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Immunogenetics

, Volume 67, Issue 3, pp 195–201 | Cite as

Diversity in the Toll-like receptor genes of the Tasmanian devil (Sarcophilus harrisii)

  • Jian Cui
  • Yuanyuan Cheng
  • Katherine Belov
Brief Communication

Abstract

The Tasmanian devil is an endangered marsupial species that has survived several historical bottlenecks and now has low genetic diversity. Here we characterize the Toll-like receptor (TLR) genes and their diversity in the Tasmanian devil. TLRs are a key innate immune gene family found in all animals. Ten TLR genes were identified in the Tasmanian devil genome. Unusually low levels of diversity were found in 25 devils from across Tasmania. We found two alleles at TLR2, TLR3 and TLR6. The other seven genes were monomorphic. The insurance population, which safeguards the species from extinction, has successfully managed to capture all of these TLR alleles, but concerns remain for the long-term survival of this species.

Keywords

Toll-like receptors Genetic diversity Tasmanian devil Population bottleneck 

Notes

Acknowledgments

The wild devil samples used in this study were kindly provided by Menna Jones and Rodrigo Hamede from the School of Zoology at the University of Tasmania and the Save the Tasmanian Devil Program. We thank Carolyn Hogg from the Zoo and Aquarium Association for providing captive samples from the Save the Tasmanian Devil Insurance Program. This work was funded by an Australian Research Council grant to KB. KB is supported by an ARC Future Fellowship.

Supplementary material

251_2014_823_MOESM1_ESM.pdf (14.4 mb)
ESM 1 (PDF 14759 kb)

References

  1. Babik W, Pabijan M, Arntzen J, Cogalniceanu D, Durka W, Radwan J (2009) Long‐term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol 18:769–781CrossRefPubMedGoogle Scholar
  2. Bell JK, Mullen GE, Leifer CA, Mazzoni A, Davies DR, Segal DM (2003) Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol 24:528–533CrossRefPubMedGoogle Scholar
  3. Bharti D et al. (2014) The role of TLR9 polymorphism in susceptibility to pulmonary tuberculosis. Immunogenetics: 1–7Google Scholar
  4. Bochud P-Y et al (2007) Polymorphisms in Toll-like receptor 9 influence the clinical course of HIV-1 infection. Aids 21:441–446CrossRefPubMedGoogle Scholar
  5. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102CrossRefPubMedGoogle Scholar
  6. Brown OJ (2006) Tasmanian devil (Sarcophilus harrisii) extinction on the Australian mainland in the mid-Holocene: multicausality and ENSO intensification vol 30Google Scholar
  7. Brüniche-Olsen A, Jones ME, Austin JJ, Burridge CP, Holland BR (2014) Extensive population decline in the Tasmanian devil predates European settlement and devil facial tumour disease. Biol lett 10:20140619CrossRefPubMedGoogle Scholar
  8. Casanova J-L, Abel L (2002) Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol 20:581–620CrossRefPubMedGoogle Scholar
  9. Castro-Prieto A, Wachter B, Sommer S (2011) Cheetah paradigm revisited: MHC diversity in the world’s largest free-ranging population. Mol Biol Evol 28:1455–1468CrossRefPubMedGoogle Scholar
  10. Cheng Y, Belov K (2014) Characterisation of non-classical MHC class I genes in the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 66:727–735. doi: 10.1007/s00251-014-0804-3 CrossRefPubMedGoogle Scholar
  11. Cheng Y, Sanderson C, Jones M, Belov K (2012) Low MHC class II diversity in the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 64:525–533CrossRefPubMedGoogle Scholar
  12. Ellegren H, Hartman G, Johansson M, Andersson L (1993) Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc Natl Acad Sci U S A 90:8150–8153CrossRefPubMedCentralPubMedGoogle Scholar
  13. Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. P Roy Soc B-Biol Sci 274:2365–2371CrossRefGoogle Scholar
  14. Georgel P, Macquin C, Bahram S (2009) The heterogeneous allelic repertoire of human Toll-like receptor (TLR) genes. PLoS ONE 4:e7803CrossRefPubMedCentralPubMedGoogle Scholar
  15. Grueber CE, Wallis GP, King TM, Jamieson IG (2012) Variation at innate immunity Toll-like receptor genes in a bottlenecked population of a New Zealand robin. PLoS ONE 7:e45011CrossRefPubMedCentralPubMedGoogle Scholar
  16. Gutierrez‐Espeleta GA, Hedrick PW, Kalinowski ST, Garrigan D, Boyce WM (2001) Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation. Heredity 86:439–450CrossRefPubMedGoogle Scholar
  17. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series pp 95–98Google Scholar
  18. Hawkins C et al (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biol Conserv 131:307–324Google Scholar
  19. Hawn TR et al (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to Legionnaires’ disease. J Exp Med 198:1563–1572CrossRefPubMedCentralPubMedGoogle Scholar
  20. Hawn TR, Verbon A, Janer M, Zhao LP, Beutler B, Aderem A (2005) Toll-like receptor 4 polymorphisms are associated with resistance to Legionnaires’ disease. Proc Natl Acad Sci U S A 102:2487–2489CrossRefPubMedCentralPubMedGoogle Scholar
  21. Hedrick PW, Lee RN, Buchanan C (2003) Canine parvovirus enteritis, canine distemper, and major histocompatibility complex genetic variation in Mexican wolves. J Wildl Dis 39:909–913CrossRefPubMedGoogle Scholar
  22. Heng J, Su J, Huang T, Dong J, Chen L (2011) The polymorphism and haplotype of < i > TLR3</i > gene in grass carp (< i > Ctenopharyngodon idella </i>) and their associations with susceptibility/resistance to grass carp reovirus. Fish Shellfish Immunol 30:45–50CrossRefPubMedGoogle Scholar
  23. Hidmark A, von Saint PA, Dalpke AH (2012) Cutting edge: TLR13 is a receptor for bacterial RNA. J Immunol 189:2717–2721CrossRefPubMedGoogle Scholar
  24. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5:987–995CrossRefPubMedGoogle Scholar
  25. Jin MS, Lee J-O (2008) Structures of the Toll-like receptor family and its ligand complexes. Immunity 29:182–191CrossRefPubMedGoogle Scholar
  26. Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209CrossRefPubMedGoogle Scholar
  27. Jones ME et al (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proc Natl Acad Sci U S A 105:10023–10027CrossRefPubMedCentralPubMedGoogle Scholar
  28. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498CrossRefPubMedGoogle Scholar
  29. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struc Biol 11:725–732CrossRefGoogle Scholar
  30. Lazarus R et al (2004) Toll-like receptor 10 genetic variation is associated with asthma in two independent samples. Am J Resp Crit Care 170:594–600CrossRefGoogle Scholar
  31. Lazzaro BP, Sceurman BK, Clark AG (2004) Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303:1873–1876CrossRefPubMedGoogle Scholar
  32. Li X-D, Chen ZJ (2012) Sequence specific detection of bacterial 23S ribosomal RNA by TLR13. Elife 1Google Scholar
  33. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  34. Manzoor Z, Koh Y-S (2012) Bacterial 23S ribosomal RNA, a ligand for Toll-like receptor 13. J Bacteriol Virol 42:357–358CrossRefGoogle Scholar
  35. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364CrossRefPubMedGoogle Scholar
  36. McCallum H et al (2007) Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4:318–325CrossRefGoogle Scholar
  37. Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow‐necked mouse (Apodemus flavicollis). Mol Ecol 14:2233–2243CrossRefPubMedGoogle Scholar
  38. Miller W et al (2011) Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci U S A 108:12348–12353CrossRefPubMedCentralPubMedGoogle Scholar
  39. Mockenhaupt FP et al (2006) Toll-like receptor (TLR) polymorphisms in African children: common TLR-4 variants predispose to severe malaria. Proc Natl Acad Sci U S A 103:177–182CrossRefPubMedCentralPubMedGoogle Scholar
  40. Morris K, Austin JJ, Belov K (2013) Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics. Biol lett 9:20120900CrossRefPubMedCentralPubMedGoogle Scholar
  41. Murchison EP et al (2010) The Tasmanian devil transcriptome reveals Schwann cell origins of a clonally transmissible cancer. Science 327:84–87CrossRefPubMedCentralPubMedGoogle Scholar
  42. Murchison EP et al (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148:780–791CrossRefPubMedCentralPubMedGoogle Scholar
  43. Pasare C, Medzhitov R (2005) Toll-like receptors: linking innate and adaptive immunity. In: Mechanisms of Lymphocyte Activation and Immune Regulation X. Springer, pp 11–18Google Scholar
  44. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  45. Reismann P et al (2004) Lack of association between polymorphisms of the Toll-like receptor 4 gene and cerebral ischemia. J Neurol 251:853–858PubMedGoogle Scholar
  46. Roach JC et al (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A 102:9577–9582CrossRefPubMedCentralPubMedGoogle Scholar
  47. Sackesen C et al (2005) The effect of polymorphisms at the CD14 promoter and the TLR4 gene on asthma phenotypes in Turkish children with asthma. Allergy 60:1485–1492CrossRefPubMedGoogle Scholar
  48. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  49. Siddle HV, Sanderson C, Belov K (2007) Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 59:753–760CrossRefPubMedGoogle Scholar
  50. Siddle HV, Marzec J, Cheng Y, Jones M, Belov K (2010) MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. P Roy Soc B-Biol Sci 277:2001–2006CrossRefGoogle Scholar
  51. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16CrossRefPubMedCentralPubMedGoogle Scholar
  52. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376CrossRefPubMedGoogle Scholar
  53. 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 28:2731–2739CrossRefPubMedCentralPubMedGoogle Scholar
  54. Tantisira K et al (2004) Toll-like receptor 6 gene (TLR6): single-nucleotide polymorphism frequencies and preliminary association with the diagnosis of asthma. Genes Immunol 5:343–346CrossRefGoogle Scholar
  55. Uematsu S, Akira S (2007) Toll-like receptors and type I interferons. J Biol Chem 282:15319–15323CrossRefPubMedGoogle Scholar
  56. Xue Y, Zhao Z, Wang H, Jin L, Liu C, Wang Y, Li J (2010) Toll like receptors 2 and 4 gene polymorphisms in a southeastern Chinese population with tuberculosis. Int J Immunogenet 37:135–138CrossRefPubMedGoogle Scholar
  57. Zhang X-y, Gao Y-n (2004) To design PCR primers with oligo 6 and primer premier 5. Bioinforma 4:003Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Faculty of Veterinary ScienceUniversity of SydneySydneyAustralia

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