anna ; Behnke, Jerzy M.; Welc-Falȩciak, Renata; Piertney, Stuart B.

In: Scientific Reports, Vol. 8, 8361, 30.05.2018.

Research output: Contribution to journalArticle

Kloch, Agnieszka ; Wenzel, Marius A. ; Laetsch, Dominik R. ; Michalski, Olek ; Bajer, Anna ; Behnke, Jerzy M. ; Welc-Falȩciak, Renata ; Piertney, Stuart B. / Signatures of balancing selection in toll-like receptor (TLRs) genes – novel insights from a free-living rodent. In: Scientific Reports. 2018 ; Vol. 8.
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abstract = "Selective pressure from pathogens is considered a key selective force driving the evolution of components of the immune system. Since single components of the immune system may interact with many pathogens, and single pathogens may be recognized by multiple components of the immune system, gaining a better understanding of the mechanisms of parasite-driven selection requires the study of multiple genes and pathogens. Toll-like receptors (TLRs) are a large gene family that code for antigen-presenting components of the innate immune response. In the present paper we characterize polymorphism and signatures of selection in seven TLRs in free-living bank voles Myodes glareolus. We report the first evidence of balancing selection in several TLR genes, supported by positive values of Fu and Li's D∗in TLR2 and TLR5, and positive values of Tajima's D in LRR regions within TLR1 and TLR2. We further found significant associations between amino-acid alleles of TLR1 and TLR5 and susceptibility to infection with the blood pathogen Bartonella. Interestingly, selection patterns in TLRs presenting virus-derived motifs (TLR7 and TLR9) differed considerably from those interacting with bacterial PAMPs. In contrast to the highly variable TLRs presenting bacterial motifs, TLR7 and TLR9 had low polymorphism and displayed signatures of directional selection. These findings suggest different functional responses across the TLR gene family and highlight the complexity of parasite-driven selection.",
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N2 - Selective pressure from pathogens is considered a key selective force driving the evolution of components of the immune system. Since single components of the immune system may interact with many pathogens, and single pathogens may be recognized by multiple components of the immune system, gaining a better understanding of the mechanisms of parasite-driven selection requires the study of multiple genes and pathogens. Toll-like receptors (TLRs) are a large gene family that code for antigen-presenting components of the innate immune response. In the present paper we characterize polymorphism and signatures of selection in seven TLRs in free-living bank voles Myodes glareolus. We report the first evidence of balancing selection in several TLR genes, supported by positive values of Fu and Li's D∗in TLR2 and TLR5, and positive values of Tajima's D in LRR regions within TLR1 and TLR2. We further found significant associations between amino-acid alleles of TLR1 and TLR5 and susceptibility to infection with the blood pathogen Bartonella. Interestingly, selection patterns in TLRs presenting virus-derived motifs (TLR7 and TLR9) differed considerably from those interacting with bacterial PAMPs. In contrast to the highly variable TLRs presenting bacterial motifs, TLR7 and TLR9 had low polymorphism and displayed signatures of directional selection. These findings suggest different functional responses across the TLR gene family and highlight the complexity of parasite-driven selection.

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