Immunogenetic heterogeneity in a widespread ungulate: The European roe deer (Capreolus capreolus)

Molecular Ecology

Volumn 24, Issue 15, 2015, Pages 3873-3887

  Quéméré, Erwan ^a   Galan, Maxime ^b   Cosson, Jean François ^b   Klein, François ^c   Aulagnier, Stéphane ^a   Gilot Fromont, Emmanuelle ^d,e   Merlet, Joël ^a   Bonhomme, Maxime ^f   Hewison, A J Mark ^a   Charbonnel, Nathalie ^b  

^a CEMAGREF   (France)

^b CENTRE DE BIOLOGIE ET DE GESTION DES POPULATIONS   (France)

^c CNERA cervidés sanglier   (France)

^d UNIVERSITÉ DE LYON   (France)

^e VETAGRO SUP   (France)

^f UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

genetic drift; immunity; major histocompatibility complex; selection; toll like receptors; wild ungulates

Indexed keywords

CAPREOLUS; CAPREOLUS CAPREOLUS; POSIBACTERIA; UNGULATA;

CYTOKINE; MICROSATELLITE DNA; TOLL LIKE RECEPTOR;

ANIMAL; DEER; DNA SEQUENCE; FRANCE; GENETIC DRIFT; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; IMMUNOLOGY; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; CYTOKINES; DEER; FRANCE; GENETIC DRIFT; GENETIC VARIATION; GENETICS, POPULATION; HAPLOTYPES; IMMUNITY, INNATE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; TOLL-LIKE RECEPTORS;

EID: 84937736078     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13292     Document Type: Article

References (117)

1. Acevedo-Whitehouse K, Cunningham A, (2006) Is MHC enough for understanding wildlife immunogenetics? Trends in Ecology & Evolution, 21, 433-438.
2. Akira S, Takeda K, Kaisho T, (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunology, 2, 675-680.
3. Alcaide M, (2010) On the relative roles of selection and genetic drift in shaping MHC variation. Molecular Ecology, 19, 3842-3844.
4. Andersen R, Duncan P, Linnell JD, (1998) The European roe Deer: The Biology of Success. Scandinavian University Press, Oslo.
5. Apollonio M, Andersen R, Putman R, (2010) European Ungulates and Their Management in the 21st Century. Cambridge University Press, Cambridge.
6. Areal H, Abrantes J, Esteves PJ, (2011) Signatures of positive selection in toll-like receptor (TLR) genes in mammals. BMC Evolutionary Biology, 11, 368.
7. Bandelt HJ, Forster P, Röhle A, (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
8. 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 Genetics, 5, e1000562.
9. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
10. Beaumont MA, Nichols RA, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263, 1619-1626.
11. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, (1996 -2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier (France).
12. Bergman I-M, (2011) Toll-like receptors (TLRs) and mannan-binding lectin (MBL): on constant alert in a hostile environment. Upsala Journal of Medical Sciences, 116, 90-99.
13. Bergman I-M, Edman K, van As P, Huisman A, Juul-Madsen HR, (2014) A two-nucleotide deletion renders the mannose-binding lectin 2 (MBL2) gene nonfunctional in Danish Landrace and Duroc pigs. Immunogenetics, 66, 171-184.
14. Bernatchez L, Landry C, (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology, 16, 363-377.
15. Bhide MR, Mucha R, Mikula I, et al,. (2009) Novel mutations in TLR genes cause hyporesponsiveness to Mycobacterium avium subsp. paratuberculosis infection. BMC Genetics, 10, 21.
16. Bollmer JL, Ruder EA, Johnson JA, Eimes JA, Dunn PO, (2011) Drift and selection influence geographic variation at immune loci of prairie-chickens. Molecular Ecology, 20, 4695-4706.
17. Bonhomme M, Chevalet C, Servin B, et al,. (2010) Detecting selection in population trees: the Lewontin and Krakauer test extended. Genetics, 186, 241-262.
18. Borish LC, Steinke JW, (2003) 2. Cytokines and chemokines. Journal of Allergy and Clinical Immunology, 111, S460-S475.
19. Brown JH, Jardetzky TS, Gorga JC, et al,. (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364, 33.
20. Candela MG, Serrano E, Sevila J, et al,. (2014) Pathogens of zoonotic and biological importance in roe deer (Capreolus capreolus): seroprevalence in an agro-system population in France. Research in Veterinary Science, 96, 254-259.
21. Charbonnel N, Cosson J-F, (2012) Molecular epidemiology of disease resistance genes with perspectives for researches on biological invasions and hybrid zones. In: New Frontiers of Molecular Epidemiology of Infectious Diseases (eds, Morand S, Beaudeau F, Cabaret J,), pp. 255-290. Springer, Heidelberg.
22. Choi K-S, Scorpio DG, Dumler JS, (2004) Anaplasma phagocytophilum ligation to toll-like receptor (TLR) 2, but not to TLR4, activates macrophages for nuclear factor-κB nuclear translocation. Journal of Infectious Diseases, 189, 1921-1925.
23. Cooper MD, Alder MN, (2006) The evolution of adaptive immune systems. Cell, 124, 815-822.
24. Cornuet JM, Luikart G, (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014.
25. Coulon A, Cosson JF, Angibault JM, et al,. (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: An individual-based approach. Molecular Ecology, 13, 2841-2850.
26. Cui J, Cheng Y, Belov K, (2015) Diversity in the toll-like receptor genes of the Tasmanian devil (Sarcophilus harrisii). Immunogenetics, 00, 1-7.
27. Darlay R, McCarthy A, Illot N, Smith J, Shaw MA, (2011) Novel polymorphisms in ovine immune response genes and their association with abortion. Animal Genetics, 42, 535-543.
28. Di Rienzo A, Peterson A, Garza J, et al,. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences, USA, 91, 3166-3170.
29. Ditchkoff SS, Hoofer SR, Lochmiller RL, et al,. (2005) MHC-DRB evolution provides insight into parasite resistance in white-tailed deer. The Southwestern Naturalist, 50, 57-64.
30. Ejsmond MJ, Radwan J, (2011) MHC diversity in bottlenecked populations: A simulation model. Conservation Genetics, 12, 129-137.
31. Excoffier L, Lischer HE, (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
32. Excoffier L, Ray N, (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends in Ecology & Evolution, 23, 347-351.
33. Fernández-de-Mera I, Vicente J, Pérez De La Lastra J, et al,. (2009) Reduced major histocompatibility complex class II polymorphism in a hunter-managed isolated Iberian red deer population. Journal of Zoology, 277, 157-170.
34. Ferrer-Admetlla A, Bosch E, Sikora M, et al,. (2008) Balancing selection is the main force shaping the evolution of innate immunity genes. The Journal of Immunology, 181, 1315-1322.
35. Fisher CA, Bhattarai EK, Osterstock JB, et al,. (2011) Evolution of the bovine TLR gene family and member associations with Mycobacterium avium subspecies paratuberculosis infection. PLoS ONE, 6, e27744.
36. Fornuskova A, Vinkler M, Pages M, et al,. (2013) Contrasted evolutionary histories of two toll-like receptors (Tlr4 and Tlr7) in wild rodents (Murinae). BMC Evolutionary Biology, 13, 194.
37. Fumagalli M, Pozzoli U, Cagliani R, et al,. (2009) Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. The Journal of Experimental Medicine, 206, 1395-1408.
38. Galan M, Cosson J, Aulagnier S, et al,. (2003) Cross-amplification tests of ungulate primers in roe deer (Capreolus capreolus) to develop a multiplex panel of 12 microsatellite loci. Molecular Ecology Notes, 3, 142-146.
39. Galan M, Guivier E, Caraux G, Charbonnel N, Cosson JF, (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics, 11, 296.
40. Galan M, Pagès M, Cosson J-F, (2012) Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS ONE, 7, e48374.
41. Garantziotis S, Hollingsworth JW, Zaas AK, Schwartz DA, (2008) The effect of toll-like receptors and toll-like receptor genetics in human disease. Annual Review of Medicine, 59, 343-359.
42. Garred P, (2008) Mannose-binding lectin genetics: from A to Z. Biochemical Society Transactions, 36, 1461.
43. Garrigan D, Hedrick PW, (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution, 57, 1707-1722.
44. Garza J, Williamson E, (2001) Detection of reduction in population size using data from microsatellite loci. Molecular Ecology, 10, 305-318.
45. Gazzinelli RT, Denkers EY, (2006) Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nature Reviews Immunology, 6, 895-906.
46. Georgel P, Macquin C, Bahram S, (2009) The heterogeneous allelic repertoire of human toll-like receptor (TLR) genes. PLoS ONE, 4, e7803.
47. Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J, (2007) Diseases shared between wildlife and livestock: A European perspective. European Journal of Wildlife Research, 53, 241-256.
48. 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.
49. 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. Molecular Ecology, 22, 4470-4482.
50. 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.
51. Haldane JBS, (1949) Disease and evolution. La Ricercia Scientificica, Supplemento, 19, 1-11.
52. Hedrick PW, (2012) What is the evidence for heterozygote advantage selection? Trends in Ecology & Evolution, 27, 698-704.
53. Hewison AJM, Angibault JM, Cargnelutti B, et al,. (2007) Using radio-tracking and direct observation to estimate roe deer Capreolus capreolus density in a fragmented landscape: A pilot study. Wildlife Biology, 13, 313-320.
54. Hewison A, Morellet N, Verheyden H, et al,. (2009) Landscape fragmentation influences winter body mass of roe deer. Ecography, 32, 1062-1070.
55. Hollegaard M, Bidwell J, (2006) Cytokine gene polymorphism in human disease: on-line databases, Supplement 3. Genes and Immunity, 7, 269-276.
56. Iwasaki A, Medzhitov R, (2010) Regulation of adaptive immunity by the innate immune system. Science, 327, 291-295.
57. Juul-Madsen HR, Kjærup RM, Toft C, et al,. (2011) Structural gene variants in the porcine mannose-binding lectin 1 (MBL1) gene are associated with low serum MBL-A concentrations. Immunogenetics, 63, 309-317.
58. Kaluzinski J, (1982) Dynamics and structure of a field roe deer population. Acta Theriologica, 27, 449-455.
59. Kawai T, Akira S, (2006) TLR signaling. Cell Death & Differentiation, 13, 816-825.
60. Lee KA, Klasing KC, (2004) A role for immunology in invasion biology. Trends in Ecology & Evolution, 19, 523-529.
61. Lewontin R, Krakauer J, (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics, 74, 175-195.
62. Librado P, Rozas J, (2009) dnasp v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
63. Lillie BN, Keirstead ND, James Squires E, Anthony Hayes M, (2007) Gene polymorphisms associated with reduced hepatic expression of porcine mannan-binding lectin C. Developmental & Comparative Immunology, 31, 830-846.
64. Lotterhos KE, Whitlock MC, (2014) Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Molecular Ecology, 23, 2178-2192.
65. McKinney ML, (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation, 127, 247-260.
66. Mikko S, Røed K, Schmutz S, Andersson L, (1999) Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants. Immunological Reviews, 167, 169-178.
67. Miller HC, Allendorf F, Daugherty CH, (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Molecular Ecology, 19, 3894-3908.
68. Mona S, Crestanello B, Bankhead-Dronnet S, et al,. (2008) Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Molecular Ecology, 17, 4053-4067.
69. Mucha R, Bhide M, Chakurkar E, Novak M, Mikula I Sr, (2009) Toll-like receptors TLR1, TLR2 and TLR4 gene mutations and natural resistance to Mycobacterium avium subsp. paratuberculosis infection in cattle. Veterinary Immunology and Immunopathology, 128, 381-388.
70. 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. Proceedings of the National Academy of Sciences, USA, 106, 7073-7078.
71. Muñoz PM, Boadella M, Arnal M, et al,. (2010) Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates. BMC Infectious Diseases, 10, 46.
72. Nei M, (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583-590.
73. Nei M, (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
74. Nielsen R, Yang Z, (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics, 148, 929-936.
75. Offord V, Coffey T, Werling D, (2010) lrrfinder: A web application for the identification of leucine-rich repeats and an integrative Toll-like receptor database. Developmental & Comparative Immunology, 34, 1035-1041.
76. Oliver MK, Piertney SB, (2012) Selection maintains MHC diversity through a natural population bottleneck. Molecular Biology and Evolution, 29, 1713-1720.
77. Parham P, (2003) Innate immunity: the unsung heroes. Nature, 423, 20.
78. Parmesan C, Yohe G, (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
79. Piertney S, Oliver M, (2005) The evolutionary ecology of the major histocompatibility complex. Heredity, 96, 7-21.
80. Pinedo PJ, Buergelt CD, Donovan G, et al,. (2009) Candidate gene polymorphisms (BoIFNG, TLR4, SLC11A1) as risk factors for paratuberculosis infection in cattle. Preventive Veterinary Medicine, 91, 189-196.
81. Pioz M, Loison A, Gauthier D, et al,. (2008) Diseases and reproductive success in a wild mammal: example in the alpine chamois. Oecologia, 155, 691-704.
82. Piry S, Luikart G, Cornuet J-M, (1999) BOTTLENECK: A program for detecting recent effective population size reductions from allele data frequencies. The Journal of Heredity, 90, 502-503.
83. Piry S, Guivier E, Realini A, Martin J, (2012) SESAME Barcode: NGS-oriented software for amplicon characterization-application to species and environmental barcoding. Molecular Ecology Resources, 12, 1151-1157.
84. R Development Core Team (2015) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
85. Richman AD, Herrera LG, Nash D, Schierup MH, (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genetical Research, 82, 89-99.
86. Roach JC, Glusman G, Rowen L, et al,. (2005) The evolution of vertebrate Toll-like receptors. Proceedings of the National Academy of Sciences, USA, 102, 9577-9582.
87. Satta Y, (1997) Effects of intra-locus recombination on HLA polymorphism. Hereditas, 127, 105-112.
88. Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman S, (2006) Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity, 97, 427-437.
89. Schou TW, Permin A, Christensen JP, Cu H, Juul-Madsen HR, (2010) Mannan-binding lectin (MBL) in two chicken breeds and the correlation with experimental Pasteurella multocida infection. Comparative Immunology, Microbiology and Infectious Diseases, 33, 183-195.
90. Seabury CM, Seabury PM, Decker JE, et al,. (2010) Diversity and evolution of 11 innate immune genes in Bos taurus taurus and Bos taurus indicus cattle. Proceedings of the National Academy of Sciences, USA, 107, 151-156.
91. Sellis D, Callahan BJ, Petrov DA, Messer PW, (2011) Heterozygote advantage as a natural consequence of adaptation in diploids. Proceedings of the National Academy of Sciences, USA, 108, 20666-20671.
92. Sigurdardottir S, Borsch C, Gustafsson K, Andersson L, (1991) Cloning and sequence analysis of 14 DRB alleles of the bovine major histocompatibility complex by using the polymerase chain reaction. Animal Genetics, 22, 199-209.
93. Sironi M, Cagliani R, Forni D, Clerici M, (2015) Evolutionary insights into host-pathogen interactions from mammalian sequence data. Nature Reviews Genetics, 16, 224-236.
94. Slatkin M, Excoffier L, (2012) Serial founder effects during range expansion: A spatial analog of genetic drift. Genetics, 191, 171-181.
95. Smith SA, Jann OC, Haig D, et al,. (2012) Adaptive evolution of Toll-like receptor 5 in domesticated mammals. BMC Evolutionary Biology, 12, 122.
96. Smith S, Haig D, Emes R, (2014) Novel ovine polymorphisms and adaptive evolution in mammalian TLR2 suggest existence of multiple pathogen binding regions. Gene, 540, 217-225.
97. Sommer S, (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology, 2, 16.
98. Strand TM, Segelbacher G, Quintela M, et al,. (2012) Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse? Ecology and Evolution, 2, 341-353.
99. Sutton JT, Nakagawa S, Robertson BC, Jamieson IG, (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Molecular Ecology, 20, 4408-4420.
100. Takahata N, Nei M, (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124, 967-978.
101. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, (2013) mega 6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
102. Tschirren B, Råberg L, Westerdahl H, (2011) Signatures of selection acting on the innate immunity gene Toll-like receptor 2 (TLR2) during the evolutionary history of rodents. Journal of Evolutionary Biology, 24, 1232-1240.
103. Turner AK, Begon M, Jackson JA, Bradley JE, Paterson S, (2011) Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLoS Genetics, 7, e1002343.
104. Van Den Bussche RA, Hoofer SR, Lochmiller RL, (1999) Characterization of Mhc-DRB allelic diversity in white-tailed deer (Odocoileus virginianus) provides insight into Mhc-DRB allelic evolution within Cervidae. Immunogenetics, 49, 429-437.
105. Vinkler M, Albrecht T, (2009) The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zoologica, 58, 15-28.
106. Werling D, Piercy J, Coffey TJ, (2006) Expression of toll-like receptors (TLR) by bovine antigen-presenting cells-potential role in pathogen discrimination? Veterinary Immunology and Immunopathology, 112, 2-11.
107. Werling D, Jann OC, Offord V, Glass EJ, Coffey TJ, (2009) Variation matters: TLR structure and species-specific pathogen recognition. Trends in Immunology, 30, 124-130.
108. White TA, Perkins SE, (2012) The ecoimmunology of invasive species. Functional Ecology, 26, 1313-1323.
109. Wilfert L, Schmid-Hempel P, (2008) The genetic architecture of susceptibility to parasites. BMC Evolutionary Biology, 8, 187.
110. Wlasiuk G, Nachman MW, (2010) Adaptation and constraint at toll-like receptors in primates. Molecular Biology and Evolution, 27, 2172-2186.
111. Wright S, (1978) Evolution and the Genetics of Populations vol. 4. Variability Within and Among Natural Populations, University of Chicago Press, Chicago, Illinois.
112. Yamazaki K, Boyse E, Mike V, et al,. (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. The Journal of Experimental Medicine, 144, 1324-1335.
113. Yang Z, (2007) paml 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586-1591.
114. Yang Z, Bielawski JP, (2000) Statistical methods for detecting molecular adaptation. Trends in Ecology & Evolution, 15, 496-503.
115. Yang X, Joyee A, (2008) Role of toll-like receptors in immune responses to chlamydial infections. Current Pharmaceutical Design, 14, 593-600.
116. Yarovinsky F, (2014) Innate immunity to Toxoplasma gondii infection. Nature Reviews Immunology, 14, 109-121.
117. Zhao F, Zhao Z, Yan G, et al,. (2011) Polymorphisms in mannose-binding lectin (MBL) gene and their association with MBL protein levels in serum in the Hu sheep. Veterinary Immunology and Immunopathology, 140, 297-302.