Episodic positive diversifying selection on key immune system genes in major avian lineages
- 78 Downloads
The major histocompatibility complex (MHC) of the adaptive immune system and the toll-like receptor (TLR) family of the innate immune system are involved in the detection of foreign invaders, and thus are subject to parasite-driven molecular evolution. Herein, we tested for macroevolutionary signatures of selection in these gene families within and among all three major clades of birds (Paleognathae, Galloanserae, and Neoaves). We characterized evolutionary relationships of representative immune genes (Mhc1 and Tlr2b) and a control gene (ubiquitin, Ubb), using a relatively large and phylogenetically diverse set of species with complete coding sequences (34 orthologous loci for Mhc1, 29 for Tlr2b, and 37 for Ubb). Episodic positive diversifying selection was found in the gene-wide phylogenies of the two immune genes, as well as at specific sites within each gene (8.5% of codon sites in Mhc1 and 2.7% in Tlr2b), but not in the control gene (Ubb). We found 20% of lineages under episodic diversifying selection in Mhc1 versus 9.1% in Tlr2b. For Mhc1, selection was relaxed in the Galloanserae and intensified in the Neoaves relative to the other clades, but no differences were detected among clades in the Tlr2b gene. In summary, we provide evidence of episodic positive diversifying selection in key immune genes and demonstrate differential strengths of selection within Class Aves, with the adaptive gene showing an increased divergence and evolutionary rate over the innate gene, contributing to the growing understanding of vertebrate immune gene evolution.
KeywordsMajor histocompatibility complex Toll-like receptor Paleognathae Galloanserae Neoaves
We thank M. Christie, J. Dunning, R. Ricklefs, C. Searle and members of the DeWoody Lab for critical review of a previous version of this manuscript.
This work was funded by the U.S. National Institute of Food and Agriculture, Purdue’s Department of Forestry & Natural Resources, and the University Faculty Scholar program.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334 CrossRefPubMedGoogle Scholar
- Gill FB (2007) Ornithology. Macmillan, New YorkGoogle Scholar
- Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
- Huang YH, Temperley ND, Ren LM, Smith J, Li N, Burt DW (2011) Molecular evolution of the vertebrate TLR1 gene family—a complex history of gene duplication, gene conversion, positive selection and co-evolution. BMC Evol Biol. https://doi.org/10.1186/1471-2148-11-149 CrossRefPubMedPubMedCentralGoogle Scholar
- Janeway C (2005) Immunobiology: the immune system in health and disease, 6th edn. Garland Science, New YorkGoogle Scholar
- Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New YorkGoogle Scholar
- Krishnegowda G et al (2005) Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum—cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 280:8606–8616. https://doi.org/10.1074/jbc.m413541200 CrossRefPubMedGoogle Scholar
- Mukherjee S, Sarkar-Roy N, Wagener DK, Majumder PP (2009) Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. Proc Natl Acad Sci USA 106:7073–7078. https://doi.org/10.1073/pnas.0811357106 CrossRefPubMedGoogle Scholar
- Piontkivska H, Rooney AP, Nei M (2002) Purifying selection and birth-and-death evolution in the histone H4 gene family. Mol Biol Evol 19:689–697. https://doi.org/10.1093/oxfordjournals.molbev.a004127 CrossRefPubMedGoogle Scholar
- Sibley CG, Monroe BL (1990) Distribution and taxonomy of birds of the world. Yale University Press, New HavenGoogle Scholar
- Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL (2015) Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol 32:1342–1353. https://doi.org/10.1093/molbev/msv022 CrossRefPubMedPubMedCentralGoogle Scholar
- Vinkler M, Albrecht T (2009) The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zool 58:15–28Google Scholar