Abstract
Increased global temperature and associated changes to Arctic habitats will likely result in the northward advance of species, including an influx of pathogens novel to the Arctic. How species respond to these immunological challenges will depend in part on the adaptive potential of their immune response system. We compared levels of genetic diversity at a gene associated with adaptive immune response [Class II major histocompatibility complex (MHC), DQB exon 2] between populations of walrus (Odobenus rosmarus), a sea ice-dependent Arctic species. Walrus was represented by only five MHC DQB alleles, with frequency differences observed between Pacific and Atlantic populations. MHC DQB alleles appear to be under balancing selection, and most (80 %; n = 4/5) of the alleles were observed in walruses from both oceans, suggesting broad scale differences in the frequency of exposure and diversity of pathogens may be influencing levels of heterozygosity at DQB in walruses. Limited genetic diversity at MHC, however, suggests that walrus may have a reduced capacity to respond to novel immunological challenges associated with shifts in ecological communities and environmental stressors predicted for changing climates. This is particularly pertinent for walrus, since reductions in summer sea ice may facilitate both northward expansion of marine species and associated pathogens from more temperate regions, and exchange of marine mammals and associated pathogens through the recently opened Northwest Passage between the Atlantic and Pacific Oceans in the Canadian high Arctic.
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References
Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol 21:433–438
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723
Allen PJ, Amos W, Pomeroy PP, Twiss SD (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol Ecol 4:653–662
Bandelt HJ, Forster P, Sykes BC, Richards MB (1995) Mitochondrial portraits of human populations. Genetics 141:743–753
Born EW (2005) An assessment of the effects of hunting and climate on walruses in Greenland. Doctorate of philosophy dissertation, NMH, University of Oslo, Oslo
Born EW, Andersen LW, Gjertz I, Wiig Ø (2001) A review of the genetic relationships of Atlantic walrus (Odobenus rosmarus rosmarus) east and west Greenland. Polar Biol 24:713–718
Buchanan FC, Maiers LD, Thue TD, De March BGE, Stewart REA (1998) Microsatellites from the Atlantic walrus Odobenus rosmarus rosmarus. Mol Ecol 7:1083–1090
Cammen K, Hoffman JI, Knapp LA, Harwood J, Amos W (2011) Geographic variation of the major histocompatibility complex in eastern Atlantic grey seals (Halichoerus grypus). Mol Ecol 20:740–752
Chapskii KK (1940) Distribution of the walrus in the Laptev and East Siberian seas. Probl Sev 6:80–94
Cronin MA, Hills S, Born EW, Patton JC (1994) Mitochondrial DNA variation in Atlantic and Pacific walruses. Can J Zool 72:1035–1043
Cronin MA, Amstrup SC, Talbot SL, Sage GK, Amstrup KS (2009) Genetic variation, relatedness, and effective population size of polar bears (Ursus maritimus) in the southern Beaufort Sea, Alaska. J Hered 100:681–690
Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52
Edwards SV, Potts WK (1996) Polymorphism of MHC genes: implications for conservation genetics of vertebrates. In: Smith TB, Wayne RK (eds) Molecular genetic approaches to conservation. Oxford University Press, Oxford, pp 214–237
Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens Illiger, vol 74. U.S. Department of the Interior, Fish and Wildlife Service, Washington, DC
Fay FH (1985) Odobenus rosmarus. Mammalian species No. 238. The American Society of Mammalogists
Fay FH, Eberhardt LL, Kelly BP, Burns JJ, Quakenbush LT (1997) Status of the Pacific walrus population, 1950–1989. Mar Mamm Sci 13:537–565
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gangoso L, Alcaide M, Grande JM, Muñoz J, Talbot SL, Sonsthagen SA, Sage GK, Figuerola J (2012) Colonizing the world in spite of reduced MHC variation. J Evol Biol 25:1438–1447
Goodman SJ (1997) Dinucleotide repeat polymorphisms at seven anonymous microsatellite loci cloned from the European harbor seal (Phoca vitulina vitulina). Anim Genet 28:310–311
Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Hasegawa M, Kishino K, Yano T (1985) Dating the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Heide-Jørgensen M, Laidre KL, Quakenbush LT, Citta J (2012) The Northwest Passage opens for bowhead whales. Biol Lett 8:270–273
Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. J Biogeogr 35:1533–1550
Hoelzel AR, Stephens JC, O’Brien SJ (1999) Molecular genetic diversity and evolution at the MHC DQB locus in four species of pinnipeds. Mol Biol Evol 16:611–618
Hueffer K, O’Hara T, Follmann EH (2011) Adaptation of mammalian host-pathogen interactions in a changing Arctic environment. Acta Vet Scand 53:17
Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170
Jay CV, Marcot BG, Douglas DC (2011) Projected status of the Pacific walrus (Odobenus rosmarus divergens) in the twenty-first century. Polar Biol 34:1065–1084
Jay CV, Fischbach AS, Kochnev AA (2012) Walrus areas of use in the Chukchi Sea during sparse sea ice cover. Mar Ecol Prog Ser 468:1–13
Jenkins EJ, Veitch AM, Kutz SJ, Hoberg EP, Polley L (2006) Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall’s sheep (Ovis dalli dalli). Parasitology 132:387–401
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HM (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
Kirkpatrick BW (1992) Identification of a conserved microsatellite site in porcine and bovine insulin-like growth factor-1 gene 5′ flank. Anim Genet 23:543–548
Kovacs KM, Lydersen C, Overland JE, Moore SE (2011) Impacts of changing sea-ice conditions on Arctic marine mammals. Mar Biodivers 41:181–194
Kutz SJ, Hoberg EP, Polley L, Jenkins EJ (2005) Global warming is changing the dynamics of Arctic host–parasite systems. Proc R Soc Lond B 272:2571–2576
Laidre KL, Stirling I, Lowry LF, Wiig Ø, Heide-Jorgensen MP, Ferguson SH (2008) Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat change. Ecol Appl 18:S97–S125
Lento GM, Baker CS, David V, Yuhki N, Gales NJ, O’Brien SJ (2003) Automated single-strand conformation polymorphism reveals low diversity of a major histocompatibility complex Class II gene in the threatened New Zealand sea lion. Mol Ecol Notes 3:346–349
Lenz T, Wells K, Pfeiffer M, Sommer S (2009) Diverse MHC IIB allele repertoire increases parasite resistance and body condition in the long-tailed giant rat (Leopoldamys sabanus). BMC Evol Biol 9:269
Lindqvist C, Bachmann L, Andersen LW, Born EW, Arnason U, Kovacs KM, Lydersen C, Abramov AV, Wiig Ø (2009) The Laptev Sea walrus Odobenus rosmarus laptevi: an enigma revisited. Zool Scr 38:113–127
MacCracken JG (2012) Pacific walrus and climate change: observations and predictions. Ecol Evol 2:2072–2090
Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol Ecol 14:2233–2243
Moore GWK (2006) Reduction in seasonal sea ice concentration surrounding southern Baffin Island 1979–2004. Geophys Res Lett 33:L20501
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Overland JE, Wang M (2013) When will the summer Arctic be nearly sea ice free? Geophys Res Lett 40. doi:10.1002/grl.50316
Parkinson CL, Cavalieri DJ (2008) Arctic sea ice variability and trends, 1979–2006. J Geophys Res C 113:C07003
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Høye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGruire AD, Rysgaard S, Schindler DE, Stirling I, Tamstorf MP, Tyler MJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358
Prowse TD, Furgal C, Wrona FJ, Reist JD (2009) Implications of climate change for northern Canada: freshwater, marine, and terrestrial ecosystems. Ambio 38:282–289
Rausch RL, George JC, Brower HK (2007) Effect of climatic warming on the Pacific walrus, and potential modification of its helminth fauna. J Parasitol 93:1247–1251
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN version 2.0: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva
Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proc R Soc B 249:463–471
Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16
Sonsthagen SA, Talbot SL, White CM (2004) Gene flow and genetic characterization of northern goshawks breeding in Utah. Condor 106:826–836
Sonsthagen SA, Jay CV, Fischbach AS, Sage GK, Talbot SL (2012) Spatial genetic structure and asymmetrical gene flow within the Pacific walrus. J Mamm 93:1512–1524
Stirling I, Parkinson CL (2006) Possible effects of climate warming on selected populations of polar bears (Ursus maritimus) in the Canadian Arctic. Arctic 59:261–275
Sunnucks P, Wilson ACC, Beheregaray LB, Zenger K, French J, Taylor AC (2000) SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol Ecol 9:1699–1710
Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601
Tamura K, Nei M (1989) Positive Darwinian selection observed at the variable-region genes of immunoglobulins. Mol Biol Evol 6:447–459
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 28:2731–2739
Trenberth KE, Jones PD, Ambenje P, Bojariu R, Easterling D, Klein Tank A, Parker D, Rahimzadeh F, Renwick JA, Rusticucci M, Soden B, Zhai P (2007) Observations: surface and atmospheric climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 235–336
Villanueva-Noriega MJ, Baker CS, Medrano-González L (2013) Evolution of MHC-DQB exon 2 in marine and terrestrial mammals. Immunogenetics 65:47–61
Wakeland EK, Boehme S, She JX, Lu CC, McIndoe RA, Cheng I, Ye Y, Potts WK (1990) Ancestral polymorphism of MHC Class II genes: divergent allele advantage. Immunol Res 9:115–122
Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three Class II loci in the northern elephant seal. Mol Ecol 13:711–718
Wedekind C, Walker M, Little TJ (2005) The course of malaria in mice: major histocompatibility complex effects, but no general MHC heterozygote advantage in single-strain infections. Genetics 170:1427–1430
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121
Acknowledgments
This research was funded by the US Geological Survey, Ecosystems Mission Area, Wildlife Program. Research was conducted under institutional animal care and use committee approval (approval number 06SOP06). We thank the scientific staff and crew for sample collections during cruises aboard the USCG Healy, R/V Magadan, and R/V Stimson; E.W. Born for providing samples from Atlantic walruses; A. Fischbach for assisting with Pacific walrus sample collection; and R. Dial, Alaska Pacific University, for undergraduate mentorship of K.F. The manuscript was improved by comments from C. Lindqvist, University at Buffalo, and R. Wilson, University of Alaska Fairbanks. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement of the US Government.
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Sonsthagen, S.A., Fales, K., Jay, C.V. et al. Spatial variation and low diversity in the major histocompatibility complex in walrus (Odobenus rosmarus). Polar Biol 37, 497–506 (2014). https://doi.org/10.1007/s00300-014-1450-9
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DOI: https://doi.org/10.1007/s00300-014-1450-9