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Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance?

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Abstract

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.

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References

  • Abplanalp H (1979)The role of genetics in the immune response. Avian Dis.,23, 299–308.

    Google Scholar 

  • Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding:Disease susceptibility in California sea lions. Nature, 422, p.35.

    PubMed  Google Scholar 

  • Aiello SE, Mays A (eds.)(1998)The Merck Veterinary Manual, 8th edn.Merck & Co.Inc. Whitehouse Station,NJ,USA.

  • 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 

  • 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 

  • Benz G (1966)On the chemical nature of the heat stable exotoxin of Bacillus thuringiensis. Experientia, 22, 81–82.

    PubMed  Google Scholar 

  • Benz G, Graf E (1971)Antagonism of terramycin on action of Bacillus thuringiensis 'exotoxin' in Drosophila melanogaster. Experientia, 27, 73–75.

    PubMed  Google Scholar 

  • Black FL (1992)Why did they die?Science, 258, 1739–1740.

    PubMed  Google Scholar 

  • Blood DC, Studdert VP (1999)Saunders Comprehensive Veterinary Dictionary, 2nd edn.WB Saunders, London.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Burdon JJ (1987)Diseases and Plant Population Biology. Cambridge University Press, Cambridge,UK.

    Google Scholar 

  • Burges HD, Hurst JA (1977)Ecology of Bacillus thuringiensis in storage moths.J.Invert.Pathol.,30, 131–139.

    Google Scholar 

  • 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 

  • Caro TM, Laurenson MK (1994)Ecological and genetic factors in conservation:A cautionary tale.Science, 263, 485–486.

    PubMed  Google Scholar 

  • Caughley G (1994)Directions in conservation biology.J.Anim. Ecol.,63, 215–244.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Clay K, Kover PX (1996)The red queen hypothesis and plant/ pathogen interactions.Annu.Rev.Phytopathol.,34, 29–50.

    PubMed  Google Scholar 

  • 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 

  • Daszak P, Cunningham AA, Hyatt AD (2000)Emerging infectious diseases of wildlife:threats to biodiversity and human health.Science, 287, 443–449.

    PubMed  Google Scholar 

  • Dieraut LA, Gulland MD (2001)CRC Handbook of Marine Mammal Medicine, 2nd edn.CRC Press, Boca Paton.

    Google Scholar 

  • Diamond JM (1998)Guns,Germs and Steel:A Short History of Everybody for the Last 13,000 Years. Vintage, London,UK.

    Google Scholar 

  • 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 

  • Elgar MA, Clode D (2001)Inbreeding and extinctions in island populations:A cautionary tale.Conserv.Biol.,15, 284–286.

    Google Scholar 

  • England PR (1997)Conservation Genetics of Population Bottlenecks. Ph.D.thesis,Macquarie University, Sydney.

    Google Scholar 

  • Falconer DS, Mackay TFC (1996)Introduction to Quantitative Genetics, 4th edn.Longman, Harlow,UK.

    Google Scholar 

  • Ferguson MM, Drahuschchak LR (1990)Disease resistance and enzyme heterozygosity in rainbow trout.Heredity, 64, 413–417.

    PubMed  Google Scholar 

  • Flyg C, Dalhammar G, Rasmuson B, Boman HG (1987)Insect immunity–inducible antibacterial activity in Drosophila. Insect Biochem.,17, 153–160.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Frank SA (1992)Models of plant-pathogen coevolution.Trends Genet.,8, 213–219.

    PubMed  Google Scholar 

  • 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 

  • Frankham R, Briscoe DA, Ballou JD (2002)Introduction to Conservation Genetics. Cambridge University Press, Cambridge,UK.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Gardner MB, Kozak CA, O'Brien SJ (1991)The Lake Casitas wild mouse:Evolving genetic resistance to retroviral disease. Trends Genet.,7, 22–27.

    PubMed  Google Scholar 

  • Glazer AN, Nikaido H (1995)Microbial Biotechnology:Fundamentals of Applied Microbiology. WH Freeman and Company, New York.

    Google Scholar 

  • Haldane JBS (1949)Disease and evolution.Ricerca Sci., 19 (Suppl.),3–10.

    Google Scholar 

  • 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 

  • Hedrick PW, Kim TJ, Parker KM (2001)Parasite resistance and genetic variation in the endangered Gila topminnow. Anim.Conserv.,4, 103–109.

    Google Scholar 

  • Hilton-Taylor C (2000)2000 IUCN Red List of Threatened Species. IUCN, Gland,Switzerland.

    Google Scholar 

  • Huber BT (1992)Mls genes and self-superantigens.Trends Genet.,8, 399–402.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Lewontin RC (1974)The Genetic Basis of Evolutionary Change. Columbia University Press, New York.

    Google Scholar 

  • 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 

  • 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 

  • Lively CM (1996)Host-parasite coevolution and sex.Bio Science, 46, 107–114.

    Google Scholar 

  • Lively CM, Craddock C, Vrijenhoek RC (1990)Red queen hypothesis supported by parasitism in sexual clonal fish. Nature, 344, 864–866.

    Google Scholar 

  • 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 

  • 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 

  • May RM(1995)The cheetah controversy.Nature, 574, 309–310.

    Google Scholar 

  • McCallum H, Dobson A (1995)Detecting disease and parasite threats to endangered species and ecosystems.Trends Ecol. Evol.,10, 190–194.

    Google Scholar 

  • Meagher S (1999)Genetic diversity and Capillaria hepatica (Nematoda)prevalence in Michigan deer mouse populations.Evolution, 53, 1318–1324.

    Google Scholar 

  • Meltzer DGA (1993)Historical survey of disease problems in wildlife populations:Southern Africa mammals.J.Zoo Wildl.Med.,24, 237–244.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Nicholas FW (1987)Veterinary Genetics. Clarendon Press, Oxford.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Parker MA (1990)The pleiotropy theory for polymorphism of disease resistance genes in plants.Evolution, 44, 1872–1875.

    Google Scholar 

  • 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.

  • 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 

  • Plowright W (1982)The effects of rinderpest and rinderpest control on wildlife in Africa.Sym.Zool.Soc.Lond. 50, 1–28.

    Google Scholar 

  • Real LA (1996)Sustainability and the ecology of infectious disease.Bioscience,46,88–97.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Schmid-Hempel P, Crozier R (1999)Polyandry versus polygyny versus parasites.Proc.Roy Soc.Lond.B, 354, 507–515.

    Google Scholar 

  • Seal US (1991)Disease and captive conservation of threatened species.SSC Working Group meeting 28–29 May 1991, National Zoo,Washington,DC.

  • 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 

  • Sorci G, Moller AP, Boulinier T (1997)Genetics of host–parasite interaction.Trends Ecol.Evol.,12, 196–199.

    Google Scholar 

  • Spielman D (2002)Does Inbreeding and Loss of Genetic Diversity Decrease Resistance to Disease?Ph.D.thesis,Macquarie University, Sydney,Australia.

    Google Scholar 

  • Stevens L, Yan G, Pray LA (1997)Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution, 51, 2032–2039.

    Google Scholar 

  • Thorne ET, Williams ES (1988)Disease and endangered species: The black-footed ferret as a recent example.Conserv. Biol.,2, 66–74.

    Google Scholar 

  • Uhlig R (2002)10 million animals were slaughtered in foot and mouth cull.The Telegraph 23 Jan 2002 (//www.telegraph.co. uk/news/main.jhtml?xml=%2Fnews %2F2002 %2F01 %2F).

  • 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 

  • 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 

  • 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 

  • Warner RE (1968)The role of introduced diseases in the extinction of the endemic Hawaiian avifauna.Condor,70, 101–120.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Weatherall D (2003)Evolving with the enemy.New Scient., 180 (2422),44–47.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

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Spielman, D., Brook, B.W., Briscoe, D.A. et al. Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance?. Conservation Genetics 5, 439–448 (2004). https://doi.org/10.1023/B:COGE.0000041030.76598.cd

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