Abstract
Wildlife immune genes are subject to natural selection exerted by pathogens. In contrast, domestic immune genes are largely protected from pathogen selection by veterinary care. Introgression of domestic alleles into the wild could lead to increased disease susceptibility, but observations are scarce due to low introgression rates, low disease prevalence and reduced survival of domestic hybrids. Here we report the first observation of a deleterious effect of domestic introgression on disease prevalence in a free-living large mammal. A fraction of 462 randomly sampled free-living European wild boar (Sus scrofa) was genetically identified as recent wild boar–domestic pig hybrids based on 351 SNP data. Analysis of antibody prevalence against the bacterial pathogen Mycoplasma hyopneumoniae (Mhyo) showed an increased Mhyo prevalence in wild–domestic hybrids. We argue that the most likely mechanism explaining the observed association between domestic hybrid status and Mhyo antibody prevalence would be introgression of deleterious domestic alleles. We hypothesise that large-scale use of antibiotics in the swine breeding sector may have played a role in shaping the relatively deleterious properties of domestic swine immune genes and that domestic introgression may also lead to increased wildlife disease susceptibility in the case of other species.
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References
Acevedo-Whitehouse K, Vicente J, Gortazar C, Hofle U, Fernandez-De-Mera IG, and Amos W (2005). Genetic resistance to bovine tuberculosis in the Iberian wild boar. Molecular Ecology 14:3209-3217.
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, and Rohani P (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9:467-484.
Altizer S, Harvell D, and Friedle E (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution 18:589-596.
Bar-David S, Lloyd-Smith JO, and Getz WM (2006). Dynamics and management of infectious disease in colonizing populations. Ecology 87:1215-1224.
Bengis RG, Kock RA, and Fischer J (2002). Infectious animal diseases: the wildlife/livestock interface. Revue Scientifique Et Technique De L Office International Des Epizooties 21:53-65.
Berger RL (1996). More Powerful Tests from Confidence Interval p Values. The American Statistician 50:314-318.
Berger RL, and Boos DD (1994). P Values Maximized Over a Confidence Set for the Nuisance Parameter. Journal of the American Statistical Association 89:1012-1016.
Booth WD (1995). Wild boar farming in the United Kingdom. IBEX, Journal of Mountain Ecology, 3:245-248
Briedermann L (1990). Schwarzwild. VEB Deutscher Landwirtschaftsverlag, Berlin, Germany.
Caruso JP, and Ross RF (1990). Effects of Mycoplasma-Hyopneumoniae and Actinobacillus (Hemophilus) Pleuropneumoniae Infections on Alveolar Macrophage Functions in Swine. American Journal of Veterinary Research 51:227-231.
Charley B, Riffault S, Van Reeth K (2006) Porcine innate and adaptative immune responses to influenza and coronavirus infections. In: Impact of Emerging Zoonotic Diseases on Animal Health, Oxford: Blackwell Publishing, pp 130–136
Chiari M, Ferrari N, Zanoni M, and Alborali L (2014). Mycoplasma hyopneumoniae temporal trends of infection and pathological effects in wild boar populations. European Journal of Wildlife Research 60:187-192.
Closa-Sebastià F, Casas-Díaz E, Cuenca R, Lavín S, Mentaberre G, and Marco I (2011). Antibodies to selected pathogens in wild boar (Sus scrofa) from Catalonia (NE Spain). European Journal of Wildlife Research 57:977-981.
Cohen ML (1992). Epidemiology of Drug-Resistance - Implications for a Post-antimicrobial Era. Science 257:1050-1055.
Curtis J, and Bourne FJ (1971). Immunoglobulin quantitation in sow serum, colostrum and milk, and the serum of young pigs.. Biochimica et Biophysica Acta (BBA) - Protein Structure 236:319-332.
Daszak P (2000). Emerging infectious diseases of wildlife - Threats to biodiversity and human health (vol 287, pg 443, 2000). Science 287:1756-1756.
Dee S, Otake S, Oliveira S, and Deen J (2009). Evidence of long distance airborne transport of porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae. Veterinary Research 40, 1–13.
Epstein PR (1995). Emerging diseases and ecosystem instability: new threats to public health. Am J Public Health 85:168-172.
Goedbloed DJ, Megens HJ, van Hooft P, Herrero-Medrano JM, Lutz W, Panoraia A, et al. (2013a). Genome-wide single nucleotide polymorphism reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Molecular Ecology 22:856-866.
Goedbloed DJ, Van Hooft P, Megens HJ, Langenbeck K, Lutz W, Crooijmans RP, et al. (2013b). Reintroductions and genetic introgression from domestic pigs have shaped the genetic population structure of Northwest European wild boar. Bmc Genetics 14:43.
Goedbloed DJ, van Hooft P, Megens HJ, Bosch T, Lutz W, van Wieren SE, et al. (2014). Host genetic heterozygosity and age are important determinants of porcine circovirus type 2 disease prevalence in European wild boar. European Journal of Wildlife Research 60:803–810.
Goodwin RFW (1985). Apparent Reinfection of Enzootic-Pneumonia-Free Pig Herds - Search for Possible Causes. Veterinary Record 116:690-694.
Gortazar C, Acevedo P, Ruiz-Fons F, and Vicente J (2006). Disease risks and overabundance of game species. European Journal of Wildlife Research 52:81-87.
Gortazar C, Ferroglio E, Hoefle U, Froelich K, and Vicente J (2007). Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53:15.
Grenfell BT, and Dobson AP (1995). Ecology of infectious diseases in natural populations. Cambridge University press, Cambridge.
Hälli O, Ala-Kurikka E, Nokireki T, Skrzypczak T, Raunio-Saarnisto M, Peltoniemi OAT, et al. (2012). Prevalence of and risk factors associated with viral and bacterial pathogens in farmed European wild boar. The Veterinary Journal 194:98-101.
Janeway CA, Travers P, Walport M, Shlomchik MJ (2001) Immunobiology. Garland Science
Kishima M, and Ross RF (1985). Suppressive Effect of Nonviable Mycoplasma-Hyopneumoniae on Phytohemagglutinin-Induced Transformation of Swine Lymphocytes. American Journal of Veterinary Research 46:2366-2368.
Kruse H, Kirkemo AM, and Handeland K (2004). Wildlife as source of zoonotic infections. Emerging Infectious Diseases 10:2067-2072.
Kuhnert P, Overesch G (2014). Molecular epidemiology of Mycoplasma hyopneumoniae from outbreaks of enzootic pneumonia in domestic pig and the role of wild boar. Veterinary Microbiology 174:261–266
Lamaze FC, Pavey SA, Normandeau E, Roy G, Garant D, and Bernatchez L (2014). Neutral and selective processes shape MHC gene diversity and expression in stocked brook charr populations (Salvelinus fontinalis). Molecular Ecology 23:1730-1748.
Lebarbenchon C, Poulin R, Gauthier-Clerc M, and Thomas F (2007). Parasitological consequences of overcrowding in protected areas. Ecohealth 3:303-307.
Lipowski A (2003). European wild boar (Sus scrofa L.) as a reservoir of infectious diseases for domestic pigs. Medycyna Weterynaryjna 59:861-863.
Lydersen S, Langaas M, and Bakke O (2012). The exact unconditional z-pooled test for equality of two binomial probabilities: optimal choice of the Berger and Boos confidence coefficient. Journal of Statistical Computation and Simulation 82:1311-1316.
Maes D, Segales J, Meyns T, Sibila M, Pieters M, and Haesebrouck F (2008). Control of Mycoplasma hyopneumoniae infections in pigs. Veterinary Microbiology 126:297-309.
Meyns T, Maes D, Dewulf J, Vicca J, Haesebrouck F, and de Kruif A (2004). Quantification of the spread of Mycoplasma hyopneumoniae in nursery pigs using transmission experiments. Preventive Veterinary Medicine 66:265-275.
Patterson N, Price AL, and Reich D (2006). Population structure and eigenanalysis. PLoS Genet 2:e190.
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, and Reich D (2006). Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics 38:904-909.
Pritchard JK, Stephens M, and Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155:945-959.
Reiner G, Bronnert B, Hohloch C, Reinacher M, and Willems H (2011). Distribution of ORF2 and ORF3 genotypes of porcine circovirus type 2 (PCV-2) in wild boars and domestic pigs in Germany. Veterinary Microbiology 148:372-376.
Ruiz-Fons F, Segales J, and Gortazar C (2008). A review of viral diseases of the European wild boar: Effects of population dynamics and reservoir role. Veterinary Journal 176:158-169.
Ruiz-Fons F, Vicente J, Vidal D, Hofle U, Villanua D, Gauss C, et al. (2006). Seroprevalence of six reproductive pathogens in European wild boar (Sus scrofa) from Spain: The effect on wild boar female reproductive performance. Theriogenology 65:731-743.
Saez-Royuela C, Gomariz C, and Telleria JL (1989). Age determination of European wild boar (Sus scrofa). Wildlife Society Bulletin 17:326–329.
Segales J, Valero O, Espinal A, Lopez-Soria S, Nofrarias M, Calsamiglia M, et al. (2012). Exploratory study on the influence of climatological parameters on Mycoplasma hyopneumoniae infection dynamics. International Journal of Biometeorology 56:1167-1171.
Servanty S, Gaillard JM, Toïgo C, Brandt S, and Baubet E (2009). Pulsed resources and climate-induced variation in the reproductive traits of wild boar under high hunting pressure. Journal of Animal Ecology 78:1278-1290.
Sibila M, Mentaberre G, Boadella M, Huerta E, Casas-Díaz E, Vicente J, et al. (2010). Serological, pathological and polymerase chain reaction studies on Mycoplasma hyopneumoniae infection in the wild boar. Veterinary Microbiology 144:214-218.
Stark KD (1999). The role of infectious aerosols in disease transmission in pigs. Vet J 158:164-181.
Team RDC (2010). R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, Austria.
Thacker EL, Thacker BJ, Boettcher TB, and Jayappa H (1998). Comparison of antibody production, lymphocyte stimulation, and protection induced by four commercial Mycoplasma hyopneumoniae bacterins. Swine Health and Production 6:107-112.
Vengust G, Valencak Z, and Bidovec A (2006). A serological survey of selected pathogens in wild boar in Slovenia. Journal of Veterinary Medicine Series B-Infectious Diseases and Veterinary Public Health 53:24-27.
Vicente J, Segales J, Hofle U, Balasch M, Plana-Duran J, Domingo M, et al. (2004). Epidemiological study on porcine circovirus type 2 (PCV2) infection in the European wild boar (Sus scrofa). Veterinary Research 35:243-253.
Whiteman NK, Matson KD, Bollmer JL, and Parker PG (2006). Disease ecology in the Galapagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proceedings of the Royal Society B-Biological Sciences 273:797-804.
Wuensch U, Nitter G, and Schueler L (1999). Genetic and economic evaluation of genetic improvement schemes in pigs I. Methodology with an application to a three-way crossbreeding scheme. Archiv Fur Tierzucht-Archives of Animal Breeding 42:571-582.
Acknowledgments
We thank Mike Nieuwland and Ger de Vries-Reilingh for technical assistance. Thanks goes to Maarten Witvliet from Intervet® for contributing Mycoplasma hyopneumoniae antigen, and to the Animal Health Service Centre Deventer (GDD) and Karl Zimmer from the Landesuntersuchungsamt Rheinland-Pfalz for sample contributions. Finally, we thank the Royal Dutch Hunters Association (KNJV) for financial support.
Funding
This study was funded by the Royal Dutch Hunters Association (KNJV).
Conflict of interest
The authors declare that they have no conflict of interest.
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Goedbloed, D.J., van Hooft, P., Lutz, W. et al. Increased Mycoplasma hyopneumoniae Disease Prevalence in Domestic Hybrids Among Free-Living Wild Boar. EcoHealth 12, 571–579 (2015). https://doi.org/10.1007/s10393-015-1062-z
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DOI: https://doi.org/10.1007/s10393-015-1062-z