Divergent cis-regulatory haplotypes at Tlr2 are associated with immune responsiveness
(2026) In Molecular biology and evolution 43(5).- Abstract
Positive and balancing selection on pattern recognition receptors (PRRs) is widely thought to target ligand-binding domains and affect the specificity of recognition of different pathogens. Alternatively, positive/balancing selection on PRRs could affect general responsiveness by targeting for example signaling domains or cis-regulatory variation. Studies of a wild rodent (the bank vole, Clethrionomys glareolus) have shown that Tlr2—a lipoprotein-binding PRR—is highly polymorphic with divergent haplotypes and signatures of balancing selection and that Tlr2 genotype is associated with susceptibility to Borrelia afzelii infection in the wild. To investigate what aspect of TLR2 function has been under selection, we here perform integrated... (More)
Positive and balancing selection on pattern recognition receptors (PRRs) is widely thought to target ligand-binding domains and affect the specificity of recognition of different pathogens. Alternatively, positive/balancing selection on PRRs could affect general responsiveness by targeting for example signaling domains or cis-regulatory variation. Studies of a wild rodent (the bank vole, Clethrionomys glareolus) have shown that Tlr2—a lipoprotein-binding PRR—is highly polymorphic with divergent haplotypes and signatures of balancing selection and that Tlr2 genotype is associated with susceptibility to Borrelia afzelii infection in the wild. To investigate what aspect of TLR2 function has been under selection, we here perform integrated population genetic and functional analyses. Ex vivo infection experiments show that the protective Tlr2 haplotype produces a stronger proinflammatory response to B. afzelii compared to the haplotype associated with susceptibility. Tlr2 genotype has a similar, albeit not statistically significant, effect on responsiveness to the phylogenetically distant pathogen Streptococcus pyogenes. We find that the strongest signature of balancing selection is 4.6 kb upstream of the Tlr2 CDS, near a putative enhancer, and that Tlr2 exhibits allele-specific expression such that the protective haplotype is more expressed. Collectively, these results indicate that balancing selection has primarily acted on cis-regulatory variation affecting the general responsiveness via TLR2 signaling rather than on polymorphisms affecting TLR2 ligand-binding specificity.
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- author
- Nandakumar, Mridula
LU
; Lundberg, Max
LU
; Nouri, Mehrnaz
LU
; Valfridsson, Christine
LU
; Carlsson, Fredric
LU
and Råberg, Lars
LU
- organization
- publishing date
- 2026-05
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- allelic imbalance, evolutionary immunology, Myodes glareolus, pathogen-mediated selection, Toll-like receptor
- in
- Molecular biology and evolution
- volume
- 43
- issue
- 5
- article number
- msag113
- publisher
- Oxford University Press
- external identifiers
-
- scopus:105040360618
- pmid:42052896
- ISSN
- 0737-4038
- DOI
- 10.1093/molbev/msag113
- language
- English
- LU publication?
- yes
- id
- b891f19f-bc3a-46a0-b003-0c908749f727
- date added to LUP
- 2026-09-04 14:57:30
- date last changed
- 2026-09-18 15:43:07
@article{b891f19f-bc3a-46a0-b003-0c908749f727,
abstract = {{<p>Positive and balancing selection on pattern recognition receptors (PRRs) is widely thought to target ligand-binding domains and affect the specificity of recognition of different pathogens. Alternatively, positive/balancing selection on PRRs could affect general responsiveness by targeting for example signaling domains or cis-regulatory variation. Studies of a wild rodent (the bank vole, Clethrionomys glareolus) have shown that Tlr2—a lipoprotein-binding PRR—is highly polymorphic with divergent haplotypes and signatures of balancing selection and that Tlr2 genotype is associated with susceptibility to Borrelia afzelii infection in the wild. To investigate what aspect of TLR2 function has been under selection, we here perform integrated population genetic and functional analyses. Ex vivo infection experiments show that the protective Tlr2 haplotype produces a stronger proinflammatory response to B. afzelii compared to the haplotype associated with susceptibility. Tlr2 genotype has a similar, albeit not statistically significant, effect on responsiveness to the phylogenetically distant pathogen Streptococcus pyogenes. We find that the strongest signature of balancing selection is 4.6 kb upstream of the Tlr2 CDS, near a putative enhancer, and that Tlr2 exhibits allele-specific expression such that the protective haplotype is more expressed. Collectively, these results indicate that balancing selection has primarily acted on cis-regulatory variation affecting the general responsiveness via TLR2 signaling rather than on polymorphisms affecting TLR2 ligand-binding specificity.</p>}},
author = {{Nandakumar, Mridula and Lundberg, Max and Nouri, Mehrnaz and Valfridsson, Christine and Carlsson, Fredric and Råberg, Lars}},
issn = {{0737-4038}},
keywords = {{allelic imbalance; evolutionary immunology; Myodes glareolus; pathogen-mediated selection; Toll-like receptor}},
language = {{eng}},
number = {{5}},
publisher = {{Oxford University Press}},
series = {{Molecular biology and evolution}},
title = {{Divergent cis-regulatory haplotypes at Tlr2 are associated with immune responsiveness}},
url = {{http://dx.doi.org/10.1093/molbev/msag113}},
doi = {{10.1093/molbev/msag113}},
volume = {{43}},
year = {{2026}},
}