Skip to main content
SpringerLink
Log in

Lineage-Specific Duplications of Muroidea Faim and Spag6 Genes and Atypical Accelerated Evolution of the Parental Spag6 Gene

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Gene duplications restricted to single lineage combined with an asymmetric evolution of the resulting genes may play particularly important roles in this lineage’s biology. We searched and identified asymmetrical evolution in nine gene families that duplicated exclusively in rodents and are present as single-copies in human, dog, cow, elephant, opossum, chicken, lizard, and Western clawed frog. Among those nine gene families are Fas apoptosis inhibitory molecule (Faim), implicated in apoptosis, and Sperm antigen 6 (Spag6), implicated in sperm mobility. Both genes were duplicated in or before the Muroidea ancestor. Due to the highly asymmetric evolution of the resulting paralogs, the existence of these duplications had been previously overlooked. Interestingly, Spag6, previously regarded and characterized as a single-copy ortholog of human Spag6, turns out to be a Muroidea-specific paralog. Conversely, the newly identified, highly divergent Spag6-BC061194 is in fact the parental gene. In consequence, this gene represents a rare exception from the general rule of rapid evolution of derived rather than parental genes following gene duplication. Unusual genes such as murine Spag6 may help to understand which mechanisms are responsible for this rule.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40:D48–D53

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blanco-Rodriguez J (1998) A matter of death and life: the significance of germ cell death during spermatogenesis. Int J Androl 21:236–248

    Article  CAS  PubMed  Google Scholar 

  • Boguski MS, Lowe TM, Tolstoshev CM (1993) dbEST—database for “expressed sequence tags”. Nat Genet 4:332–333

    Article  CAS  PubMed  Google Scholar 

  • Castillo-Davis CI, Kondrashov FA, Hartl DL, Kulathinal RJ (2004) The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res 14:802–811

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, Bult CJ, Agarwala R, Cherry JL, DiCuccio M, Hlavina W, Kapustin Y, Meric P, Maglott D, Birtle Z et al (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7:e1000112

    Article  PubMed Central  PubMed  Google Scholar 

  • Ciccarelli FD, von Mering C, Suyama M, Harrington ED, Izaurralde E, Bork P (2005) Complex genomic rearrangements lead to novel primate gene function. Genome Res 15:343–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22

    Article  CAS  PubMed  Google Scholar 

  • Conant GC, Wagner A (2003) Asymmetric sequence divergence of duplicate genes. Genome Res 13:2052–2058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conrad B, Antonarakis SE (2007) Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu Rev Genomics Hum Genet 8:17–35

    Article  CAS  PubMed  Google Scholar 

  • Cusack BP, Wolfe KH (2007) Not born equal: increased rate asymmetry in relocated and retrotransposed rodent gene duplicates. Mol Biol Evol 24:679–686

    Article  CAS  PubMed  Google Scholar 

  • Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigo R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW et al (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–528

    Article  PubMed Central  PubMed  Google Scholar 

  • Fletcher W, Yang Z (2010) The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection. Mol Biol Evol 27:2257–2267

    Article  CAS  PubMed  Google Scholar 

  • Friedman R, Hughes AL (2007) Likelihood-ratio tests for positive selection of human and mouse duplicate genes reveal nonconservative and anomalous properties of widely used methods. Mol Phylogenet Evol 42:388–393

    Article  CAS  PubMed  Google Scholar 

  • Goodstadt L, Ponting CP (2006) Phylogenetic reconstruction of orthology, paralogy, and conserved synteny for dog and human. PLoS Comput Biol 2:e133

    Article  PubMed Central  PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Haider S, Ballester B, Smedley D, Zhang J, Rice P, Kasprzyk A (2009) BioMart central portal—unified access to biological data. Nucleic Acids Res 37:W23–W27

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han MV, Demuth JP, McGrath CL, Casola C, Hahn MW (2009) Adaptive evolution of young gene duplicates in mammals. Genome Res 19:859–867

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164

    Article  PubMed Central  PubMed  Google Scholar 

  • Hemond M, Rothstein TL, Wagner G (2009) Fas apoptosis inhibitory molecule contains a novel beta-sandwich in contact with a partially ordered domain. J Mol Biol 386:1024–1037

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huo J, Xu S, Guo K, Zeng Q, Lam KP (2009) Genetic deletion of Faim reveals its role in modulating c-FLIP expression during CD95-mediated apoptosis of lymphocytes and hepatocytes. Cell Death Differ 16:1062–1070

    Article  CAS  PubMed  Google Scholar 

  • Jun J, Ryvkin P, Hemphill E, Nelson C (2009) Duplication mechanism and disruptions in flanking regions determine the fate of Mammalian gene duplicates. J Comput Biol 16:1253–1266

    Article  CAS  PubMed  Google Scholar 

  • Kaessmann H, Vinckenbosch N, Long M (2009) RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 10:19–31

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krasnov AN, Kurshakova MM, Ramensky VE, Mardanov PV, Nabirochkina EN, Georgieva SG (2005) A retrocopy of a gene can functionally displace the source gene in evolution. Nucleic Acids Res 33:6654–6661

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  CAS  PubMed  Google Scholar 

  • Liao BY, Scott NM, Zhang J (2006) Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 23:2072–2080

    Article  CAS  PubMed  Google Scholar 

  • Lynch M (2002) Genomics. Gene duplication and evolution. Science 297:945–947

    Article  CAS  PubMed  Google Scholar 

  • Nozawa M, Suzuki Y, Nei M (2009) Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci USA 106:6700–6705

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Panhuis TM, Clark NL, Swanson WJ (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond B Biol Sci 361:261–268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pegueroles C, Laurie S, Alba MM (2013) Accelerated evolution after gene duplication: a time-dependent process affecting just one copy. Mol Biol Evol 30:1830–1842

    Article  CAS  PubMed  Google Scholar 

  • Pohl AA, Sugnet CW, Clark TA, Smith K, Fujita PA, Cline MS (2009) Affy exon tissues: exon levels in normal tissues in human, mouse and rat. Bioinformatics 25:2442–2443

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  PubMed  Google Scholar 

  • Prasad AB, Allard MW, Green ED (2008) Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol Biol Evol 25:1795–1808

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rothstein TL, Zhong X, Schram BR, Negm RS, Donohoe TJ, Cabral DS, Foote LC, Schneider TJ (2000) Receptor-specific regulation of B-cell susceptibility to Fas-mediated apoptosis and a novel Fas apoptosis inhibitory molecule. Immunol Rev 176:116–133

    Article  CAS  PubMed  Google Scholar 

  • Sanborn JZ, Benz SC, Craft B, Szeto C, Kober KM, Meyer L, Vaske CJ, Goldman M, Smith KE, Kuhn RM, Karolchik D, Kent WJ, Stuart JM, Haussler D, Zhu J (2011) The UCSC Cancer Genomics Browser: update 2011. Nucleic Acids Res 39:D951–D959

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sapiro R, Tarantino LM, Velazquez F, Kiriakidou M, Hecht NB, Bucan M, Strauss JF 3rd (2000) Sperm antigen 6 is the murine homologue of the Chlamydomonas reinhardtii central apparatus protein encoded by the PF16 locus. Biol Reprod 62:511–518

    Article  CAS  PubMed  Google Scholar 

  • Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, Strauss IJ (2002) Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 22:6298–6305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    CAS  PubMed  Google Scholar 

  • Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison RC, Haussler D, Miller W (2003) Human-mouse alignments with BLASTZ. Genome Res 13:103–107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Segura MF, Sole C, Pascual M, Moubarak RS, Perez-Garcia MJ, Gozzelino R, Iglesias V, Badiola N, Bayascas JR, Llecha N, Rodriguez-Alvarez J, Soriano E, Yuste VJ, Comella JX (2007) The long form of Fas apoptotic inhibitory molecule is expressed specifically in neurons and protects them against death receptor-triggered apoptosis. J Neurosci 27:11228–11241

    Article  CAS  PubMed  Google Scholar 

  • Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062–6067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor JS, Van de Peer Y, Meyer A (2001) Genome duplication, divergent resolution and speciation. Trends Genet 17:299–301

    Article  CAS  PubMed  Google Scholar 

  • Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E (2009) EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19:327–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW 3rd, Su AI (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:R130

    Article  PubMed Central  PubMed  Google Scholar 

  • Xu X, Nagarajan H, Lewis NE, Pan S, Cai Z, Liu X, Chen W, Xie M, Wang W, Hammond S, Andersen MR, Neff N, Passarelli B, Koh W, Fan HC et al (2011) The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat Biotechnol 29:735–741

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, dos Reis M (2011) Statistical properties of the branch-site test of positive selection. Mol Biol Evol 28:1217–1228

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Z, Wong WS, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  CAS  PubMed  Google Scholar 

  • Zhai W, Nielsen R, Goldman N, Yang Z (2012) Looking for darwin in genomic sequences–validity and success of statistical methods. Mol Biol Evol 29:2889–2893

    Article  CAS  PubMed  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479

    Article  CAS  PubMed  Google Scholar 

  • Zhong X, Schneider TJ, Cabral DS, Donohoe TJ, Rothstein TL (2001) An alternatively spliced long form of Fas apoptosis inhibitory molecule (FAIM) with tissue-specific expression in the brain. Mol Immunol 38:65–72

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly supported by Jagiellonian University, Institute of Zoology Grant (K/ZDS/003254). We acknowledge the release and sharing of whole-genome sequences of guinea pig, squirrel, rabbit and elephant prior to publication by the Broad Institute, Cambridge, MA, USA. We thank the editor and the two anonymous reviewers for constructive suggestions for improving the paper.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Huan Qiu

    Present address: Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ, USA

Authors and Affiliations

  1. Department of Pharmacology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

    Huan Qiu & Leszek Wojnowski

  2. Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, 30-387, Kraków, Poland

    Aniela Gołas & Paweł Grzmil

Authors
  1. Huan Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aniela Gołas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paweł Grzmil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leszek Wojnowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huan Qiu.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1,665 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qiu, H., Gołas, A., Grzmil, P. et al. Lineage-Specific Duplications of Muroidea Faim and Spag6 Genes and Atypical Accelerated Evolution of the Parental Spag6 Gene. J Mol Evol 77, 119–129 (2013). https://doi.org/10.1007/s00239-013-9585-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-013-9585-9

Keywords

Search

Navigation