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The evolution of innate immune genes : Purifying and balancing selection on β-Defensins in waterfowl

Chapman, Joanne R. LU ; Hellgren, Olof LU ; Helin, Anu S.; Kraus, Robert H S; Cromie, Ruth L. and Waldenström, Jonas LU (2016) In Molecular Biology and Evolution 33(12). p.3075-3087
Abstract

In disease dynamics, high immune gene diversity can confer a selective advantage to hosts in the face of a rapidly evolving and diverse pathogen fauna. This is supported empirically for genes involved in pathogen recognition and signalling. In contrast, effector genes involved in pathogen clearance may be more constrained. b-Defensins are innate immune effector genes; their main mode of action is via disruption of microbial membranes. Here, five b-defensin genes were characterized in mallards (Anas platyrhynchos) and other waterfowl; key reservoir species for many zoonotic diseases.All five genes showed remarkably low diversity at the individual-, population-, and species-level. Furthermore, there was widespread sharing of identical... (More)

In disease dynamics, high immune gene diversity can confer a selective advantage to hosts in the face of a rapidly evolving and diverse pathogen fauna. This is supported empirically for genes involved in pathogen recognition and signalling. In contrast, effector genes involved in pathogen clearance may be more constrained. b-Defensins are innate immune effector genes; their main mode of action is via disruption of microbial membranes. Here, five b-defensin genes were characterized in mallards (Anas platyrhynchos) and other waterfowl; key reservoir species for many zoonotic diseases.All five genes showed remarkably low diversity at the individual-, population-, and species-level. Furthermore, there was widespread sharing of identical alleles across species divides. Thus, specific b-defensin alleles were maintained not only spatially but also over long temporal scales, with many amino acid residues being fixed across all species investigated. Purifying selection to maintain individual, highly efficacious alleles was the primary evolutionary driver of these genes in waterfowl. However, we also found evidence for balancing selection acting on the most recently duplicated b-defensin gene (AvBD3b). For this gene, we found that amino acid replacements were more likely to be radical changes, suggesting that duplication of b-defensin genes allows exploration of wider functional space. Structural conservation to maintain function appears to be crucial for avian b-defensin effector molecules, resulting in low tolerance for new allelic variants. This contrasts with other types of innate immune genes, such as receptor and signalling molecules, where balancing selection to maintain allelic diversity has been shown to be a strong evolutionary force.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Antimicrobial peptides, Avian immune system, Ecoimmunology, Host defense peptides, Host-pathogen dynamics
in
Molecular Biology and Evolution
volume
33
issue
12
pages
13 pages
publisher
Oxford University Press
external identifiers
  • scopus:85016214902
  • wos:000387925300005
ISSN
0737-4038
DOI
10.1093/molbev/msw167
language
English
LU publication?
yes
id
00a85e49-d42d-438e-b643-d23ae5e43873
date added to LUP
2017-04-24 13:30:00
date last changed
2017-10-01 05:33:34
@article{00a85e49-d42d-438e-b643-d23ae5e43873,
  abstract     = {<p>In disease dynamics, high immune gene diversity can confer a selective advantage to hosts in the face of a rapidly evolving and diverse pathogen fauna. This is supported empirically for genes involved in pathogen recognition and signalling. In contrast, effector genes involved in pathogen clearance may be more constrained. b-Defensins are innate immune effector genes; their main mode of action is via disruption of microbial membranes. Here, five b-defensin genes were characterized in mallards (Anas platyrhynchos) and other waterfowl; key reservoir species for many zoonotic diseases.All five genes showed remarkably low diversity at the individual-, population-, and species-level. Furthermore, there was widespread sharing of identical alleles across species divides. Thus, specific b-defensin alleles were maintained not only spatially but also over long temporal scales, with many amino acid residues being fixed across all species investigated. Purifying selection to maintain individual, highly efficacious alleles was the primary evolutionary driver of these genes in waterfowl. However, we also found evidence for balancing selection acting on the most recently duplicated b-defensin gene (AvBD3b). For this gene, we found that amino acid replacements were more likely to be radical changes, suggesting that duplication of b-defensin genes allows exploration of wider functional space. Structural conservation to maintain function appears to be crucial for avian b-defensin effector molecules, resulting in low tolerance for new allelic variants. This contrasts with other types of innate immune genes, such as receptor and signalling molecules, where balancing selection to maintain allelic diversity has been shown to be a strong evolutionary force.</p>},
  author       = {Chapman, Joanne R. and Hellgren, Olof and Helin, Anu S. and Kraus, Robert H S and Cromie, Ruth L. and Waldenström, Jonas},
  issn         = {0737-4038},
  keyword      = {Antimicrobial peptides,Avian immune system,Ecoimmunology,Host defense peptides,Host-pathogen dynamics},
  language     = {eng},
  month        = {12},
  number       = {12},
  pages        = {3075--3087},
  publisher    = {Oxford University Press},
  series       = {Molecular Biology and Evolution},
  title        = {The evolution of innate immune genes : Purifying and balancing selection on β-Defensins in waterfowl},
  url          = {http://dx.doi.org/10.1093/molbev/msw167},
  volume       = {33},
  year         = {2016},
}