Conservation Genetics

, Volume 5, Issue 4, pp 439–448 | Cite as

Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance?

  • Derek Spielman
  • Barry W. Brook
  • David A. Briscoe
  • Richard Frankham


Inbreeding and loss of genetic diversity are predicted to decrease the resistance of species to disease. However, this issue is controversial and there is limited rigorous scientific evidence available. To test whether inbreeding and loss of genetic diversity affect a host's resistance to disease, Drosophila melanogasterpopulations with different levels of inbreeding and genetic diversity were exposed separately to (a) thuringiensin, an insecticidal toxin produced by some strains of Bacillus thuringiensis, and (b) live Serratia marcescensbacteria. Inbreeding and loss of genetic diversity significantly reduced resistance of D. melanogasterto both the thuringiensin toxin and live Serratia marcescens. For both, the best fitting relationships between resistance and inbreeding were curvilinear. As expected, there was wide variation among replicate inbred populations in disease resistance. Lowered resistances to both the toxin and the pathogen in inbred populations were due to specific resistance alleles, rather than generalized inbreeding effects, as correlations between resistance and population fitness were low or negative. Wildlife managers should strive to minimise inbreeding and loss of genetic diversity within threatened populations and to minimise exposure of inbred populations to disease.

disease resistance Drosophila melanogaster genetic diversity inbreeding population size 


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  1. Abplanalp H (1979)The role of genetics in the immune response. Avian Dis.,23, 299–308.Google Scholar
  2. Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding:Disease susceptibility in California sea lions. Nature, 422, p.35.PubMedGoogle Scholar
  3. Aiello SE, Mays A (eds.)(1998)The Merck Veterinary Manual, 8th edn.Merck & Co.Inc. Whitehouse Station,NJ,USA.Google Scholar
  4. Baer B, Schmid-Hempel P (1999)Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature, 397, 151–154.Google Scholar
  5. Behnke JM, Ali NMH, Jenkins SN (1984)Survival to patency of low-level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Ann.Trop.Med. Hyg.,78, 509–517.Google Scholar
  6. Benz G (1966)On the chemical nature of the heat stable exotoxin of Bacillus thuringiensis. Experientia, 22, 81–82.PubMedGoogle Scholar
  7. Benz G, Graf E (1971)Antagonism of terramycin on action of Bacillus thuringiensis 'exotoxin' in Drosophila melanogaster. Experientia, 27, 73–75.PubMedGoogle Scholar
  8. Black FL (1992)Why did they die?Science, 258, 1739–1740.PubMedGoogle Scholar
  9. Blood DC, Studdert VP (1999)Saunders Comprehensive Veterinary Dictionary, 2nd edn.WB Saunders, London.Google Scholar
  10. Boyle JF, Weismiller DG, Holmes KV (1987)Genetic resistance to mouse hepatitis virus correlates with absence of virus-binding activity on target tissues.J.Virol.,61, 185–189.PubMedGoogle Scholar
  11. Burdon JJ (1987)Diseases and Plant Population Biology. Cambridge University Press, Cambridge,UK.Google Scholar
  12. Burges HD, Hurst JA (1977)Ecology of Bacillus thuringiensis in storage moths.J.Invert.Pathol.,30, 131–139.Google Scholar
  13. Campbell DP, Dieball DE, Brackett JM (1987)Rapid HPLC assay for the b exotoxin of Bacillus thuringiensis. J.Agr. Food Chem.,35, 156–158.Google Scholar
  14. Caro TM, Laurenson MK (1994)Ecological and genetic factors in conservation:A cautionary tale.Science, 263, 485–486.PubMedGoogle Scholar
  15. Caughley G (1994)Directions in conservation biology.J.Anim. Ecol.,63, 215–244.Google Scholar
  16. Chesebro B, Miyazawa M, Britt WJ (1990)Host genetic control of spontaneous and induced immunity to Friend murine retrovirus infection.Annu.Rev.Immunol.,8, 477–499.PubMedGoogle Scholar
  17. Clay K, Kover PX (1996)The red queen hypothesis and plant/ pathogen interactions.Annu.Rev.Phytopathol.,34, 29–50.PubMedGoogle Scholar
  18. Coltman DW, Pilkington JG, Smith JM, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living island population.Evolution, 53, 1259–1267.Google Scholar
  19. Daszak P, Cunningham AA, Hyatt AD (2000)Emerging infectious diseases of wildlife:threats to biodiversity and human health.Science, 287, 443–449.PubMedGoogle Scholar
  20. Dieraut LA, Gulland MD (2001)CRC Handbook of Marine Mammal Medicine, 2nd edn.CRC Press, Boca Paton.Google Scholar
  21. Diamond JM (1998)Guns,Germs and Steel:A Short History of Everybody for the Last 13,000 Years. Vintage, London,UK.Google Scholar
  22. Dobson AP, May RM (1986)Disease and conservation.In: Conservation Biology:The Science of Scarcity and Diversity (ed.Soulé ME),pp.345–365.Sinauer,Sunderland, Massachusetts.Google Scholar
  23. Elgar MA, Clode D (2001)Inbreeding and extinctions in island populations:A cautionary tale.Conserv.Biol.,15, 284–286.Google Scholar
  24. England PR (1997)Conservation Genetics of Population Bottlenecks. Ph.D.thesis,Macquarie University, Sydney.Google Scholar
  25. Falconer DS, Mackay TFC (1996)Introduction to Quantitative Genetics, 4th edn.Longman, Harlow,UK.Google Scholar
  26. Ferguson MM, Drahuschchak LR (1990)Disease resistance and enzyme heterozygosity in rainbow trout.Heredity, 64, 413–417.PubMedGoogle Scholar
  27. Flyg C, Dalhammar G, Rasmuson B, Boman HG (1987)Insect immunity–inducible antibacterial activity in Drosophila. Insect Biochem.,17, 153–160.Google Scholar
  28. Flyg C, Kenne K, Boman HG (1980)Insect pathogenic properties of Serratia marcescens:Phage-resistant mutants with a decreased resistance to Cercropia immunity and a decreased virulence to Drosophila. J.Gen.Microbiol.,120, 173–181.PubMedGoogle Scholar
  29. Frank SA (1992)Models of plant-pathogen coevolution.Trends Genet.,8, 213–219.PubMedGoogle Scholar
  30. Frankham R (2000)Modeling problems in conservation genetics using laboratory animals.In: Quantitative Methods for Conservation Biology (eds.Ferson S, Burgman MA),pp. 259–273.Springer-Verlag, New York.Google Scholar
  31. Frankham R, Briscoe DA, Ballou JD (2002)Introduction to Conservation Genetics. Cambridge University Press, Cambridge,UK.Google Scholar
  32. Frankham R, Lees K, Montgomery ME, England PR, Lowe E, Briscoe DA (1999)Do population size bottlenecks reduce evolutionary potential?Anim.Conserv.,2, 255–260.Google Scholar
  33. Frankham R, Loebel DA (1992)Modeling problems in conservation genetics using captive Drosophila populations: Rapid adaptation to captivity.Zoo Biol.,11, 333–342.Google Scholar
  34. Frankham R, Yoo BH, Sheldon BL (1988)Reproductive tness and arti cial selection in animal breeding:culling on tness prevents a decline in reproductive tness in lines of Drosophila melanogaster selected for increased inebriation time. Theor.Appl.Genet. 76, 909–914.Google Scholar
  35. Franklin IR (1981)An analysis of temporal variation in isozyme loci in Drosophila melanogaster. In:Genetic Studies of Drosophila Populations (eds.Gibson JB, Oakeshott JG), pp.217–236.Australian National University Press, Canberra.Google Scholar
  36. Gardner MB, Kozak CA, O'Brien SJ (1991)The Lake Casitas wild mouse:Evolving genetic resistance to retroviral disease. Trends Genet.,7, 22–27.PubMedGoogle Scholar
  37. Glazer AN, Nikaido H (1995)Microbial Biotechnology:Fundamentals of Applied Microbiology. WH Freeman and Company, New York.Google Scholar
  38. Haldane JBS (1949)Disease and evolution.Ricerca Sci., 19 (Suppl.),3–10.Google Scholar
  39. Hedrick PW, Kim TJ (1999)Genetics of complex polymorphisms:Parasites and maintenance of MHC variation.In: Evolutionary Genetics: From Molecules to Man (eds.Singh RS, Krimbas CB),pp.204–234.Cambridge University Press, Cambridge,UK.Google Scholar
  40. Hedrick PW, Kim TJ, Parker KM (2001)Parasite resistance and genetic variation in the endangered Gila topminnow. Anim.Conserv.,4, 103–109.Google Scholar
  41. Hilton-Taylor C (2000)2000 IUCN Red List of Threatened Species. IUCN, Gland,Switzerland.Google Scholar
  42. Huber BT (1992)Mls genes and self-superantigens.Trends Genet.,8, 399–402.PubMedGoogle Scholar
  43. Jacobsen ER, Gaskin JM, Brown MB, Harris RK, Gardiner CH, La Pointe JL, Adams HP, Reggiardo C (1991)Chronic upper respiratory tract disease of free-ranging desert tortoises (Xerobates agassizii). J.Wildl.Dis.,27, 296–316.PubMedGoogle Scholar
  44. Lewontin RC (1974)The Genetic Basis of Evolutionary Change. Columbia University Press, New York.Google Scholar
  45. Lerner IM, Taylor LW, Beach JR (1950)Evidence for genetic variation in resistance to a respiratory infection in chickens. Poultry Sci.,29, 862–869.Google Scholar
  46. Liersch S, Schmid-Hempel P (1998)Genetic variability within social insect colonies reduces parasite load.Proc.Royal Soc. Lond.B, 265, 221–225.Google Scholar
  47. Lively CM (1996)Host-parasite coevolution and sex.Bio Science, 46, 107–114.Google Scholar
  48. Lively CM, Craddock C, Vrijenhoek RC (1990)Red queen hypothesis supported by parasitism in sexual clonal fish. Nature, 344, 864–866.Google Scholar
  49. Lyles AM, Dobson AP (1993)Infectious disease and intensive management:population dynamics,threatened hosts,and their parasites.J.Zoo Wildife Med.,24, 315–326.Google Scholar
  50. Marec F, Matha V, Weiser J (1988)Analysis of the genotoxic activity of Bacillus thuringiensis beta-exotoxin by means of the Drosophila wing spot test.J.Invert.Pathol.,53, 347–353.Google Scholar
  51. May RM(1995)The cheetah controversy.Nature, 574, 309–310.Google Scholar
  52. McCallum H, Dobson A (1995)Detecting disease and parasite threats to endangered species and ecosystems.Trends Ecol. Evol.,10, 190–194.Google Scholar
  53. Meagher S (1999)Genetic diversity and Capillaria hepatica (Nematoda)prevalence in Michigan deer mouse populations.Evolution, 53, 1318–1324.Google Scholar
  54. Meltzer DGA (1993)Historical survey of disease problems in wildlife populations:Southern Africa mammals.J.Zoo Wildl.Med.,24, 237–244.Google Scholar
  55. Merola M (1994)A reassessment of homozygosity and the case for inbreeding depression in the cheetah,Acinonyx jubatus: Implications for conservation.Conserv.Biol.,8, 961–971.Google Scholar
  56. Mitchell GF, Goding JW, Rickard MD (1977)Studies on immune responses to larval cestodes in mice:Increased susceptibility of certain mouse strains and hypothymic mice to Taenia taeniaeformis and analysis of passive transfer with serum.Aust.J.Exp.Biol.Med.,55, 165–186.Google Scholar
  57. Montgomery ME, Woodworth LM, Nurthen RK, Gilligan DM, Briscoe DA, Frankham R (2000)Relationship between population size and loss of genetic diversity:Comparisons of experimental results with theoretical predictions.Conserv. Genet.,1, 33–43.Google Scholar
  58. Nicholas FW (1987)Veterinary Genetics. Clarendon Press, Oxford.Google Scholar
  59. O'Brien SJ, Evermann JF (1988)Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol.Evol.,3, 254–259.Google Scholar
  60. O'Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science, 227,1428–1434.Google Scholar
  61. Oostermeijer JGB, Van Eijck MW, den Nijs JMC (1994)Off-springtness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae).Oecologia, 97, 289–296.Google Scholar
  62. Parker MA (1990)The pleiotropy theory for polymorphism of disease resistance genes in plants.Evolution, 44, 1872–1875.Google Scholar
  63. Paumard-Rigal S, Rosenberg-Bourgin M (1992)Increase in the resistance of the Bacillus thuringiensis supernatant effect in a Drosophila melanogaster wild type Oregon R line.Heredity, 69, 539–546.Google Scholar
  64. Pimm SL, Gittleman JL, McCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity.Trends Ecol.Evol.,4, 176–178.Google Scholar
  65. Plowright W (1982)The effects of rinderpest and rinderpest control on wildlife in Africa.Sym.Zool.Soc.Lond. 50, 1–28.Google Scholar
  66. Real LA (1996)Sustainability and the ecology of infectious disease.Bioscience,46,88–97.Google Scholar
  67. Roelke ME, Martenson JS, OBrien SJ (1993)The consequences of demographic reduction and genetic depletion in the endangered Florida panther.Curr.Biol.,3, 340–350.PubMedGoogle Scholar
  68. Schmid-Hempel P, Crozier R (1999)Polyandry versus polygyny versus parasites.Proc.Roy Soc.Lond.B, 354, 507–515.Google Scholar
  69. Seal US (1991)Disease and captive conservation of threatened species.SSC Working Group meeting 28–29 May 1991, National Zoo,Washington,DC.Google Scholar
  70. Sokal RR, Rohlf FJ (1995)Biometry:The Principles and Practice of Statistics in Biological Research, 3rd edn.WH Freeman and Company, New York.Google Scholar
  71. Sorci G, Moller AP, Boulinier T (1997)Genetics of host–parasite interaction.Trends Ecol.Evol.,12, 196–199.Google Scholar
  72. Spielman D (2002)Does Inbreeding and Loss of Genetic Diversity Decrease Resistance to Disease?Ph.D.thesis,Macquarie University, Sydney,Australia.Google Scholar
  73. Stevens L, Yan G, Pray LA (1997)Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution, 51, 2032–2039.Google Scholar
  74. Thorne ET, Williams ES (1988)Disease and endangered species: The black-footed ferret as a recent example.Conserv. Biol.,2, 66–74.Google Scholar
  75. Uhlig R (2002)10 million animals were slaughtered in foot and mouth cull.The Telegraph 23 Jan 2002 (// uk/news/main.jhtml?xml=%2Fnews %2F2002 %2F01 %2F).Google Scholar
  76. van Riper C, van Riper SG, Goff ML, Laird M (1986)The epizootiology and ecological signi cance of malaria in Hawaiian land birds.Ecol.Monogr.,56, 327–344.Google Scholar
  77. Vrijenhoek RC (1994)Genetic diversity and fitness in small populations.In:Conservation Genetics (eds.Loeschcke V, Tomiuk J, Jain SK),pp.37–53.Birkhäuser Verlag, Basel, Switzerland.Google Scholar
  78. Wakelin D (1985)Genetics,immunity and parasite survival.In: Ecology and Genetics of Host–Parasite Interactions (eds. Rollison D, Anderson RM),pp.39–54.Academic Press, London.Google Scholar
  79. Warner RE (1968)The role of introduced diseases in the extinction of the endemic Hawaiian avifauna.Condor,70, 101–120.Google Scholar
  80. Wassom DL, Brooks BO, Babisch JG, David CS (1983)A gene mapping between the S and D regions of the H-2 complex influences resistance to Trichinella spiralis infections of mice. J.Immunogenet.,10, 371–378.PubMedGoogle Scholar
  81. Weatherall D (2003)Evolving with the enemy.New Scient., 180 (2422),44–47.Google Scholar
  82. Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2002)Rapid genetic deterioration in captivity:Causes and conservation implications.Conserv.Genet.,3, 277–288.Google Scholar
  83. Yan G, Norman S(1995)Infection of Tribolium beetles with a tapeworm:Variation in susceptibility within and between beetle species and among genetic strains. J.Parasitol.,81, 37–42.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Derek Spielman
    • 1
    • 1
  • Barry W. Brook
    • 2
  • David A. Briscoe
    • 1
  • Richard Frankham
    • 1
    • 3
    • 1
  1. 1.Key Centre for Biodiversity and Bioresources, Department of Biological SciencesMacquarie UniversityAustralia
  2. 2.Key Centre for Tropical Wildlife ManagementCharles Darwin UniversityDarwinAustralia
  3. 3.School of Tropical BiologyJames Cook UniversityTownsvilleAustralia

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