Published February 12, 2024 | Version v1

Diversity of MHC class II DRB alleles in the Northern chamois genus Rupicapra

Description

Stipoljev, Sunčica, Buzan, Elena, Iacolina, Laura, Safner, Toni, Rezić, Andrea, Galov, Ana, Križanović, Krešimir, Ambarlı, Hüseyin, Arnal, MariaCruz, Babaev, Elmar, Bego, Ferdinand, Farkas, Attila, Gačić, Dragan, Lazar, Peter, Maletić, Vladimir, Markov, Georgi, Milošević, Dragana, Papaioannou, Haritakis, Scandura, Massimo, Šprem, Nikica (2024): Diversity of MHC class II DRB alleles in the Northern chamois genus Rupicapra. Journal of Mammalogy 105 (2): 312-322, DOI: 10.1093/jmammal/gyae008, URL: https://doi.org/10.1093/jmammal/gyae008

Files

Restricted

The record is publicly accessible, but files are restricted. Log in to check if you have access.

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:FFC5FFCCFF971752FFBBC765F14A831C

References

  • Acevedo-Whitehouse K, Cunningham AA. 2006. Is MHC enough for understanding wildlife immunogenetics? Trends in Ecology and Evolution 21(8):433-438. https://doi.org/10.1016/j. tree.2006.05.010
  • Alcaide M. 2010. On the relative roles of selection and genetic drift in shaping MHC variation. Molecular Ecology 19(18):3842-3844. https://doi.org/10.1111/j.1365-294X.2010.04772.x
  • Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, et al. 2003. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34(1):517-547. https://doi. org/10.1146/annurev.ecolsys.34.030102.151725
  • Alvarez-Busto J, Garcia-Etxebarria K, Herrero J, Garin I, Jugo BM. 2007. Diversity and evolution of the Mhc-DRB1 gene in the two endemic Iberian subspecies of Pyrenean Chamois, Rupicapra pyrenaica. Heredity 99(4):406-413. https://doi.org/10.1038/ sj.hdy.6801016
  • Amos W, Balmford A. 2001. When does conservation genetics matter? Heredity 87(Pt 3):257-265. https://doi. org/10.1046/j.1365-2540.2001.00940.x
  • Anderwald P, Ambarli H, Avramov S, Ciach, M, Corlatti L, Farkas A, Jovanovic M, Papaioannou H, Peters W, Sarasa M, et al. 2021. Rupicapra rupicapra (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021: e.T39255A195863093 [accessed 11 Mar 2022]. www.iucnredlist. org/species/39255/195863093.
  • Awadi A, Ben Slimen H, Smith S, Knauer F, Makni M, Suchentrunk F. 2018. Positive selection and climatic effects on MHC class II gene diversity in hares (Lepus capensis) from a steep ecological gradient. Scientific Reports 8(1):11514. https://doi.org/10.1038/ s41598-018-29657-3
  • Bekessy SA, Ennos RA, Burgman MA, Newton AC, Ades PK. 2003. Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biological Conservation 110(2):267- 275. https://doi.org/10.1016/s0006-3207(02)00225-2
  • 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(3):363-377. https://doi. org/10.1046/j.1420-9101.2003.00531.x
  • Biedrzycka A, Konopinski M, Hoffman E, Trujillo A, Zalewski A. 2020. Comparing raccoon major histocompatibility complex diversity in native and introduced ranges: evidence for the importance of functional immune diversity for adaptation and survival in novel environments. Evolutionary Applications 13(4):752-767. https://doi.org/10.1111/eva.12898
  • Brown JH. 2001. Mammals on mountainsides: elevational patterns of diversity. Global Ecology and Biogeography 10(1):101-109. https://doi.org/10.1046/j.1466-822x.2001.00228.x
  • Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. 1993.Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364(6432):33-39. https://doi.org/10.1038/364033a0
  • Buzan E, Potusek S, Urzi F, Pokorny B, Sprem N. 2020. Genetic characterisation of wild ungulates: successful isolation and analysis of DNA from widely available bones can be cheap, fast and easy. Zookeys 965:141-156. https://doi.org/10.3897/ zookeys.965.54862
  • Buzan EV, Bryja J, Zemanova B, Krystufek B. 2013. Population genetics of chamois in the contact zone between the Alps and the Dinaric Mountains: uncovering the role of habitat fragmentation and past management. Conservation Genetics 14(2):401- 412. https://doi.org/10.1007/s10592-013-0469-8
  • Cavallero S, Marco I, Lavin S, D'Amelio S, Lopez-Olvera JR. 2012. Polymorphisms at MHC class II DRB1 exon 2 locus in Pyrenean chamois (Rupicapra pyrenaica pyrenaica). Infection, Genetics and Evolution 12(5):1020-1026. https://doi.org/10.1016/j. meegid.2012.02.017
  • Corlatti L, Lacolina L, Safner T, Apollonio M, Buzan E, Ferretti F, Hammer SE, Herrero J, Rossi L, Serrano E, et al. 2022. Past, present and future of chamois science. Wildlife Biology: e01025. https://doi.org/10.1002/wlb3.01025
  • Corlatti L., Herrero J., Ferretti F., Anderwald P., Garcia-Gonzalez R., Hammer S., Nores C., Rossi L., Lovari S. 2021. Northern Chamois, Rupicapra rupicapra (Linnaeus, 1758) and Southern Chamois, Rupicapra pyrenaica Bonaparte, 1845. In: Corlatti L, Zachos F, editors. Handbook of the mammals of Europe - terrestrial Cetartiodactyla. Switzerland: Springer Nature; p. 1-42. https:// doi.org/10.1007/978-3-030-24475-0_30
  • Corlatti L, Lorenzini R, Lovari S. 2011. The conservation of the chamois Rupicapra spp. Mammal Review 41(2):163-174. https://doi. org/10.1111/j.1365-2907.2011.00187.x
  • Crestanello B, Pecchioli E, Vernesi C, Mona S, Martinkova N, Janiga M, Hauffe HC, Bertorelle G. 2009. The genetic impact of translocations and habitat fragmentation in chamois (Rupicapra) spp. Journal of Heredity 100(6):691-708. https://doi.org/10.1093/ jhered/esp053
  • Doytchinova IA, Flower DR.2005.In silico identification of supertypes for class II MHCs. The Journal of Immunology 174(11):7085- 7095. https://doi.org/10.4049/jimmunol.174.11.7085
  • Ejsmond MJ, Radwan J. 2015. Red queen processes drive positive selection on major histocompatibility complex (MHC) genes. PLoS Computational Biology 11(11):e1004627. https://doi. org/10.1371/journal.pcbi.1004627
  • Excoffier L, Lischer H. 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. https:// doi.org/10.1111/j.1755-0998.2010.02847.x
  • Ezard THG, Travis JMJ. 2006.The impact of habitat loss and fragmentation on genetic drift and fixation time. Oikos 114(2):367-375. https://doi.org/10.1111/j.2006.0030-1299.14778.x
  • Fuchs K, Deutz A, Gressmann G. 2000. Detection of space-time clusters and epidemiological examinations of scabies in chamois. Veterinary Parasitology 92(1):63-73. https://doi.org/10.1016/ s0304-4017(00)00269-7
  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW. 2012. Harnessing genomics for delineating conservation units.Trends in Ecology and Evolution 27(9):489-496. https://doi.org/10.1016/j.tree.2012.05.012
  • Fuselli S, Baptista RP, Panziera A, Magi A, Guglielmi S, Tonin R, Benazzo A, Bauzer LG, Mazzoni CJ, Bertorelle G. 2018. A new hybrid approach for MHC genotyping: high-throughput NGS and long read MinION nanopore sequencing, with application to the non-model vertebrate Alpine chamois (Rupicapra rupicapra). Heredity 121(4):293-303. https://doi.org/10.1038/ s41437-018-0070-5
  • Gao F, Chen C, Arab DA, Du Z, He Y, Ho SYW. 2019. EasyCodeML: a visual tool for analysis of selection using CodeML. Ecology and Evolution 9(7):3891-3898. https://doi.org/10.1002/ece3.5015
  • Garrigan D, Hedrick PW. 2003. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57(8):1707-1722. https://doi.org/10.1111/j.0014-3820.2003. tb00580.x
  • Hassanin A, Ropiquet A, Couloux A, et al. 2009. Evolution of the mitochondrial genome in mammals living at high altitude: new insights from a study of the tribe caprini (Bovidae, Antilopinae). Journal of Molecular Evolution 68:293-310. https://doi.org/10.1007/ s00239-009-9208-7
  • Hedrick PW. 2001. Conservation genetics: where are we now? Trends in Ecology and Evolution 16(11):629-636. https://doi. org/10.1016/s0169-5347(01)02282-0
  • Herrero J., Lovari, S., Nores C., Toigo C. 2020. Rupicapra pyrenaica. The IUCN Red List of Threatened Species 2020: e.T19771A171131310 [accessed 11 Mar 2022]. www.iucnredlist. org/species/19771/171131310.
  • Hoffmann AA, Sorensen JG, Loeschcke V. 2003. Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28(3):175-216. https://doi.org/10.1016/s0306-4565(02)00057-8
  • Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23(2):254-267. https://doi.org/10.1093/molbev/msj030
  • Iacolina L, Corlatti L, Buzan E, Safner T, Sprem N. 2019. Hybridisation in European ungulates: an overview of the current status, causes, and consequences. Mammal Review 49:45-59. https:// doi.org/10.1111/mam.12140
  • Jombart T. 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11):1403-1405. https:// doi.org/10.1093/bioinformatics/btn129
  • Jombart T, Devillard S, Balloux F. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11(94). https://doi. org/10.1186/1471-2156-11-94
  • Juola FA, Dearborn DC. 2011. Sequence-based evidence for major histocompatibility complex-disassortative mating in a colonial seabird. Proceedings of the Royal Society of London, B: Biological Sciences 279(1726):153-162. https://doi.org/10.1098/ rspb.2011.0562
  • Kalinowski ST. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5(4):539-543. https://doi. org/10.1023/b:coge.0000041021.91777.1a
  • Klein J. 1986. Natural history of the major histocompatibility complex. New York (NY, USA): John Wiley and Sons.
  • Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI. 1990. Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31(4):217-219. https://doi.org/10.1007/BF00204890
  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6):1547-1549. https://doi. org/10.1093/molbev/msy096
  • Leugger F, Broquet T, Karger DN, Rioux D, Buzan E, Corlatti L, Crestanello B, Curt-Grand-Gaudin N, Hauffe HC, RoleCkova B, et al. 2022. Dispersal and habitat dynamics shape the genetic structure of the Northern Chamois in the Alps. Journal of Biogeography 49(10):1848-1861. https://doi.org/10.1111/ jbi.14363
  • Lovari S, Franceschi S, Chiatante G, Fattorini L, Fattorini N, Ferretti F. 2020. Climatic changes and the fate of mountain herbivores. Climatic Change 162(4):2319-2337. https://doi.org/10.1007/ s10584-020-02801-7
  • Markov G, Zhelev P, Ben Slimen H, Suchentrunk F. 2016. Population genetic data pertinent to the conservation of Bulgarian chamois (Rupicapra rupicapra balcanica). Conservation Genetics 17:155- 164. https://doi.org/10.1007/s10592-015-0768-3
  • Miller HC, Lambert DM. 2004. Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56(3):178-191. https://doi.org/10.1007/ s00251-004-0666-1
  • Mona S, Crestanello B, Bankhead-Dronnet S, Pecchioli E, Ingrosso S, D'Amelio S, Rossi L, Meneguz PG, Bertorelle G. 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(18):4053-4067. https://doi. org/10.1111/j.1365-294x.2008.03892.x
  • Nielsen R. 2005. Molecular signatures of natural selection. Annual Review of Genetics 39:197-218. https://doi.org/10.1146/annurev. genet.39.073003.112420
  • O'Brien SJ, Evermann JF. 1988. Interactive influence of infectious disease and genetic diversity in natural populations. Trends in Ecology and Evolution 3(10):254-259. https://doi. org/10.1016/0169-5347(88)90058-4
  • Oosterhout C, Joyce DA, Cummings SM, Blais J, Barson NJ, Ramnarine IW, Mohammed RS, Persad N, Cable J. 2006. Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60(12):2562-2574. https://doi. org/10.1111/j.0014-3820.2006.tb01890.x
  • Papaioannou H, Fernandez M, Perez T, Dominguez A. 2019. Genetic variability and population structure of chamois in Greece (Rupicapra rupicapra balcanica). Conservation Genetics 20(4):939- 945. https://doi.org/10.1007/s10592-019-01177-1
  • Perez T, Albornoz J, Dominguez A. 2002. Phylogeography of chamois (Rupicapra spp.) inferred from microsatellites. Molecular Phylogenetics and Evolution 25(3):524-534. https://doi. org/10.1016/s1055-7903(02)00296-8
  • Perez T, Fernandez M, Hammer SE, Dominguez A. 2017. Multilocus intron trees reveal extensive male-biased homogenization of ancient populations of chamois (Rupicapra spp.) across Europe during Late Pleistocene. PLoS One 12(2):e0170392. https://doi. org/10.1371/journal.pone.0170392
  • Perez T, Fernandez M, Palacios B, Dominguez A. 2022. Phylogenetic analysis of the complete mitochondrial genomes in the ten Rupicapra subspecies and implications for the existence of multiple glacial refugia in Europe. Animals 12(11):1430. https://doi. org/10.3390/ani12111430
  • Petit RJ,Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S,Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, et al. 2003. Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300(5625):1563-1565. https://doi.org/10.1126/ science.1083264
  • Piertney SB, Oliver MK. 2006. The evolutionary ecology of the major histocompatibility complex. Heredity 96(1):7-21. https://doi. org/10.1038/sj.hdy.6800724
  • Punt J., Stranford S.A., Jones P.P., Owen J.A. 2019. Kuby Immunology. 8th ed. New York (NY, USA): W. H. Freeman and Company.
  • R Development Core Team. 2020. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. www.R-project.org/.
  • Radwan J, Biedrzycka A, Babik W. 2010. Does reduced MHC diversity decrease viability of vertebrate populations? Biological Conservation 143(3):537-544. https://doi.org/10.1016/j. biocon.2009.07.026
  • ReziC A, Iacolina L, Buzan E, Safner T, Bego F, GaCiC D, MaletiC V, Markov G, MiloseviC D, Papaioannou H, et al. 2022a. The Balkan chamois, an archipelago or a peninsula? Insights from nuclear and mitochondrial DNA. Conservation Genetics 23(3):527-539. https://doi.org/10.1007/s10592-022-01434-w
  • ReziC A, Safner T, Iacolina L, Buzan E, Sprem N. 2022b. Traces of past reintroduction in genetic diversity: the case of the Balkan chamois (Mammalia, Artiodactyla). Zookeys 1116:57-70. https://doi. org/10.3897/zookeys.1116.84577
  • Rodriguez F,Hammer S,Perez T, Suchentrunk F,Lorenzini R,Michallet J, Martinkova N, Albornoz J, Dominguez A. 2009. Cytochrome b phylogeography of chamois (Rupicapra spp.). Population contractions, expansions and hybridizations governed the diversification of the genus. Journal of Heredity 100(1):47-55. https:// doi.org/10.1093/jhered/esn074
  • Rodriguez F, Perez T, Hammer SE, Albornoz J, Dominguez A. 2010. Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois (genus Rupicapra). BMC Evolutionary Biology 10(222). https://doi. org/10.1186/1471-2148-10-222
  • Rossi L, Meneguz PG, Martin PD, Rodolfi M. 1995. The epizootiology of sarcoptic mange in chamois, Rupicapra rupicapra, from the Italian eastern Alps. Parassitologia 37(2-3):233-240. PMID: 8778664.
  • Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sanchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34(12):3299-3302. https://doi.org/10.1093/ molbev/msx248
  • Schaschl H, Goodman SJ, Suchentrunk F. 2004. Sequence analysis of the MHC class II DRB alleles in Alpine chamois (Rupicapra r. rupicapra). Developmental and Comparative Immunology 28(3):265- 277. https://doi.org/10.1016/j.dci.2003.08.003
  • Schaschl H, Suchentrunk F, Hammer S, Goodman SJ. 2005. Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.). Immunogenetics 57(1-2):108-115. https://doi.org/10.1007/s00251-005-0784-4
  • Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman SJ. 2006. Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity 97(6):427-437. https://doi.org/10.1038/sj.hdy.6800892
  • Sebastian A, Herdegen M, Migalska M, Radwan J. 2016. AMPLISAS: a web server for multilocus genotyping using next-generation amplicon sequencing data. Molecular Ecology Resources 16(2):498-510. https://doi.org/10.1111/1755-0998.12453
  • Shackleton D. 1997. Wild sheep and goats and their relatives. Gland (Switzerland): International Union for Conservation of Nature.
  • Soglia D, Rossi L, Cauvin E, Citterio C, Ferroglio E, Maione S, Meneguz PG, Spalenza V, Rasero R, Sacchi P. 2010. Population genetic structure of Alpine chamois (Rupicapra r. rupicapra) in the Italian Alps. European Journal of Wildlife Research 56(6):845-854. https://doi.org/10.1007/s10344-010-0382-0
  • Sommer S. 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology 2(1):1-18. https://doi.org/10.1186/1742-9994-2-16
  • Spielman D, Brook BW, Frankham R. 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101(42):15261-15264. https://doi.org/10.1073/ pnas.0403809101
  • Sprem N, Buzan E. 2016.The genetic impact of chamois management in the dinarides. Journal of Wildlife Management 80(5):783-793. https://doi.org/10.1002/jwmg.21081
  • Spurgin LG, Richardson DS. 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society of London, B: Biological Sciences 277(1684):979-988. https://doi.org/10.1098/rspb.2009.2084
  • StefanCikova A, Chovancova B, Hajek B, Dudinak V, Snabel V. 2011. Revision of chamois infection by lung nematodes under ecological conditions of national parks of Slovakia with respect to ongoing global climate changes. Helminthologia 48(3):145-154. https://doi.org/10.2478/s11687-011-0022-6
  • Stipoljev S, Buzan E, RoleCkova B, Iacolina L, Sprem N. 2020.MHC genotyping by SSCP and amplicon-based NGS approach in chamois. Animals 10(9):1694. https://doi.org/10.3390/ani10091694
  • Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585-595. https://doi.org/10.1093/genetics/123.3.585
  • Tesicky M, Vinkler M. 2015. Trans-species polymorphism in immune genes: general pattern or MHC-restricted phenomenon? Journal of Immunology Research 2015:838035. https://doi. org/10.1155/2015/838035
  • Weaver S, Shank SD, Spielman SJ,Li M, Muse SV, Kosakovsky Pond SL. 2018. Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Molecular Biology and Evolution 35(3):773-777. https://doi.org/10.1093/ molbev/msx335
  • Willi Y, Van Buskirk J, Schmid B, Fischer M. 2007. Genetic isolation of fragmented populations is exacerbated by drift and selection. Journal of Evolutionary Biology 20(2):534-542. https://doi. org/10.1111/j.1420-9101.2006.01263.x
  • Yang Z, Swanson WJ. 2002. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Molecular Biology and Evolution 19(1):49-57. https://doi.org/10.1093/oxfordjournals.molbev. a003981
  • Zagalska-Neubauer M, Babik W, Stuglik M, Gustafsson L, Cichon M, Radwan J. 2010. 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the Collared Flycatcher. BMC Evolutionary Biology 10(395). https://doi. org/10.1186/1471-2148-10-395