Skip to main content
SpringerLink
Log in

Genome-wide analysis reveals the genomic features of the turkey vulture (Cathartes aura) as a scavenger

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Cathartidae is a small family of large-bodied carrion-feeding birds, of which the turkey vulture (Cathartes aura, Cathartidae) is the most widespread distributed. To investigate the chemoreception system, detoxification system, and immune system in the turkey vulture, we compared its genome to 14 other avian genomes. Comparative genomics demonstrated the expansion in the chemoreception system, especially the olfactory receptors, while the genes in the detoxification system of the turkey vulture did not show apparent expansion. We identified five positively selected genes associated with the immune system in the turkey vulture, which was likely to strengthen the immune defense against pathogenic invasion. Functional enrichment analysis indicated that many positively selected genes were involved in the regulation of immune system processes, implying important reorganization of the immune system in the turkey vulture. The turkey vulture-specific missense mutations were found in one positively selected gene (BCL6), and all the missense mutations were classified as deleterious by PolyPhen-2, possibly contributing to immune adaptation to the carrion feeding. Furthermore, we identified four turkey vulture-specific missense mutations in three β-defensin genes of the turkey vulture, which was an indispensable part in the innate immunity (a natural barrier against invasive microbes including bacteria, fungi, and viruses). Our genomic analyses in the turkey vulture provided insights into the genetic signatures of the adaptation to the carrion feeding.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arguello JR, Cardoso-Moreira M, Grenier JK, Gottipati S, Clark AG, Benton R (2016) Extensive local adaptation within the chemosensory system following Drosophila melanogaster’s global expansion. Nat Commun 7:11855

    Article  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baxi KN, Dorries KM, Eisthen HL (2006) Is the vomeronasal system really specialized for detecting pheromones? Trends Neurosci 29:1–7

    Article  CAS  PubMed  Google Scholar 

  • Birney E, Clamp M, Durbin R (2004) GeneWise and genomewise. Genome Res 14:988–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai Q, Qian X, Lang Y, Luo Y, Xu J, Pan S, Hui Y, Gou C, Cai Y, Hao M, Zhao J (2013) Genome sequence of ground tit Pseudopodoceshumilis and its adaptation to high altitude. Genome Biol 14:R29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Yang P, Jiang F, Wei Y, Ma Z, Kang L (2010) De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS One 5:15633

    Article  CAS  Google Scholar 

  • Choi YS, Kageyama R, Eto D, Escobar TC, Johnston RJ, Monticelli L, Lao C, Crotty S (2011) ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34:932–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung O, Jin S, Cho YS, Lim J, Kim H, Jho S, Kim HM, Jun J, Lee H, Chon A, Ko J (2015) The first whole genome and transcriptome of the cinereous vulture reveals adaptation in the gastric and immune defense systems and possible convergent evolution between the Old and New World vultures. Genome Biol 16:215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuperus T, Coorens M, van Dijk A, Haagsman HP (2013) Avian host defense peptides. Dev Comp Immunol 41:352–369

    Article  CAS  PubMed  Google Scholar 

  • De Bie T, Cristianini N, Demuth JP, Hahn MW (2006) Cafe: a computational tool for the study of gene family evolution. Bioinformatics 22:1269–1271

    Article  CAS  PubMed  Google Scholar 

  • Del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (2018) Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. https://www.hbw.com/node/52940. Accessed 19 Sept 2018

  • DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl Protein Crystallogr 40:82–92

    Google Scholar 

  • Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206

    Article  CAS  PubMed  Google Scholar 

  • Ericson PG, Anderson CL, Britton T, Elzanowski A, Johansson US, Källersjö M, Ohlson JI, Parsons TJ, Zuccon D, Mayr G (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2:543–547

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaudet P, Lane L, Fey P, Bridge A, Poux S, Auchincloss A, Axelsen K, Braconi Quintaje S, Boutet E, Brown P, Coudert E (2009) Collaborative annotation of genes and proteins between UniProtKB/Swiss-Prot and dictyBase. Database 2009:bap016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez LG, Houston DC, Cotton P, Tye A (1994) The role of greater yellow-headed vultures Cathartesmelambrotus as scavengers in neotropical forest. Ibis 136:193–196

    Article  Google Scholar 

  • Griffiths CS, Barrowclough GF, Groth JG, Mertz LA (2007) Phylogeny, diversity, and classification of the Accipitridae based on DNA sequences of the RAG-1 exon. J Avian Biol 38:587–602

    Article  Google Scholar 

  • Gruber CW, Muttenthaler M (2012) Discovery of defense-and neuropeptides in social ants by genome-mining. PLoS One 7:e32559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    Article  CAS  PubMed  Google Scholar 

  • Helbig AJ, Seibold I (1996) Are storks and new world vultures paraphyletic? Mol Phylogenet Evol 2:315–319

    Article  Google Scholar 

  • Hellgren O, Ekblom R (2010) Evolution of a cluster of innate immune genes (β-defensins) along the ancestral lines of chicken and zebra finch. Immunome Res 6:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrada G, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90:763–773

    Article  CAS  PubMed  Google Scholar 

  • Hertel F (1994) Diversity in body size and feeding morphology within past and present vulture assemblages. Ecology 75:1074–1084

    Article  Google Scholar 

  • Higgs R, Lynn DJ, Cahalane S, Alaña I, Hewage CM, James T, Lloyd AT, O’Farrelly C (2007) Modification of chicken avian β-defensin-8 at positively selected amino acid sites enhances specific antimicrobial activity. Immunogenetics 59:573–580

    Article  CAS  PubMed  Google Scholar 

  • Houston DC (1988) Competition for food between Neotropical vultures in forest. Ibis 130:402–417

    Article  Google Scholar 

  • Hron JD, Caplan L, Gerth AJ, Schwartzberg PL, Peng SL (2004) SH2D1A regulates T-dependent humoral autoimmunity. J Exp Med 200:261–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu YM, Zhang Y, You Y, Wang D, Li H, Duramad O, Qin XF, Dong C, Lin X (2007) The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol 8:198

    Article  CAS  PubMed  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2008) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1

    Article  CAS  PubMed Central  Google Scholar 

  • Huang Y, Li Y, Burt DW, Chen H, Zhang Y, Qian W, Kim H, Gan S, Zhao Y, Li J, Yi K (2013) The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet 45:776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes AL (1999) Evolutionary diversification of the mammalian defensins. Cell Mol Life Sci 56:94–103

    Article  CAS  PubMed  Google Scholar 

  • Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SY, Faircloth BC, Nabholz B, Howard JT, Suh A (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D, Barnett B, Dent AL, Craft J, Crotty S (2009) Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325:1006–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan H, Chen H, Chen LC, Wang BB, Sun L, Ma MY, Fang SG, Wan QH (2014) The first report of a Pelecaniformes defensin cluster: characterization of β-defensin genes in the crested ibis based on BAC libraries. Sci Rep 4:6923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Duc D, Renaud G, Krishnan A, Almén MS, Huynen L, Prohaska SJ, Ongyerth M, Bitarello BD, Schiöth HB, Hofreiter M, Stadler PF (2015) Kiwi genome provides insights into evolution of a nocturnal lifestyle. Genome Biol 16:147

    Article  PubMed  PubMed Central  Google Scholar 

  • Lerner HR, Mindell DP (2005) Phylogeny of eagles, Old World vultures, and other Accipitridae based on nuclear and mitochondrial DNA. Mol Phylogenet Evol 37:327–346

    Article  CAS  PubMed  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  • Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Zhu S, Jia Q, Yuan D, Ren C, Li K, Liu S, Cui Y, Zhao H, Cao Y, Fang G (2018) The genomic and functional landscapes of developmental plasticity in the American cockroach. Nat Commun 9:1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long SA, Cerosaletti K, Wan JY, Ho JC, Tatum M, Wei S, Shilling HG, Buckner JH (2011) An autoimmune-associated variant in PTPN2 reveals an impairment of IL-2R signaling in CD4+ T cells. Genes Immun 12:116

    Article  CAS  PubMed  Google Scholar 

  • Löytynoja A, Goldman N (2010) webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinform 11:579

    Article  CAS  Google Scholar 

  • Lynn DJ (2007) Avian beta-defensin nomenclature: a community proposed update. Immunol Lett 110:86–89

    Article  CAS  PubMed  Google Scholar 

  • Matsunami H, Buck LB (1997) A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90:775–784

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951

    Article  CAS  PubMed  Google Scholar 

  • Pillai PS, Molony RD, Martinod K, Dong H, Pang IK, Tal MC, Solis AG, Bielecki P, Mohanty S, Trentalange M, Homer RJ (2016) Mx1 reveals innate pathways to antiviral resistance and lethal influenza disease. Science 352:463–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D, Crandall K (2005) Modeltest 3.7. Program and documentation. http://darwin.uvigo.es. Accessed 8 June 2018

  • Reed TM, Rocke TE (1992) The role of avian carcasses in botulism epizootics. Wildl Soc Bull 20:175–182

    Google Scholar 

  • Reeves NM (2009) Taphonomic effects of vulture scavenging. J Forensic Sci 54:523–528

    Article  PubMed  Google Scholar 

  • Roggenbuck M, Schnell IB, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, Sørensen SJ, Gilbert MT, Graves GR, Hansen LH (2014) The microbiome of new world vultures. Nat Commun 5:5498

    Article  CAS  PubMed  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) Swiss-model: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semple F, Dorin JR (2012) β-Defensins: multifunctional modulators of infection, inflammation and more? J Innate Immun 4:337–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semple CA, Taylor K, Eastwood H, Barran PE, Dorin JR (2006) β-Defensin evolution: selection complexity and clues for residues of functional importance. Biochem Soc Trans 34:257–262

    Article  CAS  PubMed  Google Scholar 

  • Seo MD, Won HS, Kim JH, Mishig-Ochir T, Lee BJ (2012) Antimicrobial peptides for therapeutic applications: a review. Molecules 17:12276–12286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Slack KE, Delsuc F, Mclenachan PA, Arnason U, Penny D (2007) Resolving the root of the avian mitogenomic tree by breaking up long branches. Mol Phylogenet Evol 42:1–3

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Mura JC, Lemus ML, Hertel F (2015) Plastic material in the diet of the turkey vulture (Cathartes aura) in the Atacama Desert, Chile. Wilson J Ornithol 127:134–138

    Article  Google Scholar 

  • Unni S, Huang Y, Hanson RM, Tobias M, Krishnan S, Li WW, Nielsen JE, Baker NA (2011) Web servers and services for electrostatics calculations with APBS and PDB2PQR. J Comput Chem 32:1488–1491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Liu P, Wan ZY, Huang SQ, Wen YF, Lin G, Yue GH (2016) RNA-Seq revealed the impairment of immune defence of tilapia against the infection of Streptococcus agalactiae with simulated climate warming. Fish Shellfish Immun 55:679–689

    Article  CAS  Google Scholar 

  • Wu J, Mao X, Cai T, Luo J, Wei L (2006) KOBAS server: a web-based platform for automated annotation and pathway identification. Nucleic Acids Res 34:W720–W724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Hughes AL, Ando J, Matsuda Y, Cheng JF, Skinner-Noble D, Zhang G (2004) A genome-wide screen identifies a single β-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genom 5:56

    Article  CAS  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A (2014) Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346:1311–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Fuchs CD, Halilbasic E, Trauner M (2016) Bile acids in regulation of inflammation and immunity: friend or foe. Clin Exp Rheumatol 34:25–31

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Mr. Qinchao Wen for valuable advice.

Funding

This work was supported by the National Natural Science Foundation of China (31702032) and the National Key Program of Research and Development, Ministry of Science and Technology (2016YFC0503200).

Author information

Authors and Affiliations

  1. Key Laboratory of Bioresources and Ecoenvironment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, 610064, People’s Republic of China

    Chuang Zhou, Guannan Wang, Haoran Yu, Hongmei Tu, Megan Price, Yang Meng & Bisong Yue

  2. Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu, 610064, People’s Republic of China

    Yang Geng, Wei Wu & Zhenxin Fan

Authors
  1. Chuang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guannan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haoran Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yang Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongmei Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Megan Price
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhenxin Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yang Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bisong Yue
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CZ and BSY designed and supervised the project CZ, GNW, HY, YG, WW, and HMT performed the bioinformatic analyses. CZ wrote the manuscript. All authors contributed to revising the manuscript.

Corresponding authors

Correspondence to Yang Meng or Bisong Yue.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1172 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, C., Wang, G., Yu, H. et al. Genome-wide analysis reveals the genomic features of the turkey vulture (Cathartes aura) as a scavenger. Mol Genet Genomics 294, 679–692 (2019). https://doi.org/10.1007/s00438-019-01541-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-019-01541-3

Keywords

Search

Navigation