Abstract
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.
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Acknowledgements
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.
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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.
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Supplementary material 1 (TXT 36 kb)
Fig. S1. The nucleotide CDS fasta file for the 34 avian species with Mhc1 sequences used in this study. Sequences were required to be complete for the entire alpha chain, including both the variable regions α1 and α2, which forms the peptide-binding groove, and the conserved region α3 which encodes the alpha chain immunoglobulin domain
Supplementary material 2 (TXT 66 kb)
Fig. S2. The nucleotide CDS fasta file for the 29 avian species with Tlr2b sequences used in this study. Sequences were required to be complete with the variable region, the extracellular N-terminal LRR (leucine-rich repeat) region which is involved in pathogen recognition, the conserved TIR (Toll/interleukin-1 receptor) region, and the intracellular domain that initiates a signal cascade for downstream immune response
Supplementary material 3 (TXT 33 kb)
Fig. S3. The nucleotide CDS fasta file for the 37 avian species with Ubb sequences used in this study. Sequences were required to be complete with repeat conserved ubiquitin domains
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Supplementary material 4 (RTF 568 kb)
Fig. S4. Curated peptide MSA alignment of Mhc1 for 34 species produced by T-coffee (Di Tommaso P 2011) and Gblocks (Castresana 2000) in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical amino acids, gray shading designates similar amino acids (>=50%), and white shading indicates no amino acid similarity
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Supplementary material 5 (RTF 646 kb)
Fig. S5. Curated peptide MSA alignment of Tlr2b for 29 species produced by T-coffee (Di Tommaso P 2011) and Gblocks (Castresana 2000) in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical amino acids, gray shading designates similar amino acids (>=50%), and white shading indicates no amino acid similarity
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Supplementary material 6 (RTF 110 kb)
Fig. S6. Curated peptide MSA alignment of Ubb for 37 species produced by T-coffee (Di Tommaso P 2011) and Gblocks (Castresana 2000) in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical amino acids, gray shading designates similar amino acids (>=50%), and white shading indicates no amino acid similarity
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Supplementary material 7 (RTF 1238 kb)
Fig. S7. In-frame codon-based nucleotide MSA alignment of Mhc1 for 34 species produced by back translation of curated peptide MSA alignment in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical nucleotides, gray shading designates similar nucleotides (>=50%), and white shading indicates no nucleotide similarity
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Supplementary material 8 (RTF 1493 kb)
Fig. S8. In-frame codon-based nucleotide MSA alignment of Tlr2b for 29 species produced by back translation of curated peptide MSA alignment in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical nucleotides, gray shading designates similar nucleotides (>=50%), and white shading indicates no nucleotide similarity
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Supplementary material 9 (RTF 613 kb)
Fig. S9. In-frame codon-based nucleotide MSA alignment of Uaa for 37 species produced by back translation of curated peptide MSA alignment in TranslatorX (Abascal et al. 2010), and visualized with the Boxshade server (https://embnet.vital-it.ch/software/BOX_form.html). Black shading represents identical nucleotides, gray shading designates similar nucleotides (>=50%), and white shading indicates no nucleotide similarity
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Supplementary material 10 (JPEG 2097 kb)
Fig. S10. A) The species tree/cladogram from the NCBI taxonomy database (www.ncbi.nlm.nih.gov/taxonomy) for the 34 species used for Mhc1. B) The Mhc1 gene tree topology based on the majority-rule consensus maximum-likelihood tree of 37 species produced by IQ-Tree (Trifinopoulos et al. 2016). The Robinson-Foulds distance is 18 and Euclidean distance is 14.3. Lighter colors indicate less similarity in the topology as indicated by Phylo.io (Robinson et al. 2016). between the Mhc1 gene tree and its species tree were 18 and 14.3, respectively, while for Tlr2b the distances were 15 and 13.5
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Supplementary material 11 (JPEG 1794 kb)
Fig. S11. A) The species tree/cladogram from the NCBI taxonomy database (www.ncbi.nlm.nih.gov/taxonomy) for the 29 species used for Tlr2b. B) The Tlr2b gene tree topology based on the majority-rule consensus maximum-likelihood tree of 37 species produced by IQ-Tree (Trifinopoulos et al. 2016). The Robinson-Foulds distance is 15 and Euclidean distance is 13.5. Lighter colors indicate less similarity in the topology as indicated by Phylo.io (Robinson et al. 2016)
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Supplementary material 12 (JPEG 2358 kb)
Fig. S12. A) The species tree/cladogram from the NCBI taxonomy database (www.ncbi.nlm.nih.gov/taxonomy) for the 37 species used for Uaa. B) The Uaa gene tree topology based on the majority-rule consensus maximum-likelihood tree of 37 species produced by IQ-Tree (Trifinopoulos et al. 2016). The Robinson-Foulds distance is 6 and Euclidean distance is 4.0. Lighter colors indicate less similarity in the topology as indicated by Phylo.io (Robinson et al. 2016)
Supplementary material 13 (XLSX 12 kb)
Table S1. The 34 avian species with Mhc1 sequences used in this study. The CDS was required to be complete for the entire alpha chain, including both the variable regions α1 and α2, which forms the peptide-binding groove, and the conserved region α3 which encodes the alpha chain immunoglobulin domain
Supplementary material 14 (XLSX 12 kb)
Table S2. The 29 avian species with Tlr2b sequences used in this study. The CDS was required to be complete with the variable region, the extracellular N-terminal LRR (leucine-rich repeat) region which is involved in pathogen recognition, the conserved TIR (Toll/interleukin-1 receptor) region, and the intracellular domain that initiates a signal cascade for downstream immune response. Species in which the Tlr locus was not specified as Tlr2a or Tlr2b were not included
Supplementary material 15 (XLSX 13 kb)
Table S3. The 37 avian species with Ubb sequences used in this study. The CDS was required to be complete with repeat conserved ubiquitin domains
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Supplementary material 16 (XLSX 12 kb)
Table S4. Statistical results of model fits for ration or intensification of selection pressure at each clade relative to the rest of the tree for Mhc1 and Tlr2b, as determined by the RELAX algorithm (Wertheim et al. 2015) in the Datamonkey server (Weaver et al. 2018). The best fit model for each of the three clades is bolded
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Antonides, J., Mathur, S. & DeWoody, J.A. Episodic positive diversifying selection on key immune system genes in major avian lineages. Genetica 147, 337–350 (2019). https://doi.org/10.1007/s10709-019-00081-3
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DOI: https://doi.org/10.1007/s10709-019-00081-3