Abstract
The Swedish moose was analysed for genetic variability at major histocompatibility complex (MHC) class I and class II DQA, DQB and DRB loci using restriction fragment length polymorphism (RFLP) and single strand conformation polymorphism (SSCP) techniques. Both methods revealed limited amounts of polymorphism. Since the SSCP analysis concerned an expressed DRB gene it can be concluded that the level of functional MHC class II polymorphism, at least at the DRB locus, is low in Swedish moose. DNA fingerprinting was used to determine if the unusual pattern of low MHC variability could be explained by a low degree of genome‐wide genetic diversity. Hybridizations with two minisatellite probes gave similarity indices somewhat higher than the average for other natural population, but the data suggest that the low MHC variability cannot be explained by a recent population bottleneck. However, since minisatellite sequences evolve more rapidly than MHC sequences, the low levels of MHC diversity may be attributed to a bottleneck of more ancient origin. The selection pressure for MHC variability in moose may also be reduced and we discuss the possibility that its solitary life style may reduce lateral transmission of pathogens in the population.
Keywords: bottleneck, DNA fingerprinting, genetic variation, MHC, moose, SSCP
This work is a part of Elisabetta Giuffra's PhD thesis on the geographical variation at protein loci and mtDNA in the S. trutta complex from Northern Italy. René Guyomard is a population geneticist at the Laboratory of Fish Genetics of INRA. This laboratory is involved in research programs on conservation, management and selective breeding of freshwater fish species. Gilberto Forneris is ichthyologist at the Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia of the University of Turino and is responsible for programs of conservation of natural population of freshwater fish in the Piemonte Province.
References
- Andersson L., Davies CJ (1994) The major histocompatibility complex In: Cell‐Mediated Immunity in Ruminants (eds Goddeeris BM, Morrison WI.), pp. 37–57. CRC Press Inc., Boca Raton , FL . [Google Scholar]
- Andersson L., Lundberg C., Rask L., Gissel‐Nielsen B., Simonsen M. (1987) Analysis of class II genes of the chicken MHC (B) by use of human DNA probes. Immunogenetics, 26, 79–84. [DOI] [PubMed] [Google Scholar]
- Baccus R., Ryman N., Smith MH, Reuterwall C., Cameron D. (1983) Genetic variability and differentiation of large grazing mammals. Journal of Mammology, 64, 109–120. [Google Scholar]
- Bodmer WF (1972) Evolutionary significance of the HLA‐system. Nature, 237, 139–145. [DOI] [PubMed] [Google Scholar]
- Brown JH, Jardetzky T., Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1988) Three‐dimensional structure of the human class II histocompatibility complex antigen HLA‐DR1. Nature, 364, 33–39. [DOI] [PubMed] [Google Scholar]
- Darden AG, Streilein JW (1984) Syrian hamsters express two monomorphic class I major histocompatibility complex molecules. Immunogenetics, 20, 603–622. [DOI] [PubMed] [Google Scholar]
- Doherty PC, Zinkernagel RM (1975) A biological role for major histocompatibility antigens. Lancet, i, 1406–1409. [DOI] [PubMed] [Google Scholar]
- Ellegren H., Andersson L., Wallin K. (1991) DNA polymorphism in the moose (A. alces) revealed by the polynucleotide probe (TC)n . Journal of Heredity, 82, 429–431. [Google Scholar]
- Ellegren H., Hartman G., Johansson M., Andersson L. (1993) Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proceedings of the National Academy of Sciences of the USA, 90, 8150–8153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georges M., Lequaree AS, Catelli M., Hanset R., Vassart G. (1988) DNA fingerprinting in domestic animals using four different minisatellite probes. Cytogenetics and Cell Genetics, 47, 127–131. [DOI] [PubMed] [Google Scholar]
- Gustafsson K., Wiman K., Emmoth E., Larhammar D., Böhme J., Hyldig‐Nielsen JJ, Ronne H., Peterson PA, Rask L. (1984) Mutations and selection in the generation of class II histocompatibility antigen polymorphism. EMBO Journal, 3, 1655–1661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hedrick PW, Thomson G. (1983) Evidence for balancing selection at HLA. Genetics, 104, 449–456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hedrick PW, Thomsen G. (1988) Maternal‐fetal interactions and the maintenance of HLA polymorphism. Genetics, 119, 205–212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hedrick P., Jain S., Holden L. (1978) Multilocus systems in evolution. Evolutionary Biology, 11, 101–184. [Google Scholar]
- Hill WG (1974) Estimation of linkage disequilibrium in randomly mating population. Heredity, 33, 229–239. [DOI] [PubMed] [Google Scholar]
- Hughes AL (1991) MHC polymorphism and the design of captive breeding programs. Conservation Biology, 5, 249–251. [Google Scholar]
- Jeffreys AJ, Wilson V., Thein SL (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature, 314, 67–73. [DOI] [PubMed] [Google Scholar]
- Jeffreys AJ, Royle NJ, Wilson V., Wong Z. (1988) Spontaneous mutation rates to new length alleles at tandem‐repetitive hypervariable loci in human DNA. Nature, 332, 278–281. [DOI] [PubMed] [Google Scholar]
- Klein J. (1986) Natural History of the Major Histocompatibility Complex. John Wiley & Sons, New York . [Google Scholar]
- Klein J., Satta Y., O'hUigin C., Takahata N. (1993) The molecular descent of the major histocompatibility complex. Annual Review of Immunology, 11, 269–295. [DOI] [PubMed] [Google Scholar]
- Larhammar D., Schenning L., Gustafsson K., Wiman K., Claesson L., Rask L., Peterson PA (1982) Complete amino acid sequence of an HLA‐DR antigen‐like β chain as predicted from the nucleotide sequence: similarities with immunoglobulins and HLA‐A, ‐B, and ‐C antigens. Proceedings of the National Academy of Sciences of the USA, 79, 3687–3691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindberg PG, Andersson L. (1988) Close association between DNA polymorphism of bovine major histocompatibility complex class I genes and serological BoLA‐A specificities. Animal Genetics, 19, 245–255. [DOI] [PubMed] [Google Scholar]
- Maekawa M., Sudo K., Li SSL, Kanno T. (1992) Detection of genetic mutations in LDH‐A and LDH‐B genes by PCR‐SSCP analysis on PhastSystem. Science Tools, 36, 6–8. [Google Scholar]
- Mariani P., Johansson M., Ellegren H., Harbitz I., Juneja RK, Andersson L. (1992) Multiple RFLPs in the porcine calcium release channel gene (CRC): assignment to the halothane (HAL) linkage group. Animal Genetics, 23, 257–262. [DOI] [PubMed] [Google Scholar]
- McGuire KL, Duncan WR, Tucker PW (1985) Syrian Hamster DNA shows limited polymorphism at class I‐like loci. Immunogenetics, 22, 257–268. [DOI] [PubMed] [Google Scholar]
- Menotti‐Raymond M., O'Brien SJ (1993) Dating the genetic bottleneck of the African cheetah. Proceedings of the National Academy of Sciences of the USA, 90, 3172–3176. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michaud J., Brody LC, Steel G., Fontaine G., Martin LS, Valle D., Mitchell G. (1992) Strand‐separating conformational polymorphism analysis: efficacy of detection of point mutations in the human omithine d‐aminotransferase gene. Genomics, 13, 389–394. [DOI] [PubMed] [Google Scholar]
- Mikko S., Andersson L. (1995) Low major histocompatibility complex class II diversity in European and North‐American Moose. Proceedings of the National Academy of Sciences of the USA, 92, 4259–4263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nevo E. (1978) Genetic variation in natural populations: patterns and theory. Theoretical Population Biology, 13, 121–177. [DOI] [PubMed] [Google Scholar]
- O'Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends in Ecology and Evolution, 3, 254–259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Brien SJ, Roelke ME, Marker L., Newman A., Winkler CA, Meltzer D., Cooly L., Evermann JF, Bush M., Wildt DE (1985) Genetic basis for species vulnerability in the Cheetah. Science, 227, 1428–1434. [DOI] [PubMed] [Google Scholar]
- Orita M., Suzuki Y., Sekiya T., Hayashi K. (1989) Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics, 5, 874–879. [DOI] [PubMed] [Google Scholar]
- Potts WK, Wakeland EK (1993) Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends in Genetics, 9, 408–412. [DOI] [PubMed] [Google Scholar]
- Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA ‘fingerprinting’ reveals high levels of inbreeding in colonies of the eusocial naked mole‐rat. Proceedings of the National Academy of Sciences of the USA, 87, 2496–2500. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ryman N., Reuterwall C., Nygren K., Nygren T. (1980) Genetic variation and differentiation in Scandinavian moose (Alces alces): are large mammals monomorphic Evolution, 34, 1037–1049. [DOI] [PubMed] [Google Scholar]
- Schenning L., Larhammar D., Bill P., Wiman K., Jonsson AK, Rask L., Peterson PA (1984) Both α and β chains of HLA‐DC class II histocompatibility antigens display extensive polymorphism in their amino‐terminal domains. EMBO Journal, 3, 447–452. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheffield VC, Beck JS, Kwitek AE (1992) Analysis of the Efficiency of Single Base Substitution Detection by SSCP. Cold Spring Harbor Laboratory, New York . [Google Scholar]
- Sigurdardottir S., Lundén A., Andersson L. (1988) Restriction fragment length polymorphism of DQ and DR class II genes of the bovine major histocompatibility complex. Animal Genetics, 19, 133–150. [DOI] [PubMed] [Google Scholar]
- Sigurdardóttir S., Borsch C., Gustafsson K., Andersson L. (1991) Cloning and sequence analysis of 14 DRB alleles of the bovine MHC by using the polymerase chain reaction. Animal Genetics, 22, 199–209. [DOI] [PubMed] [Google Scholar]
- Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proceedings of the Royal Society of London, B249, 163–171. [DOI] [PubMed] [Google Scholar]
- Stéen M., Diaz R., Faber WE (1993) An erosive/ulcerative alimentary disease of undetermined etiology in Swedish moose (Alces alces L.). Rangifer, 13, 149–156. [Google Scholar]
- Trowsdale J., Groves V., Arnason A. (1989) Limited MHC polymorphism in whales. Immunogenetics, 29, 19–24. [DOI] [PubMed] [Google Scholar]
- Vassart G., Georges M., Monsieur R., Brocas H., Lequarre AS, Christiophe D. (1987) A sequence in M13 phage detects hypervariable minisatellites in human and animal DNA. Science, 235, 683–684. [DOI] [PubMed] [Google Scholar]
- Wooten MC, Smith MH (1985) Large mammals are genetically less variable. Evolution, 39, 210–212. [DOI] [PubMed] [Google Scholar]
- Yuhki N., O'Brien SJ (1990) DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proceedings of the National Academy of Sciences of the USA, 87, 836–840. [DOI] [PMC free article] [PubMed] [Google Scholar]