Toll-like receptor diversity in 10 threatened bird species: relationship with microsatellite heterozygosity

Conservation Genetics

Volumn 16, Issue 3, 2015, Pages 595-611

  Grueber, Catherine E ^a,b   Knafler, Gabrielle J ^a   King, Tania M ^a   Senior, Alistair M ^b   Grosser, Stefanie ^a   Robertson, Bruce ^a   Weston, Kerry A ^a   Brekke, Patricia ^c   Harris, Christian L W ^a   Jamieson, Ian G ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF SYDNEY   (Australia)

^c INSTITUTE OF ZOOLOGY   (United Kingdom)

Author keywords

Apterygiformes; Conservation; Gruiformes; Immunity genes; Inbreeding; Passeriformes; Psittaciformes

Indexed keywords

EID: 84939955697     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-014-0685-x     Document Type: Article

References (98)

1. Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol 21:433–438
2. Alcaide M, Edwards SV (2011) Molecular evolution of the toll-like receptor multigene family in birds. Mol Biol Evol 28:1703–1715
3. Alho JS, Lillandt BG, Jaari S, Merila J (2009) Multilocus heterozygosity and inbreeding in the Siberian jay. Conserv Genet 10:605–609. doi:10.1007/s10592-008-9588-z
4. Alho JS, Välimäki K, Merilä J (2010) Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity–heterozygosity correlation. Mol Ecol Resour 10:720–722. doi:10.1111/j.1755-0998.2010.02830.x
5. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Oxford
6. Amos W, Worthington Wilmer J, Fullard K et al (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond Ser B 268:2021–2027
7. Areal H, Abrantes J, Esteves P (2011) Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evol Biol 11:368. doi:10.1186/1471-2148-11-368
8. Babik W, Taberlet P, Ejsmond MJ, Radwan J (2009) New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol Ecol Resour 9:713–719. doi:10.1111/j.1755-0998.2009.02622.x
9. Bainová H, Králová T, Bryjová A et al (2014) First evidence of independent pseudogenization of Toll-like receptor 5 in passerine birds. Dev Comp Immunol 45:151–155
10. Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031
11. Barreiro LB, Ben-Ali M, Quach H et al (2009) Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet 5:e1000562. doi:10.1371/journal.pgen.1000562
12. Basse B, Flux I, Innes J (2003) Recovery and maintenance of North Island kokako (Callaeas cinereawilsoni) populations through pulsed pest control. Biol Conserv 109:259–270. doi:10.1016/S0006-3207(02)00154-4
13. Bates D, Maechler M (2009) lme4: linear mixed-effects models using S4 classes
14. BirdLife International (2013) Cyanoramphus novaezelandiae. IUCN 2013 IUCN Red List Threat. Species Version 20132. BirdLife International, Cambridge
15. Boessenkool S, Taylor SS, Tepolt CK et al (2007) Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges. Conserv Genet 8:705–714
16. Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Extensive MHC class II B gene duplication in a Passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448–460. doi:10.1093/jhered/esq018
17. Bollmer JL, Ruder EA, Johnson JA et al (2011) Drift and selection influence geographic variation at immune loci of prairie-chickens. Mol Ecol 20:4695–4706. doi:10.1111/j.1365-294X.2011.05319.x
18. Brekke P, Bennett PM, Santure AW, Ewen JG (2011) High genetic diversity in the remnant island population of hihi and the genetic consequences of re-introduction. Mol Ecol 20:29–45. doi:10.1111/j.1365-294X.2010.04923.x
19. Casquet J, Thebaud C, Gillespie RG (2012) Chelex without boiling, a rapid and easy technique to obtain stable amplifiable DNA from small amounts of ethanol-stored spiders. Mol Ecol Resour 12:136–141. doi:10.1111/j.1755-0998.2011.03073.x
20. Chapman JR, Nakagawa S, Coltman DW et al (2009) A quantitative review of heterozygosity–fitness correlations in animal populations. Mol Ecol 18:2746–2765. doi:10.1111/j.1365-294X.2009.04247.x
21. Clout MN (2006) A celebration of kakapo: progress in the conservation of an enigmatic parrot. Notornis 53:1–2
22. Coltman DW, Pilkington JG, Smith JA, Pemberton J (1999) Parasite-mediated selection against inbred Soay sheep in a free-living island population. Evolution 53:1259–1267
23. Cormican P, Lloyd AT, Downing T et al (2009) The avian toll-like receptor pathway—subtle differences amidst general conformity. Dev Comp Immunol 33:967–973. doi:10.1016/j.dci.2009.04.001
24. Dawe MR (1979) Behaviour and ecology of the red-crowned kakariki (Cyanoramphus novaezelandiae) in relation to management. Department of Zoology, University of Auckland, Auckland
25. Deakin JE (2012) Marsupial genome sequences: providing insight into evolution and disease. Scientifica. doi:10.6064/2012/543176
26. Duncan RP, Blackburn TM (2004) Extinction and endemism in the New Zealand avifauna. Glob Ecol Biogeogr 13:509–517
27. Ericson PGP, Christidis L, Cooper A et al (2002) A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc R Soc Lond B 269:235–241. doi:10.1098/rspb.2001.1877
28. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112
29. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
30. Galan M, Guivier E, Caraux G et al (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genom 11:296
31. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722. doi:10.1111/j.0014-3820.2003.tb00580.x
32. Gaze PD (1985) Distribution of yellowheads (Mohoua ochrocephala). Notornis 32:261–269
33. Gelman A, Su Y-S, Yajima M, et al (2009) arm: data analysis using regression and multilevel/hierarchical models. R-package. Available at http://CRAN.R-project.org/package=arm
34. Grueber CE, Jamieson IG (2011) Low genetic diversity and small population size of Takahe Porphyrio hochstetteri upon European arrival in New Zealand. Ibis 153:384–394
35. Grueber CE, Jamieson IG (2013) Primers for amplification of innate immunity Toll-like receptors in threatened birds of the Apterygiformes, Gruiformes, Psittaciformes and Passeriformes. Conserv Genet Resour 5:1043–1047. doi:10.1007/s12686-013-9965-x
36. Grueber CE, King TM, Waters JM, Jamieson IG (2008a) Isolation and characterization of microsatellite loci from the endangered New Zealand takahe (Gruiformes; Rallidae; Porphyrio hochstetteri). Mol Ecol Resour 8:884–886. doi:10.1111/j.1755-0998.2008.02098.x
37. Grueber CE, Wallis GP, Jamieson IG (2008b) Heterozygosity–fitness correlations and their relevance to studies on inbreeding depression in threatened species. Mol Ecol 17:3978–3984. doi:10.1111/j.1365-294X.2008.03910.x
38. Grueber CE, Waters JM, Jamieson IG (2011) The imprecision of heterozygosity–fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species. Mol Ecol 20:67–79
39. Grueber CE, Wallis GP, King T, Jamieson IG (2012) Variation at innate immunity Toll-like receptor genes in a bottlenecked population of a New Zealand robin. PLoS One 7:e45011. doi:10.1371/journal.pone.0045011
40. Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll-like receptor (TLR) immunity loci in a reintroduced population of a threatened species. Mol Ecol 22:4470–4482. doi:10.1111/mec.12404
41. Grueber CE, Wallis GP, Jamieson IG (2014) Episodic positive selection in the evolution of avian Toll-like receptor innate immunity genes. PLoS One. doi:10.1371/journal.pone.0089632
42. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22
43. Hartmann SA, Schaefer HM, Segelbacher G (2014) Genetic depletion at adaptive but not neutral loci in an endangered bird species. Mol Ecol. doi:10.1111/mec.12975
44. Hedrick PW (1998) Balancing selection and MHC. Genetica 104:207–214
45. Hedrick PW (2012) What is the evidence for heterozygote advantage selection? Trends Ecol Evol 27:698–704. doi:10.1016/j.tree.2012.08.012
46. Higgins PJ (1999) Handbook of Australian, New Zealand and Antarctic birds. Oxford University Press, Melbourne
47. Higgins PJ, Peter JM (2002) Handbook of Australian, New Zealand and Antarctic birds. Volume 6: Pardalotes to shrike-thrushes. Oxford University Press, Melbourne
48. Higham T, Anderson A, Jacomb C (1999) Dating the first New Zealanders: the chronology of Wairau Bar. Antiquity 73:420–427
49. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70
50. Holzapfel S, Robertson HA, McLennan JA et al (2009) Kiwi (Apteryx spp.) recovery plan, 2008–2018. Department of Conservation, Wellington
51. Hoosen S, Jamieson IG (2003) The distribution and current status of New Zealand saddleback Philesturnus carunculatus. Bird Conserv Int 13:79–95
52. Hudson QJ, Wilkins JR, Waas JR, Hogg ID (2000) Low genetic variability in small populations of New Zealand kokako Callaeas cinera wilsoni. Biol Conserv 96:105–112
53. Innes J, Hay R, Flux I et al (1999) Successful recovery of North Island kokako Callaeas cinerea wilsoni populations, by adaptive management. Biol Conserv 87:201–214. doi:10.1016/S0006-3207(98)00053-6
54. Jamieson IG, Tracy LN, Fletcher D, Armstrong DP (2007) Moderate inbreeding depression in a reintroduced population of North Island robins. Anim Conserv 10:95–102. doi:10.1111/j.1469-1795.2006.00078.x
55. Jepson A, Banya W, Sisay-Joof F et al (1997) Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Infect Immun 65:872–876
56. Keestra AM, de Zoete MR, Bouwman LI et al (2013) Unique features of chicken Toll-like receptors. Dev Comp Immunol 41:316–323. doi:10.1016/j.dci.2013.04.009
57. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi:10.1016/S0169-5347(02)02489-8
58. Kirk H, Freeland JR (2011) Applications and implications of neutral versus non-neutral markers in molecular ecology. Int J Mol Sci 12:3966–3988
59. Lee WG, Jamieson IG (2001) The takahe: fifty years of conservation management and research. University of Otago Press, Dunedin
60. Lettink M, Jamieson IG, Millar CD, Lambert DM (2002) Mating system and genetic variation in the endangered New Zealand takahe. Conserv Genet 3:427–434
61. Levene H (1949) On a matching problem arising in genetics. Ann Math Stat 20:91–94. doi:10.1214/aoms/1177730093
62. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187
63. Ljungqvist M, Akesson M, Hansson B et al (2010) Do microsatellites reflect genome-wide genetic diversity in natural populations? A comment on Väli et al. (2008). Mol Ecol 19:851–855
64. Meglécz E, Piry S, Desmarais E et al (2011) SESAME (SEquence Sorter & AMplicon Explorer): genotyping based on high-throughput multiplex amplicon sequencing. Bioinformatics 27:277–278. doi:10.1093/bioinformatics/btq641
65. Merton DV (1975) The saddleback: its status and conservation. In: Martin RD (ed) Breeding endangered species in captivity. Academic Press, London, pp 61–74
66. Michelsen-Heath S, Gaze P (2007) Changes in abundance and distribution of the rock wren (Xenicus gilviventris) in the South Island, New Zealand. Notornis 54:71–78
67. Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721
68. Miller JM, Malenfant RM, David P et al (2014) Estimating genome-wide heterozygosity: effects of demographic history and marker type. Heredity 112:240–247. doi:10.1038/hdy.2013.99
69. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
70. O’Donnell CFJ, Roberts A, Lyall J (2002) Mohua (yellowhead) recovery plan 2002–2012. Department of Conservation, Wellington
71. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. doi:10.1038/sj.hdy.6800724
72. Powlesland RG, Merton DV, Cockrem JF (2006) A parrot apart: the natural history of the kakapo (Strigops habroptilus), and the context of its conservation management. Notornis 53:3–26
73. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
74. Robertson BC, Minot EO, Lambert DM (2000) Microsatellite primers for the kakapo (Strigops habroptilus) and their utility in other parrots. Conserv Genet 1:93–95
75. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90
76. Slate J, David P, Dodds KG et al (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265
77. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988
78. Szulkin M, Bierne N, David P (2010) Heterozygosity–fitness correlations: a time for reappraisal. Evolution 64:1202–1217
79. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
80. Taylor SS, Jamieson IG (2008a) No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Mol Ecol 17:545–556. doi:10.1111/j.1365-294X.2007.03591.x
81. Taylor SS, Jamieson IG (2008b) No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Mol Ecol 17:545–556. doi:10.1111/j.1365-294X.2007.03591.x
82. Taylor C, Castro IC, Griffiths R (2005) Hihi/stitchbird (Notiomystis cincta) recovery plan, 2004–2009. Department of Conservation, Wellington
83. Taylor SS, Jamieson IG, Wallis GP (2007) Historic and contemporary levels of genetic variation in two New Zealand passerines with different histories of decline. J Evol Biol 20:2035–2047
84. Temperley N, Berlin S, Paton I et al (2008) Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 9:62
85. Tracy L, Jamieson I (2011) Historic DNA reveals contemporary population structure results from anthropogenic effects, not pre-fragmentation patterns. Conserv Genet 12:517–526. doi:10.1007/s10592-010-0158-9
86. Turner AK, Begon M, Jackson JA et al (2011) Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLoS Genet 7:e1002343
87. Uematsu S, Akira S (2008) Toll-like receptors (TLRs) and their ligands. Handb Exp Pharmacol 183:1–20. doi:10.1007/978-3-540-72167-3_1
88. Väli U, Einarsson A, Waits L, Ellegren H (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17:3808–3817. doi:10.1111/j.1365-294X.2008.03876.x
89. Veitch CR (2002) Eradication of Pacific rats (Rattus exulans) from Tiritiri Matangi Island, Hauraki Gulf, New Zealand. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN, Gland, pp 360–364
90. Vinkler M, Albrecht T (2009) The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zool 58:15–28
91. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
92. Watterson GA (1978) An analysis of multi-allelic data. Genetics 88:171–179
93. Werling D, Jann OC, Offord V et al (2009) Variation matters: TLR structure and species-specific pathogen recognition. Trends Immunol 30:124–130. doi:10.1016/j.it.2008.12.001
94. Westerdahl H (2007) Passerine MHC: genetic variation and disease resistance in the wild. J Ornithol 148:469–477. doi:10.1007/s10336-007-0230-5
95. Weston KA (2014) Conservation genetics of rock wren (Xenicus gilviventris). PhD, Department of Zoology, University of Otago
96. Weston KA, Robertson BC (2014) Isolation and characterisation of 14 microsatellites for the New Zealand rock wren Xenicus gilviventris. Conserv Genet Resour. doi:10.1007/s12686-013-0018-2
97. Wickes C, Crouchley D, Maxwell J (2009) Takahe recovery plan, 2007–2012. Department of Conservation, Wellington
98. Ziesemann B, Brunton DH, Castro IC (2011) Nesting success and breeding ecology in a high-density population of Brown Kiwi (Apteryx mantelli). Emu 111:148–154