Abstract
Gila trout (Oncorhynchus gilae gilae) was federally protected in 1973 because of severe declines in abundance and geographic range size. At present, four relict genetic lineages of the species remain in mountain streams of New Mexico and Arizona, USA. Management actions aimed at species recovery, including hatchery production and restocking of formerly occupied streams, have been guided by information from non-functional genetic markers. In this study, we investigated genetic variation at exon 2 of the major histocompatibility complex (MHC) class II β gene that is involved in pathogen resistance and thus presumably under natural selection. Phylogenetic analysis revealed trans-species polymorphism and a significantly high ratio of non-synonymous to synonymous amino acid changes consistent with the action of historical balancing selection that maintained diversity at this locus in the past. However, Gila trout exhibited low allelic diversity (five alleles from 142 individuals assayed) compared to some other salmonid fishes, and populations that originated exclusively from hatcheries possessed three or fewer MHC alleles. Comparative analysis of genetic variation at MHC and six presumably neutrally evolving microsatellite loci revealed that genetic drift cannot be rejected as a primary force governing evolution of MHC in contemporary populations of Gila trout. Maintenance of diversity at MHC will require careful implementation of hatchery breeding protocols and continued protection of wild populations to prevent loss of allelic diversity due to drift.
Similar content being viewed by others
References
Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Disease susceptibility in California sea lions. Nature 422:35
Aguilar A, Garza JC (2006) A comparison of variability and populations structure for major histocompatibility complex and microsatellite loci in California coastal steelhead (Oncorhynchus mykiss Walbaum). Mol Ecol 15:923–937
Aguilar A, Roemer G, Debenbaum S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494
Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224
Arkush KD, Giese AR, Mendonca HL, McBride AM, Marty GD, Hedrick PW (2002) Resistance to three pathogens in the endangered winter–run Chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can J Fish Aquat Sci 59:966–975
Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc Roy Soc (London) B 263:1619–1626
Behnke RJ (1992) Native trout of western North America. Amer Fish Soc Monogr 6:275
Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377
Boyce WM, Hedrick PW, Muggli-Cockett NE, Kalinowski S, Penedo MCT, Ramey RR II (1997) Genetic variation of major histocompatibility complex and microsatellite loci: a comparison in bighorn sheep. Genetics 145:421–433
Brown DK, Echelle AA, Propst DL, Brooks JE, Fisher WL (2001) Catastrophic wildfire and number of populations as factors influencing risk of extinction for Gila trout (Oncorhynchus gilae). W North Amer Nat 61:139–148
Brown JH, Jardetzsky 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 364:33–39
Carmichael G, Hanson JN, Schmidt ME, Morizot DC (1993) Introgression among Apache, Cutthroat, and Rainbow Trout in Arizona. Trans Amer Fish Soc 122:121–130
Campos JL, Posada D, Morán P (2006) Genetic variation at MHC, mitochondrial and microsatellite loci in isolated populations of Brown trout (Salmo trutta). Conserv Genet 7:515–530
Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267
Dorschner MO, Duris CR, Bronte CR, Burnham Curtis MK, Phillips RB (2000) High levels of MHC Class II allelic diversity in Lake Trout from Lake Superior. J Hered 91:359–363
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825
Garrigan D, Hedrick PW (2003) Detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722
Grimholt U, Getahum A, Hermsen T, Stet RJM (2000) The major histocompatibility class II alpha chain in salmonid fishes. Devel Comp Immunol 24:751–763
Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015
Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Amer Nat 143:945–964
Hedrick PW, Parker KM (1998) MHC variation in the endangered Gila topminnow. Evolution 52:194–199
Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics 104:449–456
Hedrick PW, Parker KM, Lee RN (2001) Using microsatellite and MHC variation to identify species, ESUs, and MU in the endangered Sonoran topminnow. Mol Ecol 10:1399–1412
Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86:958–962
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York
Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Kim TJ, Parker KM, Hedrick PW (1999) Major histocompatibility complex differentiation in Sacramento river Chinook salmon. Genetics 151:1115–1122
Klein J (1987) Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 19:155–162
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol Ecol 10:2525–2539
Landry C, Garant D, Duchesne P, Bernatchez L (2001) ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc R Soc Lond B 268:1279–1285
Langefors ÅH (2005) Adaptive and neutral genetic variation and colonization history of Atlantic salmon, Salmo salar. Env Biol Fish 74:297–308
Langefors Å, Lohm J, Grahn M, Andersen Ø, von Shantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B 268:479–485
Leary RF, Allendorf FW (1999) Genetic issues in the conservation and restoration of the endangered Gila trout: update. Wild Trout and Salmon Genetics Laboratory Report 99/2. Division of Biological Sciences, University of Montana, Missoula, Montana
Lehman N, Decker DJ, Stewart BS (2004) Divergent patterns of variation in major histocompatibility complex class II alleles among antartic phocid pinnipeds. J Mammol 85:1215–1224
Loudenslager EJ, Rinne JN, Gall GAE, David RE (1986) Biochemical genetic studies of native Arizona and New Mexico trout. Southwest Nat 31:221–234
McLean JE, Bentzen P, Quinn TP (2004) Differential reproductive success of sympatric, naturally spawning hatchery and wild steelhead, Oncorhynchus mykiss. Env Biol Fish 69:359–369
Miller RR (1950) Notes on the cutthroat and rainbow trouts with the description of a new species from the Gila River, New Mexico. Occas Pap Mus Zool Univ Mich 529:1–42
Miller KM, Kaukinen KH, Beacham TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica 111:237–257
Morris DB, Richard KR, Wright JM (1996) Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can J Fish Aquat Sci 53:120–126
Nei M, Gojobori T (1986) Simple method for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
O’Connell M, Danzmann RG, Cornuet JM, Wright JM, Ferguson MM (1997) Differentiation of rainbow trout (Oncorhynchus mykiss) populations in Lake Ontario and the evaluation of the stepwise mutation and infinite allele mutation models using microsatellite variability. Can J Fish Aquat Sci 54:1391–1399
Ohta T (1998) On the pattern of polymorphisms at major histocompatibility complex loci. J Mol Evol 46:633–638
Olsén KH, Grahn M, Lohm J, Langefors Ǻ (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim Behav 56:319–327
Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc Natl Acad Sci USA 95:3714–3719
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Propst DL, Stefferud JA (1997) Population dynamics of Gila trout in the Gila River drainage of the southwestern United States. J Fish Biol 51:1137–1154
Propst DL, Stefferud JA, Turner PR (1992) Conservation and status of Gila trout, Oncorhynchus gilae. Southwest Nat 37:117–125
Rambaut A (1996) Se–Al: sequence alignment editor. Available at http://www.evolve.zoo.ox.ac.uk/
Raymond M, Rousset F (1995) genepop (Version 1.2) population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3:301–307
Reisenbichler RR, Rubin SP (1999) Genetic changes from artificial propagation of Pacific salmon affect the productivity and viability of supplemented populations. ICES J Mar Sci 56:459–466
Rexroad CE, Coleman RL, Hershberger WK, Killefer J (2002) Rapid communication: thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. J Anim Sci 80:541–542
Riddle BR, Propst DL, Yates TL (1998) Mitochondrial DNA variation in Gila trout, Oncorhynchus gilae: implications for management of an endangered species. Copeia 1998:31–39
Ristow SS, Grabowski LD, Thompson SM, Warr GW, Kaattari SL, de Avila JM, Thorgaard GH (1999) Coding sequences of the MHC II beta chain of homozygous rainbow trout (Oncorhynchus mykiss). Devel Comp Immunol 23:51–60
Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329
Schneider S, Roessli D, Excoffier L (2000) arlequin ver 2.000: a software for population genetic analysis. Available at http://www.cmpg.unibe.ch/software/arlequin3/
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116
Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJ, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297–3308
Slade RW, McCallum HI (1992) Overdominant vs. frequency-dependent selection at MHC loci. Genetics 132:861–862
Spies IB, Brasier DJ, O’Reilly PTL, Seamons S, Bentzen P (2005) Development and characterization of novel tetra-, tri-, and dinucleotide microsatellite markers in rainbow trout (Oncorhynchus mykiss). Mol Ecol Notes 5:278–281
Stevens L, Yan G, Pray LA (1997) Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution 51:2032–2039
Swofford DL (2001) paup. Phylogenetic analysis using parsimony (*and other methods). Vers. 4 Beta. Sinauer, Sunderland, MA
Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978
US Fish and Wildlife Service (2003) Gila trout recovery plan, 3rd revision. Albuquerque, NM
Wares JP, Aló DA, Turner TF (2004) A genetic perspective on management and recovery of federally endangered trout (Oncorhynchus gilae) in the American Southwest. Can J Fish Aquat Sci 61:1890–1899
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Yang ZH (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comp Appl Biosci 13:555–556
Yang ZH, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118
Yokota M, Harada Y, Iizuka M (2003) Genetic drift in a hatchery and the maintenance of genetic diversity in hatchery-wild systems. Fish Sci 69:101–109
Acknowledgements
This work is part of a multi-agency effort to conserve and recover the Gila trout in its native range. We are indebted to personnel of the US Fish & Wildlife Service, the USDA Forest Service, the New Mexico Department of Game and Fish, and the Arizona Department of Game and Fish; especially J. Brooks, K. Young, J. Monzingo, D. Propst, and J. Seals for providing samples used in this study (collected under their permits). J. Wares provided a pilot MHC data set that motivated this study. We are grateful to M. Osborne, W. Wilson, and D. Alò for assistance in the laboratory. W. Wilson made crucial suggestions on analysis of selection on the peptide-binding region and recombination and S. Poe provided guidance on phylogenetic analysis. D. Karapatakis and the Savannah River Ecology Laboratory provided software and assistance necessary for GIS mapping of Gila trout range via funding from the Environmental Remediation Sciences Division of the Office of Biological and Environmental Research, U.S. Department of Energy through the Financial Assistance Award No. DE-FC09-96SR 18546 to the University of Georgia Research Foundation. We are grateful to R. Miller, W. Wilson, M. Osborne, J. Cook, and especially D. Propst for comments and suggestions on the manuscript. Funding for this study was provided by the National Science Foundation (NSF) DEB-0133233 (TFT). Opinions, findings and conclusions or recommendations expressed in this paper are those of the authors and do not necessarily reflect the views of the NSF. Additional funding to MBP was provided by T & E, Inc., the University of New Mexico (UNM) Biology and Graduate Professional Student Associations, the UNM Department of Biology, and the UNM Office of Graduate Studies.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Peters, M.B., Turner, T.F. Genetic variation of the major histocompatibility complex (MHC class II β gene) in the threatened Gila trout, Oncorhynchus gilae gilae . Conserv Genet 9, 257–270 (2008). https://doi.org/10.1007/s10592-007-9336-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-007-9336-9