{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T08:46:40Z","timestamp":1789634800424,"version":"4.0.0"},"reference-count":71,"publisher":"The Royal Society","issue":"1783","license":[{"start":{"date-parts":[[2014,5,22]],"date-time":"2014-05-22T00:00:00Z","timestamp":1400716800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Proc. R. Soc. B."],"published-print":{"date-parts":[[2014,5,22]]},"abstract":"<jats:p>Pathogen evasion of the host immune system is a key force driving extreme polymorphism in genes of the major histocompatibility complex (MHC). Although this gene family is well characterized in structure and function, there is still much debate surrounding the mechanisms by which MHC diversity is selectively maintained. Many studies have investigated relationships between MHC variation and specific pathogens, and have found mixed support for and against the hypotheses of heterozygote advantage, frequency-dependent or fluctuating selection. Few, however, have focused on the selective effects of multiple parasite types on host immunogenetic patterns. Here, we examined relationships between variation in the equine MHC gene, ELA<jats:italic>-DRA<\/jats:italic>, and both gastrointestinal (GI) and ectoparasitism in plains zebras (<jats:italic>Equus quagga<\/jats:italic>). Specific alleles present at opposing population frequencies had antagonistic effects, with rare alleles associated with increased GI parasitism and common alleles with increased tick burdens. These results support a frequency-dependent mechanism, but are also consistent with fluctuating selection. Maladaptive GI parasite \u2018susceptibility alleles\u2019 were reduced in frequency, suggesting that these parasites may play a greater selective role at this locus. Heterozygote advantage, in terms of allele mutational divergence, also predicted decreased GI parasite burden in genotypes with a common allele. We conclude that an immunogenetic trade-off affects resistance\/susceptibility to parasites in this system. Because GI and ectoparasites do not directly interact within hosts, our results uniquely show that antagonistic parasite interactions can be indirectly modulated through the host immune system. This study highlights the importance of investigating the role of multiple parasites in shaping patterns of host immunogenetic variation.<\/jats:p>","DOI":"10.1098\/rspb.2014.0077","type":"journal-article","created":{"date-parts":[[2014,4,9]],"date-time":"2014-04-09T09:20:57Z","timestamp":1397035257000},"page":"20140077","update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":30,"title":["Parasite-mediated selection drives an immunogenetic trade-off in plains zebras (<i>Equus quagga<\/i>)"],"prefix":"10.1098","volume":"281","author":[{"given":"Pauline L.","family":"Kamath","sequence":"first","affiliation":[{"name":"US Geological Survey, Northern Rocky Mountain Science Center, 2327 University Way, Bozeman, MT 59715, USA"},{"name":"Department of Environmental Science, Policy, and Management, University of California, 130 Mulford Hall No. 3114, Berkeley, CA 94720, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wendy C.","family":"Turner","sequence":"additional","affiliation":[{"name":"Department of Environmental Science, Policy, and Management, University of California, 130 Mulford Hall No. 3114, Berkeley, CA 94720, USA"},{"name":"Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, PO Box 1066 Blindern, Oslo 0361, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"K\u00fcsters","sequence":"additional","affiliation":[{"name":"Berkeley Etosha Anthrax Research Project, Swakopmund, Namibia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wayne M.","family":"Getz","sequence":"additional","affiliation":[{"name":"Department of Environmental Science, Policy, and Management, University of California, 130 Mulford Hall No. 3114, Berkeley, CA 94720, USA"},{"name":"School of Mathematical Sciences, University of KwaZulu-Natal, Private Bag X54001, 14, Durban 4000, South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2014,5,22]]},"reference":[{"key":"e_1_3_5_2_2","first-page":"68","article-title":"Disease and evolution","volume":"19","author":"Haldane JBS","year":"1949","journal-title":"Ric. Sci. Suppl. A."},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182000055360"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0952-7915(02)00381-3"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(99)01814-5"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2006.05.010"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-5347(98)01416-5"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/256050a0"},{"key":"e_1_3_5_9_2","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1093\/genetics\/124.4.967","article-title":"Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci","volume":"124","author":"Takahata N","year":"1990","journal-title":"Genetics"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1186\/1742-9994-2-1"},{"key":"e_1_3_5_11_2","first-page":"205","volume-title":"Genetics, evolution, and society","author":"Hedrick P","year":"2000"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2005.04.050"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/352595a0"},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2005.tb01002.x"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.7.3714"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msi112"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2009.04476.x"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0037101"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2012.01799.x"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2010.1968"},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1106893108"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2009.0011"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2009.2084"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2002.tb00116.x"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.71.4.2079-2086.2003"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2009.04374.x"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2008.1525"},{"key":"e_1_3_5_28_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02918202"},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1461-0248.2007.01141.x"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10682-012-9611-1"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.2307\/3272160"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182000044760"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1894\/0038-4909(2005)050<0057:MEPIIP>2.0.CO;2"},{"key":"e_1_3_5_34_2","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/978-3-642-68786-0_6","volume-title":"Ecology of tropical savannas","author":"Huntley BJ","year":"1982"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1645\/GE-3353"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-46.4.1108"},{"key":"e_1_3_5_37_2","volume-title":"Georgis\u2019 parasitology for veterinarians","author":"Bowman DD","year":"2003","edition":"8"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0737-0806(88)80110-2"},{"key":"e_1_3_5_39_2","first-page":"306","volume-title":"Equine Infectious Diseases VIII: Proc. of the Eighth Int. Conf.","author":"Dwinger RH","year":"1999"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1890\/ES12-00245.1"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00251-009-0380-0"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-11-128"},{"key":"e_1_3_5_43_2","doi-asserted-by":"publisher","DOI":"10.1093\/jhered\/90.1.35"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1007\/s002510050452"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0050971"},{"key":"e_1_3_5_46_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0254-6299(16)31355-2"},{"key":"e_1_3_5_47_2","first-page":"103","article-title":"Age determination in Burchells zebra Equus burchelli antiquorum from the Kruger National Park","volume":"4","author":"Smuts GL","year":"1974","journal-title":"J. South. Afr. Wildl. Manage. Assoc."},{"key":"e_1_3_5_48_2","first-page":"50","article-title":"A new technique for counting nematode eggs in sheep faeces","volume":"12","author":"Gordon HM","year":"1939","journal-title":"J. Counc. Sci. Ind. Res. Melbourne"},{"key":"e_1_3_5_49_2","volume-title":"The RVC\/FAO guide to veterinary diagnostic parasitology: faecal examination of farm animals for helminth parasites","author":"Gibbons LM","year":"2005"},{"key":"e_1_3_5_50_2","first-page":"1259","article-title":"Parasite-mediated selection against inbred Soay sheep in a free-living, island population","volume":"53","author":"Coltman DW","year":"1999","journal-title":"Evolution"},{"key":"e_1_3_5_51_2","first-page":"71","article-title":"Studies on the parasites of zebras. V. Nematodes of the Burchell and Hartmann mountain zebras from the Etosha National Park, South West Africa\/Namibia.","volume":"54","author":"Krecek RC","year":"1987","journal-title":"Onderstepoort J. Vet. Res."},{"key":"e_1_3_5_52_2","unstructured":"Drummond A et al. 2010 Geneious v. 5.0. See http:\/\/www.geneious.com. (accessed 1 November 2012)."},{"key":"e_1_3_5_53_2","doi-asserted-by":"publisher","DOI":"10.1086\/319501"},{"key":"e_1_3_5_54_2","doi-asserted-by":"publisher","DOI":"10.1093\/biomet\/73.1.13"},{"key":"e_1_3_5_55_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-0-387-87458-6"},{"key":"e_1_3_5_56_2","first-page":"xiii + 222","volume-title":"Generalized estimating equations","author":"Hardin JW","year":"2003"},{"key":"e_1_3_5_57_2","unstructured":"Turner WC. 2009 The ecology of orally ingested parasites in ungulates of Etosha National Park. PhD University of California at Berkeley Berkeley CA."},{"key":"e_1_3_5_58_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0006-341X.2001.00120.x"},{"key":"e_1_3_5_59_2","volume-title":"Model selection and multimodel inference: a practical information-theoretic approach","author":"Burnham K","year":"2002"},{"key":"e_1_3_5_60_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-0258(20000530)19:10<1265::AID-SIM486>3.0.CO;2-U"},{"key":"e_1_3_5_61_2","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1214\/aos\/1013699998","article-title":"The control of the false discovery rate in multiple testing under dependency","volume":"29","author":"Benjamini Y","year":"2001","journal-title":"Ann. Stat."},{"key":"e_1_3_5_62_2","volume-title":"R: a language and environment for statistical computing","author":"R Development Core Team","year":"2011"},{"key":"e_1_3_5_63_2","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v015.i02"},{"key":"e_1_3_5_64_2","doi-asserted-by":"crossref","unstructured":"Zuur AF Ieno EN Walker N Saveliev AA& Smith GM. 2009 Mixed effects models and extensions in ecology with R. New York NY: Springer.","DOI":"10.1007\/978-0-387-87458-6"},{"key":"e_1_3_5_65_2","unstructured":"Carey V. 2004 yags: yet another GEE solver. R package version 4.0-2.2. See http:\/\/www.biostat.harvard.edu\/\u223ccarey."},{"key":"e_1_3_5_66_2","first-page":"253","article-title":"Arthropod parasites of springbok, gemsbok, kudus, giraffes and Burchell and Hartmann zebras in the Etosha and Hardap Nature-Reserves, Namibia","volume":"59","author":"Horak IG","year":"1992","journal-title":"Onderstepoort J. Vet. Res."},{"key":"e_1_3_5_67_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.107.074815"},{"key":"e_1_3_5_68_2","first-page":"145","article-title":"Parasites of domestic and wild animals in South-Africa.17. Arthropod parasites of Burchell zebra, Equus burchelli, in the Eastern Transvaal Lowveld","volume":"51","author":"Horak IG","year":"1984","journal-title":"Onderstepoort J. Vet. Res."},{"key":"e_1_3_5_69_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2003.2635"},{"key":"e_1_3_5_70_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1112633109"},{"key":"e_1_3_5_71_2","first-page":"425","article-title":"Experimental studies of pleiotropy and epistasis in Escherichia coli 0.1. Variation in competitive fitness among mutants resistant to virus T4","volume":"42","author":"Lenski RE","year":"1988","journal-title":"Evolution"},{"key":"e_1_3_5_72_2","first-page":"392","volume-title":"Plant resistance to herbivores and pathogens","author":"Simms EL","year":"1992"}],"container-title":["Proceedings of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2014.0077","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rspb.2014.0077","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rspb.2014.0077","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,1]],"date-time":"2022-04-01T04:31:04Z","timestamp":1648787464000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rspb.2014.0077"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,5,22]]},"references-count":71,"journal-issue":{"issue":"1783","published-print":{"date-parts":[[2014,5,22]]}},"alternative-id":["10.1098\/rspb.2014.0077"],"URL":"https:\/\/doi.org\/10.1098\/rspb.2014.0077","relation":{},"ISSN":["0962-8452","1471-2954"],"issn-type":[{"value":"0962-8452","type":"print"},{"value":"1471-2954","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,5,22]]},"assertion":[{"value":"2014-01-14","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2014-03-17","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2014-05-22","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}