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Low adaptive and neutral genetic diversity in the endangered Antioquia wren (Thryophilus sernai)

Abstract

Determining the amount and distribution of genetic variation represents a fundamental step for the inference of evolutionary processes acting on populations of endangered species. For these species, adaptive evolutionary potential is highly reduced by the loss of genetic variation due to drift. Here, we examined genetic diversity at the mitochondrial control region (CR), 17 microsatellites, and six Toll-like receptor (TLR) genes, known to play a key role on the innate immune response of vertebrates in the Antioquia wren (AW) Thryophilus sernai, an endangered passerine bird inhabiting the remnant fragments of tropical dry forest in the northernmost part of the Cauca river canyon, Colombia. We found very low variation for the three types of markers. The CR showed scarce variability, while only six of the 17 microsatellites analyzed and two of the six TLRs sequenced were polymorphic. Population structure analyses suggest the occurrence of one single population in the area. Selection tests could not detect signatures of positive selection for the variable sites in the species, and assessment of amino acid changes found within the lineage do not suggest any functional effects that could be associated to selection in either polymorphic TLR loci. Comparisons with species showing widespread and restricted distribution supports a low TLR variability typical of small populations. These results suggest current low evolutionary potential for the species, as its reduced genetic diversity is expected to increase extinction risk by limiting the ability to cope with environmental changes. Our study supports current evidence suggesting drift as the main driver shaping TLR variation.

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Fig. 1
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Data availability

The microsatellite genotypes are available upon request from the corresponding author, and TLR sequences were deposited in Genbank (accession numbers MW027597-MW027612).

References

  1. Alcaide M, Edwards SV (2011) Molecular evolution of the toll-like receptor multigene family in birds. Mol Biol Evol 28:1703–1715. https://doi.org/10.1093/molbev/msq351

    CAS  Article  PubMed  Google Scholar 

  2. 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. https://doi.org/10.1111/j.1755-0998.2010.02830.x

    Article  PubMed  Google Scholar 

  3. Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Philos Trans R Soc Lond B 353:177–186. https://doi.org/10.1098/rstb.1998.0200

    CAS  Article  Google Scholar 

  4. Amos W, Wilmer JW, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc Biol Sci 268:2021–2027. https://doi.org/10.1098/rspb.2001.1751

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Aquadro CF, Greenberg BD (1983) Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics 103:287–312

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Ballard JW, Kreitman M (1995) Is mitochondrial DNA a strictly neutral marker? Trends Ecol Evol 10:485–488. https://doi.org/10.1016/s0169-5347(00)89195-8

    CAS  Article  PubMed  Google Scholar 

  7. 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. https://doi.org/10.1371/journal.pgen.1000562

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Belvin MP, Anderson KV (1996) A conserved signaling pathway: the Drosophila toll-dorsal pathway. Annu Rev Cell Dev Biol 12:393–416. https://doi.org/10.1146/annurev.cellbio.12.1.393

    CAS  Article  PubMed  Google Scholar 

  9. BirdLife I (2017) Thryophilus sernai (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017: e.T103889265A112413460. https://doi.org/10.2305/IUCN.UK.2017-1.RLTS.T103889265A112413460.en. Accessed 30 April 2018

  10. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    CAS  Article  Google Scholar 

  11. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31:24–26, 28

    CAS  Article  Google Scholar 

  12. Bowie RCK, Feldheim KA, Caro LM, Cadena CD (2012) Novel tetranucleotide microsatellite DNA markers for members of the Henicorhina Wood-wren species complex (Aves, Troglodytidae). Conserv Gen Resour 4:419–421. https://doi.org/10.1007/s12686-011-9564-7

    Article  Google Scholar 

  13. Brar RK, Schoenle LA, Stenzler LM, Hall ML, Vehrencamp SL, Lovette IJ (2007) Eleven microsatellite loci isolated from the banded wren (Thryothorus pleurostictus). Mol Ecol Notes 7:69–71. https://doi.org/10.1111/j.1471-8286.2006.01530.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Brownlie R, Allan B (2011) Avian toll-like receptors. Cell Tissue Res 343:121–130. https://doi.org/10.1007/s00441-010-1026-0

    CAS  Article  PubMed  Google Scholar 

  15. Burney CW, Brumfield RT (2009) Ecology predicts levels of genetic differentiation in Neotropical birds. Am Nat 174:358–368

    Article  Google Scholar 

  16. Cabe PR, Marshall KE (2001) Microsatellite loci from the house wren (Troglodytes aedon). Mol Ecol Notes 1:155–156

    CAS  Article  Google Scholar 

  17. Cann RL, Brown WM, Wilson AC (1984) Polymorphic sites and the mechanism of evolution in human mitochondrial DNA. Genetics 106:479–499

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157

    CAS  Article  PubMed  Google Scholar 

  19. Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7

    Article  Google Scholar 

  20. Eimes JA, Bollmer JL, Whittingham LA et al (2011) Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J Evol Biol 24:1847–1856. https://doi.org/10.1111/j.1420-9101.2011.02311.x

    CAS  Article  PubMed  Google Scholar 

  21. Excoffier L, Lischer HE (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. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  22. Fjeldså J (2018) Antioquia Wren (Thryophilus sernai). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the Birds of the World Alive. Lynx Editions, Barcelona. https://www.hbw.com/node/204359. Accessed 29 April 2018

  23. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. https://doi.org/10.1016/j.biocon.2005.05.002

    Article  Google Scholar 

  24. Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA (1999) Do population size bottlenecks reduce evolutionary potential? Animal Conservation forum, vol 4. Cambridge University Press, pp 255–260

  25. Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  26. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722. https://doi.org/10.1111/j.0014-3820.2003.tb00580.x

    CAS  Article  PubMed  Google Scholar 

  27. Gilroy DL, van Oosterhout C, Komdeur J, Richardson DS (2017) Toll-like receptor variation in the bottlenecked population of the endangered Seychelles warbler. Anim Conserv 20:235–250. https://doi.org/10.1111/acv.12307

    Article  Google Scholar 

  28. Gonzalez-Quevedo C, Spurgin LG, Illera JC, Richardson DS (2015) Drift, not selection, shapes toll-like receptor variation among oceanic island populations. Mol Ecol 24:5852–5863. https://doi.org/10.1111/mec.13437

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  30. Graham BA, Heath DD, Mennill DJ (2017) Dispersal influences genetic and acoustic spatial structure for both males and females in a tropical songbird. Ecol Evol 7:10089–10102. https://doi.org/10.1002/ece3.3456

    Article  PubMed  PubMed Central  Google Scholar 

  31. Grueber CE, Jamieson IG (2013) Primers for amplification of innate immunity toll-like receptor loci in threatened birds of the Apterygiformes, Gruiformes, Psittaciformes and Passeriformes. Conserv Genet Resour 5:1043–1047

    Article  Google Scholar 

  32. 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:e45011. https://doi.org/10.1371/journal.pone.0045011

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll-like receptor (TLR) immunity loci in a re-introduced population of a threatened species. Mol Ecol 22:4470–4482. https://doi.org/10.1111/mec.12404

    CAS  Article  PubMed  Google Scholar 

  34. Grueber CE, Wallis GP, Jamieson IG (2014) Episodic positive selection in the evolution of avian toll-like receptor innate immunity genes. PLoS ONE 9:e89632. https://doi.org/10.1371/journal.pone.0089632

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Grueber CE, Knafler GJ, King TM et al (2015) Toll-like receptor diversity in 10 threatened bird species: relationship with microsatellite heterozygosity. Conserv Genet 16:595–611. https://doi.org/10.1007/s10592-014-0685-x

    CAS  Article  Google Scholar 

  36. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  37. Hartmann SA, Schaefer HM, Segelbacher G (2014) Genetic depletion at adaptive but not neutral loci in an endangered bird species. Mol Ecol 23:5712–5725. https://doi.org/10.1111/mec.12975

    Article  PubMed  Google Scholar 

  38. Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964

    Article  Google Scholar 

  39. Hess CM, Edwards SV (2002) The Evolution of the Major Histocompatibility Complex in Birds: Scaling up and taking a genomic approach to the major histocompatibilty complex (mhc) of birds reveals surprising departures from generalities found in mammals in both large-scale structure and the mechanisms shaping the evolution of the mhc. Bioscience 52:423–431

    Article  Google Scholar 

  40. Hoarau G, Rijnsdorp AD, Van der Veer HW, Stam WT, Olsen JL (2002) Population structure of plaice (Pleuronectes platessa L.) in northern Europe: microsatellites revealed large-scale spatial and temporal homogeneity. Mol Ecol 11:1165–1176. https://doi.org/10.1046/j.1365-294x.2002.01515.x

    CAS  Article  PubMed  Google Scholar 

  41. Holdridge LR (1967) Life zone ecology. Tropical Science Center, San José

    Google Scholar 

  42. IAvH (1998) El Bosque seco Tropical (Bs-T) en Colombia. Programa de inventario de la Biodiversidad. Instituto Alexander von Humboldt, Bogotá, Colombia

    Google Scholar 

  43. Jackson H, Morgan BJT, Groombridge JJ (2013) How closely do measures of mitochondrial DNA control region diversity reflect recent trajectories of population decline in birds? Conserv Genet 14:1291–1296. https://doi.org/10.1007/s10592-013-0514-7

    CAS  Article  Google Scholar 

  44. Janeway CA Jr (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 13:11–16. https://doi.org/10.1016/0167-5699(92)90198-G

    CAS  Article  PubMed  Google Scholar 

  45. Jarne P, Lagoda PJ (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429. https://doi.org/10.1016/0169-5347(96)10049-5

    CAS  Article  PubMed  Google Scholar 

  46. Jin MS, Lee JO (2008) Structures of TLR-ligand complexes. Curr Opin Immunol 20:414–419. https://doi.org/10.1016/j.coi.2008.06.002

    CAS  Article  PubMed  Google Scholar 

  47. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik S-G, Lee H, Lee J-O (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130:1071–1082

    CAS  Article  Google Scholar 

  48. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

    CAS  Article  PubMed  Google Scholar 

  49. Kirk H, Freeland JR (2011) Applications and implications of neutral versus non-neutral markers in molecular ecology. Int J Mol Sci 12:3966–3988. https://doi.org/10.3390/ijms12063966

    Article  PubMed  PubMed Central  Google Scholar 

  50. Kobe B, Deisenhofer J (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415–421. https://doi.org/10.1016/0968-0004(94)90090-6

    CAS  Article  PubMed  Google Scholar 

  51. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis Version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460. https://doi.org/10.1126/science.3420403

    CAS  Article  PubMed  Google Scholar 

  53. Lara CE, Cuervo AM, Valderrama SV, Calderón-f D, Cadena CD (2012) A new species of wren (Troglodytidae: Thryophilus) from the dry Cauca River Canyon, northwestern Colombia. Auk 129:537–550

    Article  Google Scholar 

  54. Lara CE, Cuervo AM, Cadena CD (2016) Thryophilus sernai. In: Renjifo LM, Amaya-Villarreal ÁM, Burbano-Girón JB, Velásquez-Tibatá J (2016) Libro rojo de aves de Colombia: Vol 2. Ecosistemas abiertos, secos, insulares, acuáticos, continentales, marinos, tierras altas del Darién y Sierra Nevada de Santa Marta y bosques húmedos del centro, norte y oriente del país. Editorial Pontificia Universidad Javeriana and Instituto Alexander von Humboldt. Bogotá, Colombia

  55. Leigh JW, Bryant D, Nakagawa S (2015) popart: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210x.12410

    Article  Google Scholar 

  56. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145. https://doi.org/10.1038/35100529

    CAS  Article  PubMed  Google Scholar 

  58. Miller HC, Lambert DM (2004a) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191. https://doi.org/10.1007/s00251-004-0666-1

    CAS  Article  PubMed  Google Scholar 

  59. Miller HC, Lambert DM (2004b) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721. https://doi.org/10.1111/j.1365-294X.2004.02368.x

    CAS  Article  PubMed  Google Scholar 

  60. Misch EA, Hawn TR (2008) Toll-like receptor polymorphisms and susceptibility to human disease. Clin Sci (Lond) 114:347–360. https://doi.org/10.1042/CS20070214

    Article  Google Scholar 

  61. Moore RP, Robinson WD, Lovette IJ, Robinson TR (2008) Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol Lett 11:960–968. https://doi.org/10.1111/j.1461-0248.2008.01196.x

    CAS  Article  PubMed  Google Scholar 

  62. Mukherjee S, Sarkar-Roy N, Wagener DK, Majumder PP (2009) Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. Proc Natl Acad Sci 106:7073–7078

    Article  Google Scholar 

  63. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764. https://doi.org/10.1371/journal.pgen.1002764

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205. https://doi.org/10.1093/molbev/mst030

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Nelson-Flower MJ, Germain RR, MacDougall-Shackleton EA et al (2018) Purifying selection in the toll-like receptors of song sparrows Melospiza melodia. J Hered 109:501–509. https://doi.org/10.1093/jhered/esy027

    CAS  Article  PubMed  Google Scholar 

  66. Netea MG, Wijmenga C, O’Neill LA (2012) Genetic variation in Toll-like receptors and disease susceptibility. Nat Immunol 13:535–542. https://doi.org/10.1038/ni.2284

    CAS  Article  PubMed  Google Scholar 

  67. Omueti KO, Mazur DJ, Thompson KS, Lyle EA, Tapping RI (2007) The polymorphism P315L of human toll-like receptor 1 impairs innate immune sensing of microbial cell wall components. J Immunol 178:6387–6394

    CAS  Article  Google Scholar 

  68. Parsons TJ, Muniec DS, Sullivan K et al (1997) A high observed substitution rate in the human mitochondrial DNA control region. Nat Genet 15:363–368. https://doi.org/10.1038/ng0497-363

    CAS  Article  PubMed  Google Scholar 

  69. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21. https://doi.org/10.1038/sj.hdy.6800724

    CAS  Article  PubMed  Google Scholar 

  71. Pond SL, Frost SD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533. https://doi.org/10.1093/bioinformatics/bti320

    CAS  Article  PubMed  Google Scholar 

  72. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275. https://doi.org/10.1111/j.1558-5646.1989.tb04226.x

    Article  PubMed  Google Scholar 

  74. Raymond M, Rousset F (1995) GENEPOP on the Web (Version 3.4). http://wbiomed.curtin.edu.au/genepop/, Updated from Raymond & Rousset

  75. Renjifo LM, Amaya-Villarreal ÁM, Burbano-Girón JB, Velásquez-Tibatá J (2016) Libro rojo de aves de Colombia: Vol 2. Ecosistemas abiertos, secos, insulares, acuáticos, continentales, marinos, tierras altas del Darién y Sierra Nevada de Santa Marta y bosques húmedos del centro, norte y oriente del país. Editorial Pontificia Universidad Javeriana and Instituto Alexander von Humboldt. Bogotá, Colombia

  76. Richardson DS, Westedahl H (2003) MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler. Mol Ecol 12:3523–3529. https://doi.org/10.1046/j.1365-294X.2003.02005.x

    CAS  Article  PubMed  Google Scholar 

  77. Rivera-Gutiérrez HF, Lentijo-Jimenez GM, Chinome-Torres GA, Llano-Mejía J, Martínez-Alvarado D, Gonzalez-Quevedo C, Gomez-Ahumada MF, Parra JL (2018) Aves del Cañón del río Cauca: Guía ilustrada de la avifauna en el área de influencia del proyecto HidroItuango. EPM, Universidad de Antioquia, Medellín

    Google Scholar 

  78. Roach JC, Glusman G, Rowen L et al (2005) The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci USA 102:9577–9582. https://doi.org/10.1073/pnas.0502272102

    CAS  Article  PubMed  Google Scholar 

  79. Ruan W, Wu Y, Zheng SJ (2012) Different genetic patterns in avian Toll-like receptor (TLR)5 genes. Mol Biol Rep 39:3419–3426. https://doi.org/10.1007/s11033-011-1113-7

    CAS  Article  PubMed  Google Scholar 

  80. Sankamethawee W, Hardesty BD, Gale GA (2010) Sex-bias and timing of natal dispersal in cooperatively breeding Puff-throated Bulbuls Alophoixus pallidus. J Ornithol 151:779–789. https://doi.org/10.1007/s10336-010-0511-2

    Article  Google Scholar 

  81. Schröder NW, Schumann RR (2005) Single nucleotide polymorphisms of Toll-like receptors and susceptibility to infectious disease. Lancet Infect Dis 5:156–164. https://doi.org/10.1016/S1473-3099(05)01308-3

    Article  PubMed  Google Scholar 

  82. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234. https://doi.org/10.1038/72708

    CAS  Article  PubMed  Google Scholar 

  83. Şekercioḡlu CH, Ehrlich PR, Daily GC, Aygen D, Goehring D, Sandi RF (2002) Disappearance of insectivorous birds from tropical forest fragments. Proc Natl Acad Sci USA 99:263–267. https://doi.org/10.1073/pnas.012616199

    CAS  Article  PubMed  Google Scholar 

  84. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    CAS  Article  Google Scholar 

  85. Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL (2015) Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol 32:1342–1353

    CAS  Article  Google Scholar 

  86. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Biol Sci 277:979–988. https://doi.org/10.1098/rspb.2009.2084

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169. https://doi.org/10.1086/379378

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. Stratford JA, Stouffer PC (1999) Local extinctions of terrestrial insectivorous birds in a fragmented landscape near Manaus, Brazil. Conserv Biol 13:1416–1423

    Article  Google Scholar 

  89. Swiderska Z, Smidova A, Buchtova L et al (2018) Avian Toll-like receptor allelic diversity far exceeds human polymorphism: an insight from domestic chicken breeds. Sci Rep 8:17878. https://doi.org/10.1038/s41598-018-36226-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  90. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376. https://doi.org/10.1146/annurev.immunol.21.120601.141126

    CAS  Article  PubMed  Google Scholar 

  92. Tarr CL (1995) Primers for amplification and determination of mitochondrial control-region sequences in oscine passerines. Mol Ecol 4:527–529. https://doi.org/10.1111/j.1365-294x.1995.tb00251.x

    CAS  Article  PubMed  Google Scholar 

  93. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  94. Uematsu S, Akira S (2008) Toll-Like receptors (TLRs) and their ligands. Handb Exp Pharmacol. https://doi.org/10.1007/978-3-540-72167-3_1

  95. van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  96. van Oosterhout C, Joyce DA, Cummings SM et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60:2562–2574

    Article  Google Scholar 

  97. Vangestel C, Callens T, Vandomme V, Lens L (2013) Sex-biased dispersal at different geographical scales in a cooperative breeder from fragmented rainforest. PLoS ONE 8:e71624. https://doi.org/10.1371/journal.pone.0071624

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  98. Velová H, Gutowska-Ding MW, Burt DW et al (2018) Toll-like receptor evolution in birds: gene duplication, pseudogenization, and diversifying selection. Mol Biol Evol 35:2170–2184. https://doi.org/10.1093/molbev/msy119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. Villaseñor-Cardoso MI, Ortega E (2011) Polymorphisms of innate immunity receptors in infection by parasites. Parasite Immunol 33:643–653. https://doi.org/10.1111/j.1365-3024.2011.01327.x

    CAS  Article  PubMed  Google Scholar 

  100. Vinkler M, Albrecht T (2009) The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zool 58:15

    Google Scholar 

  101. Vinkler M, Bainova H, Bryjova A et al (2015) Characterisation of Toll-like receptors 4, 5 and 7 and their genetic variation in the grey partridge. Genetica 143:101–112. https://doi.org/10.1007/s10709-015-9819-4

    CAS  Article  PubMed  Google Scholar 

  102. Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. https://doi.org/10.1111/j.1755-0998.2010.02885.x

    Article  PubMed  Google Scholar 

  103. Wang J, Zhang Z, Liu J et al (2016) Ectodomain architecture affects sequence and functional evolution of vertebrate toll-like receptors. Sci Rep. https://doi.org/10.1038/srep26705

    Article  PubMed  PubMed Central  Google Scholar 

  104. Wilson AC, Cann RL, Carr SM et al (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Lin Soc 26:375–400

    Article  Google Scholar 

  105. Wlasiuk G, Nachman MW (2010) Adaptation and constraint at Toll-like receptors in primates. Mol Biol Evol 27:2172–2186. https://doi.org/10.1093/molbev/msq104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. Yáber MC, Rabenold KN (2002) Effects of sociality on short-distance, female‐biased dispersal in tropical wrens. J Anim Ecol 71:1042–1055

    Article  Google Scholar 

  107. Zhou H, Gu J, Lamont SJ, Gu X (2007) Evolutionary analysis for functional divergence of the toll-like receptor gene family and altered functional constraints. J Mol Evol 65:119–123. https://doi.org/10.1007/s00239-005-0008-4

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We thank Empresas Públicas de Medellín for the financial support that allowed the development of the study. Assistance by Y. Acevedo in the genetic analyses were also greatly appreciated. Two anonymous reviewers provided comments that greatly improved the manuscript. We are especially grateful to all the people in the Grupo de Ecología y Evolución de Vertebrados of the Universidad de Antioquia that made this study possible by their valuable data collection: D. Martínez, J. Llano, G. A. Chinome, A. Lopera, S. López.

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All authors contributed to the study conception and design. Material preparation, data collection was done by DZ and analyses were performed by DZ and CG-Q. The first draft of the manuscript was written by DZ and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Catalina Gonzalez-Quevedo.

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Zapata, D., Rivera-Gutierrez, H.F., Parra, J.L. et al. Low adaptive and neutral genetic diversity in the endangered Antioquia wren (Thryophilus sernai). Conserv Genet 21, 1051–1065 (2020). https://doi.org/10.1007/s10592-020-01313-2

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Keywords

  • Thryophilus sernai
  • Genetic drift
  • Genetic variation
  • Mitochondrial control region
  • Toll-like receptors
  • Microsatellites