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The Role of Evolution in the Emergence of Infectious Diseases

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The Role of Evolution in the Emergence of Infectious Diseases letters to nature whose fates have been followed since 1971. Tissue sampling for DNA analyses started in 18. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Massachusetts, Sinauer, 1988. Blood samples were taken from all captured sheep until 1993 and stored in Sunderland, 1998). preservative at 220 8C. Sampling resumed in 1997, when hair samples were taken from all 19. Hogg, J. T. & Forbes, S. H. Mating in bighorn sheep: frequent male reproduction via a high-risk captured sheep by plucking 50–100 hairs including roots from the back or flank. Hairs ‘unconventional’ tactic. Behav. Ecol. Sociobiol. 41, 33–48 (1997). were kept either in paper envelopes or plastic bags containing about 5 g of silica at room 20. Hendry, A. P. & Kinnison, M. T. Perspective: The pace of modern life: measuring rates of temperature. From 1998 to 2002, a tissue sample from each captured sheep was taken from contemporary microevolution. Evolution 53, 1637–1653 (1999). the ear with an 8-mm punch. Ear tissue was kept at 220 8C in a solution of 20% 21. Merila¨, J., Kruuk, L. E. B. & Sheldon, B. C. Cryptic evolution in a wild bird population. Nature 412, dimethylsulphoxide saturated with NaCl. We sampled 433 marked individuals over the 76–79 (2001). course of the study. 22. Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K. & Pemberton, J. M. Positive genetic DNAwas extracted from blood with a standard phenol–chloroform method, and from correlation between parasite resistance and body size in a free-living ungulate population. Evolution either 20–30 hairs including follicles or about 5 mg of ear tissue, using the QIAamp tissue 55, 2116–2125 (2001). extraction kit (Qiagen Inc., Mississauga, Ontario). Polymerase chain reaction 23. Jorgenson, J. T., Festa-Bianchet, M. & Wishart, W. D. Harvesting bighorn ewes—consequences for amplification at 20 ungulate-derived microsatellite loci, 15 as described previously5 plus population-size and trophy ram production. J. Wildl. Mgmt 57, 429–435 (1993). MCM527, BM4025, MAF64, OarFCB193 and MAF92 (refs 25, 26), and fragment analysis 24. Festa-Bianchet, M., Jorgenson, J. T., King, W. J., Smith, K. G. & Wishart, W. D. The development of were performed as described elsewhere5. After correction for multiple comparisons, we sexual dimorphism: seasonal and lifetime mass changes in bighorn sheep. Can. J. Zool. 74, 330–342 found no evidence for allelic or genotypic disequilibria at or among these 20 loci. (1996). Paternity of 241 individuals was assigned by using the likelihood-based approach 25. Crawford, A. M. et al. An autosomal genetic linkage map of the sheep genome. Genetics 140, 703–724 described in CERVUS27 at a confidence level of more than 95% with input parameters (1995). given in ref. 5. After paternity analysis, we used KINSHIP28 to identify 31 clusters of 104 26. Slate, J. et al. Bovine microsatellite loci are highly conserved in red deer (Cervus elaphus), sika deer paternal half-sibs among the unassigned offspring. A paternal half-sibship consisted of all (Cervus nippon) and Soay sheep (Ovis aries). Anim. Genet. 29, 307–315 (1998). pairs of individuals of unassigned paternity that were identified in the KINSHIP analysis as 27. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. Statistical confidence for likelihood-based having a likelihood ratio of the probability of a paternal half-sib relationship versus paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998). unrelated with an associated P , 0.05 (ref. 28). Members of reconstructed paternal half- 28. Goodnight, K. F. & Queller, D. C. Computer software for performing likelihood tests of pedigree sibships were assigned a common unknown paternal identity for the animal model relationship using genetic markers. Mol. Ecol. 8, 1231–1234 (1999). analyses. Paternal identity links in the pedigree were therefore defined for 345 individuals. 29. Groeneveld, E., Kovac, M., Wang, T. L. & Fernando, R. L. Computing algorithms in a general purpose BLUP package for multivariate prediction and estimation. Arch. Anim. Breed. 15, 399–412 (1992). 30. Groeneveld, E. User’s Guide: REML VCE, a Multivariate Multi-Model Restricted Maximum Likelihood Animal model analyses (Co)variance Estimation Package, Version 3.2 (Institute of Animal Husbandry and Animal Behaviour, Federal Research Center of Agriculture (FAL) (Mariensee, Germany, 1995). Breeding values, genetic variance components and heritabilities were estimated by using a multiple trait restricted-estimate maximum-likelihood (REML) model implemented by the programs PEST29 and VCE30. An animal model was fitted in which the phenotype of Acknowledgements We thank the many students, colleagues, volunteers and assistants that each animal was broken down into components of additive genetic value and other contributed to this research over the past 30 years. B. Wishart initiated the Ram Mountain project. random and fixed effects: y ¼ Xb þ Za þ Pc þ e, where y was a vector of phenotypic Our research was funded by the Alberta Conservation Association, Alberta Fish and Wildlife Division, Alberta Recreation, Sports, Parks and Wildlife Foundation, Eppley Foundation for values, b was a vector of fixed effects, a and c were vectors of additive genetic and Research, Foundation for North American Wild Sheep, National Geographic Society, Natural permanent environmental, e was a vector of residual values, and X, Z and P were the Environment Research Council (UK), Natural Sciences and Engineering Research Council of corresponding design matrices relating records to the appropriate fixed or random Canada, Rocky Mountain Elk Foundation (Canada), and the Universite´ de Sherbrooke. We are effects18. Fixed effects included age (factor) and the average weight of yearling ewes in the grateful for the logistical support of the Alberta Forest Service. year of measurement (covariate), which is a better index of resource availability than population size because it accounts for time-lagged effects4. The permanent environmental effect grouped repeated observations on the same individual to quantify Competing interests statement The authors declare that they have no competing financial any remaining between-individual variance over and above that due to additive genetic interests. effects, which would be due to maternal or other long-term environmental and non- additive genetic effects. Correspondence and requests for materials should be addressed to D.W.C. The total phenotypic variance (V p) was therefore partitioned into three components: (d.coltman@sheffield.ac.uk). the additive genetic variance (Va), the permanent environmental variance (Ve) and the 2 residual variance (Vr), thus: V p ¼ Va þ Ve þ Vr. Heritability was calculated as h ¼ Va/ 30 V p. The VCE program returns standard errors on all variance components and ratios. Best linear unbiased predictors of individual breeding values were quantified by using REML estimates of the variance components obtained with PEST29. All statistical tests .............................................................. were conducted in SPLUS 6.1. Received 11 August; accepted 17 October 2003; doi:10.1038/nature02177. Theroleofevolutioninthe 1. Thelen, T. H. Effects of harvest on antlers of simulated populations of elk. J. Wild. Mgmt 55, 243–249 (1991). emergence of infectious diseases 2. Harris, R. B., Wall, W. A. & Allendorf, F. W. Genetic consequences of hunting: what do we know and what should we do? Wildl. Soc. Bull. 30, 634–643 (2002). 1 1 2 3 3. Festa-Bianchet, M. in Animal Behavior and Wildlife Conservation (eds Apollonio, M. & Rustom Antia , Roland R. Regoes , Jacob C. Koella & Carl T. Bergstrom Festa-Bianchet, M.) 191–207 (Island Press, Washington DC, 2003). 4. Festa-Bianchet, M., Coltman, D. W., Turelli, L. & Jorgenson, J. T. Relative allocation to horn and body 1Department of Biology, Emory University, Atlanta, Georgia 30322, USA growth in bighorn rams varies with resource availability. Behav. Ecol. (in the press). 2Laboratoire de Parasitologie Evolutive, Universite´ Pierre et Marie Curie, 5. Coltman, D. W., Festa-Bianchet, M., Jorgenson, J. T. & Strobeck, C. Age-dependent sexual selection in 75252 Paris, France bighorn rams. Proc. R. Soc. Lond. B 269, 165–172 (2002). 3Department of Biology, University of Washington, Seattle, Washington 98195, 6. Milner-Gulland, E. J. et al. Conservation—reproductive collapse in saiga antelope harems. Nature 422, 135 (2003). USA 7. Marty, S. Sacrificial ram. Can. Geographic November/December, 37–50 (2002). ............................................................................................................................................................................. 8. Clutton-Brock, T. H., Coulson, T. N., Milner-Gulland, E. J., Thomson, D. & Armstrong, H. M. Sex It is unclear when, where and how novel pathogens such as differences in emigration and mortality affect optimal management of deer populations. Nature 415, human immunodeficiency virus (HIV), monkeypox and severe 633–637 (2002). 9. Ginsberg, J. R. & Milner Gulland, E. J. Sex-biased harvesting and population dynamics in ungulates— acute respiratory syndrome (SARS) will cross the barriers that implications for conservation and sustainable use. Conserv. Biol. 8, 157–166 (1994). separate their natural reservoirs from human populations and 10. Langvatn, R. & Loison, A. Consequences of harvesting on age structure, sex ratio and population ignite the epidemic spread of novel infectious diseases. New dynamics of red deer Cervus elaphus in central Norway. Wildl. Biol. 5,
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