100 million years of multigene family evolution: origin and evolution of the avian MHC class IIB
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
28610613
PubMed Central
PMC5470263
DOI
10.1186/s12864-017-3839-7
PII: 10.1186/s12864-017-3839-7
Knihovny.cz E-resources
- Keywords
- Birds, Birth-death evolution, Concerted evolution, Gene conversion, Gene duplication, Major histocompatibility complex, Recombination,
- MeSH
- Gene Duplication MeSH
- Genes, MHC Class II genetics MeSH
- Evolution, Molecular * MeSH
- Multigene Family genetics MeSH
- Birds genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Gene duplication has led to a most remarkable adaptation involved in vertebrates' host-pathogen arms-race, the major histocompatibility complex (MHC). However, MHC duplication history is as yet poorly understood in non-mammalian vertebrates, including birds. RESULTS: Here, we provide evidence for the evolution of two ancient avian MHC class IIB (MHCIIB) lineages by a duplication event prior to the radiation of all extant birds >100 million years ago, and document the role of concerted evolution in eroding the footprints of the avian MHCIIB duplication history. CONCLUSIONS: Our results suggest that eroded footprints of gene duplication histories may mimic birth-death evolution and that in the avian MHC the presence of the two lineages may have been masked by elevated rates of concerted evolution in several taxa. Through the presence of a range of intermediate evolutionary stages along the homogenizing process of concerted evolution, the avian MHCIIB provides a remarkable illustration of the erosion of multigene family duplication history.
CNRS UMR 5175 Centre for Functional and Evolutionary Ecology F 34293 Montpellier France
Institute of Vertebrate Biology of the Czech Academy of Sciences Kvetna 8 60365 Brno Czech Republic
MIVEGEC UMR 5290 CNRS IRD University of Montpellier Centre IRD F 34394 Montpellier France
See more in PubMed
Ota T, Nei M. Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol Biol Evol. 1994;11(3):469–482. PubMed
Nei M, Gu X, Sitnikova T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A. 1997;94(15):7799–7806. doi: 10.1073/pnas.94.15.7799. PubMed DOI PMC
Su C, Nei M. Evolutionary dynamics of the T-cell receptor VB gene family as inferred from the human and mouse genomic sequences. Mol Biol Evol. 2001;18(4):503–513. doi: 10.1093/oxfordjournals.molbev.a003829. PubMed DOI
Ohta T. Allelic and nonallelic homology of a supergene family. Proc Natl Acad Sci U S A. 1982;79(10):3251–3254. doi: 10.1073/pnas.79.10.3251. PubMed DOI PMC
Ohta T. On the evolution of multigene families. Theor Popul Biol. 1983;23(2):216–240. doi: 10.1016/0040-5809(83)90015-1. PubMed DOI
Hughes AL, Nei M. Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. Mol Biol Evol. 1990;7(6):491–514. PubMed
Takahashi K, Rooney AP, Nei M. Origins and divergence times of mammalian class II MHC gene clusters. J Hered. 2000;91(3):198–204. doi: 10.1093/jhered/91.3.198. PubMed DOI
Kriener K, CO O’hU, Tichy H, Klein J. Convergent evolution of major histocompatibility complex molecules in humans and new world monkeys. Immunogenetics. 2000;51(3):169–178. doi: 10.1007/s002510050028. PubMed DOI
Burri R, Salamin N, Studer RA, Roulin A, Fumagalli L. Adaptive divergence of ancient gene duplicates in the avian MHC Class II B. Mol Biol Evol. 2010;27(10):2360–2374. doi: 10.1093/molbev/msq120. PubMed DOI
Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet. 2005;39(1):121–152. doi: 10.1146/annurev.genet.39.073003.112240. PubMed DOI PMC
Yuhki N, Beck T, Stephens RM, Nishigaki Y, Newmann K, O'Brien SJ. Comparative genome organization of human, murine, and feline MHC Class II region. Genome Res. 2003;13(6a):1169–1179. doi: 10.1101/gr.976103. PubMed DOI PMC
Andersson L, Rask L. Characterization of the MHC class II region in cattle. The number of DQ genes varies between haplotypes. Immunogenetics. 1988;27(2):110–120. doi: 10.1007/BF00351084. PubMed DOI
Burri R, Niculita-Hirzel H, Salamin N, Roulin A, Fumagalli L. Evolutionary patterns of MHC class II B in owls and their implications for the understanding of avian MHC evolution. Mol Biol Evol. 2008;25(6):1180–1191. doi: 10.1093/molbev/msn065. PubMed DOI
Wittzell H, Bernot A, Auffray C, Zoorob R. Concerted evolution of two Mhc class II B loci in pheasants and domestic chickens. Mol Biol Evol. 1999;16(4):479–490. doi: 10.1093/oxfordjournals.molbev.a026130. PubMed DOI
Hess CM, Gasper J, Hoekstra HE, Hill CE, Edwards SV. MHC class II pseudogene and genomic signature of a 32-kb cosmid in the house finch (Carpodacus mexicanus) Genome Res. 2000;10:613–623. doi: 10.1101/gr.10.5.613. PubMed DOI PMC
Edwards SV, Gasper J, March M. Genomics and polymorphism of Agph-DAB1, an Mhc class II B gene in red-winged blackbirds (Agelaius phoeniceus) Mol Biol Evol. 1998;15:236–250. doi: 10.1093/oxfordjournals.molbev.a025921. PubMed DOI
Edwards SV, Hess CM, Gasper J, Garrigan D. Toward an evolutionary genomics of the avian Mhc. Immunol Rev. 1999;167:119–132. doi: 10.1111/j.1600-065X.1999.tb01386.x. PubMed DOI
Gasper JS, Shiina T, Inoko H, Edwards SV. Songbird genomics: analysis of 45 kb upstream of a polymorphic Mhc class II gene in red-winged blackbirds (Agelaius phoeniceus) Genomics. 2001;75:26–34. doi: 10.1006/geno.2001.6596. PubMed DOI
Eimes JA, Bollmer JL, Whittingham LA, Johnson JA, Van Oosterhout C, Dunn PO. Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J Evol Biol. 2011;24:1847–1856. doi: 10.1111/j.1420-9101.2011.02311.x. PubMed DOI
Bollmer JL, Dunn PO, Whittingham LA, Wimpee C. Extensive MHC Class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas) J Hered. 2010;101(4):448–460. doi: 10.1093/jhered/esq018. PubMed DOI
Alcaide M, Edwards SV, Negro JJ. Characterization, polymorphism, and evolution of MHC class IIB genes in birds of prey. J Mol Evol. 2007;65:541–554. doi: 10.1007/s00239-007-9033-9. PubMed DOI
Klein J. Natural history of the major histocompatibility complex. New York: Wiley; 1986.
Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346(6215):1320–1331. doi: 10.1126/science.1253451. PubMed DOI PMC
Taniguchi Y, Matsumoto K, Matsuda H, Yamada T, Sugiyama T, Homma K, Kaneko Y, Yamagishi S, Iwaisaki H. Structure and polymorphism of the major histocompatibility complex class II region in the Japanese Crested Ibis, Nipponia nippon. PLoS One. 2014;9(9) doi: 10.1371/journal.pone.0108506. PubMed DOI PMC
Chen L-C, Lan H, Sun L, Deng Y-L, Tang K-Y, Wan Q-H. Genomic organization of the crested ibis MHC provides new insight into ancestral avian MHC structure. Sci Rep. 2015;5:7963. doi: 10.1038/srep07963. PubMed DOI PMC
Dearborn DC, Gager AB, Gilmour ME, McArthur AG, Hinerfeld DA, Mauck RA. Non-neutral evolution and reciprocal monophyly of two expressed Mhc class II B genes in Leach’s storm-petrel. Immunogenetics. 2015;67(2):111–123. doi: 10.1007/s00251-014-0813-2. PubMed DOI
Eimes JA, Lee S-i, Townsend AK, Jablonski P, Nishiumi I, Satta Y. Early duplication of a single MHC IIB locus prior to the passerine radiations. PLoS One. 2016;11(9) doi: 10.1371/journal.pone.0163456. PubMed DOI PMC
Burri R, Promerová M, Goebel J, Fumagalli L. PCR-based isolation of multigene families: lessons from the avian MHC class IIB. Mol Ecol Resour. 2014;14(4):778–788. doi: 10.1111/1755-0998.12234. PubMed DOI
Zamani N, Russell P, Lantz H, Hoeppner M, Meadows J, Vijay N, Mauceli E, di Palma F, Lindblad-Toh K, Jern P, et al. Unsupervised genome-wide recognition of local relationship patterns. BMC Genomics. 2013;14(1):347. doi: 10.1186/1471-2164-14-347. PubMed DOI PMC
Ohno S. Evolution by gene duplication. New York: Springer; 1970.
Chen J-M, Cooper DN, Chuzhanova N, Ferec C, Patrinos GP. Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet. 2007;8(10):762–775. doi: 10.1038/nrg2193. PubMed DOI
Kaufman J, Jansen J, Shaw I, Walker B, Milne S, Beck S, Salomonsen J. Gene organisation determines evolution of function in the chicken MHC. Immunol Rev. 1999;167:101–117. doi: 10.1111/j.1600-065X.1999.tb01385.x. PubMed DOI
Balakrishnan C, Ekblom R, Volker M, Westerdahl H, Godinez R, Kotkiewicz H, Burt D, Graves T, Griffin D, Warren W, et al. Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol. 2010;8(1):29. doi: 10.1186/1741-7007-8-29. PubMed DOI PMC
Kelley J, Walter L, Trowsdale J. Comparative genomics of major histocompatibility complexes. Immunogenetics. 2005;56(10):683–695. doi: 10.1007/s00251-004-0717-7. PubMed DOI
Gaigher A, Burri R, Gharib W, Taberlet P, Roulin A, Fumagalli L. Family-assisted inference of the genetic architecture of MHC variation. Mol Ecol Resour. 2016; PubMed
Shiina T, Hosomichi K, Hanzawa K. Comparative genomics of the poultry major histocompatibility complex. Anim Sci J. 2006;77(2):151–162. doi: 10.1111/j.1740-0929.2006.00333.x. DOI
Chaves LD, Krueth SB, Reed KM. Defining the Turkey MHC: sequence and genes of the B locus. J Immunol. 2009;183:6530–6537. doi: 10.4049/jimmunol.0901310. PubMed DOI
Ye Q, He K, Wu S-Y, Wan Q-H. Isolation of a 97-kb minimal essential MHC B locus from a new reverse-4D BAC Library of the Golden Pheasant. PLoS One. 2012;7(3) doi: 10.1371/journal.pone.0032154. PubMed DOI PMC
Salomonsen J, Marston D, Avila D, Bumstead N, Johansson B, Juul-Madsen H, Olesen GD, Riegert P, Skjødt K, Vainio O, et al. The properties of the single chicken MHC classical class II a chain (B-LA) gene indicate an ancient origin for the DR/E-like isotype of class II molecules. Immunogenetics. 2003;55(9):605–614. doi: 10.1007/s00251-003-0620-7. PubMed DOI
Bontrop RE. Comparative genetics of MHC polymorphisms in different primate species: duplications and deletions. Hum Immunol. 2006;67(6):388–397. doi: 10.1016/j.humimm.2006.03.007. PubMed DOI
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Akaike H. A new look at the statistical model identification. IEEE Trans Autom Control. 1974;19(6):716–723. doi: 10.1109/TAC.1974.1100705. DOI
Posada D, Buckley T. Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol. 2004;53(5):793–808. doi: 10.1080/10635150490522304. PubMed DOI
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC
Rambaut A, Drummond AJ. Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer. 2007.
Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23(2):254–267. doi: 10.1093/molbev/msj030. PubMed DOI
Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 2006;7:474. doi: 10.1186/1471-2105-7-474. PubMed DOI PMC
Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI