{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:46:36Z","timestamp":1760028396500},"reference-count":57,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2014,6,13]],"date-time":"2014-06-13T00:00:00Z","timestamp":1402617600000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0100061","type":"journal-article","created":{"date-parts":[[2014,6,13]],"date-time":"2014-06-13T20:33:55Z","timestamp":1402691635000},"page":"e100061","update-policy":"http:\/\/dx.doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":11,"title":["Extreme Heterogeneity in Parasitism Despite Low Population Genetic Structure among Monarch Butterflies Inhabiting the Hawaiian Islands"],"prefix":"10.1371","volume":"9","author":[{"given":"Amanda A.","family":"Pierce","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacobus C.","family":"de Roode","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sonia","family":"Altizer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rebecca A.","family":"Bartel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2014,6,13]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.1364-3703.2010.00657.x","article-title":"Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease","volume":"12","author":"M Ravensdale","year":"2011","journal-title":"Molecular Plant Pathology"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.tree.2005.03.009","article-title":"Spatial epidemiology: an emerging (or re-emerging) discipline","volume":"20","author":"RS Ostfeld","year":"2005","journal-title":"Trends in Ecology & Evolution"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"3668","DOI":"10.1073\/pnas.042400799","article-title":"Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes","volume":"99","author":"DL Smith","year":"2002","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1046\/j.1523-1739.2003.01260.x","article-title":"Effect of forest fragmentation on Lyme disease risk","volume":"17","author":"BF Allan","year":"2003","journal-title":"Conservation Biology"},{"key":"ref5","first-page":"S1249","article-title":"Theoretical and empirical studies of metapopulations-population and genetic dynamics of the silene-usfilago system","volume":"73","author":"PH Thrall","year":"1995","journal-title":"Canadian Journal of Botany-Revue Canadienne De Botanique"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"743","DOI":"10.2307\/2960598","article-title":"Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial","volume":"85","author":"PH Thrall","year":"1997","journal-title":"Journal of Ecology"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1126\/science.1134695","article-title":"Large-scale spatial-transmission models of infectious disease","volume":"316","author":"S Riley","year":"2007","journal-title":"Science"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1890\/08-0208.1","article-title":"Habitat edges, within-patch dispersion of hosts, and parasitoid oviposition behavior","volume":"90","author":"JT Cronin","year":"2009","journal-title":"Ecology"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1038\/353255a0","article-title":"Spatial structure and chaos in insect population-dynamics","volume":"353","author":"MP Hassell","year":"1991","journal-title":"Nature"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1126\/science.1194694","article-title":"Animal migration and infectious disease risk","volume":"331","author":"S Altizer","year":"2011","journal-title":"Science"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1002\/jwmg.40","article-title":"Spread of Plague Among Black-Tailed Prairie Dogs Is Associated With Colony Spatial Characteristics","volume":"75","author":"TL Johnson","year":"2011","journal-title":"Journal of Wildlife Management"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"2423","DOI":"10.1139\/z91-340","article-title":"Parasite avoidance: the cause of post-valing migrations in <italic>Rangifer<\/italic>?","volume":"69","author":"I Folstad","year":"1991","journal-title":"Canadian Journal of Zoology"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1890\/10-0489.1","article-title":"Monarch butterfly migration and parasite transmission in eastern North America","volume":"92","author":"RA Bartel","year":"2011","journal-title":"Ecology"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1111\/j.0030-1299.2006.13292.x","article-title":"Disease dynamics, host specificity and pathogen persistence in isolated host populations","volume":"112","author":"U Carlsson-Graner","year":"2006","journal-title":"Oikos"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1034\/j.1600-0706.2002.970110.x","article-title":"The spatial distribution of plant populations, disease dynamics and evolution of resistance","volume":"97","author":"U Carlsson-Graner","year":"2002","journal-title":"Oikos"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"2216","DOI":"10.1098\/rspb.2010.1978","article-title":"Host resistance and coevolution in spatially structured populations","volume":"278","author":"A Best","year":"2011","journal-title":"Proceedings of the Royal Society B-Biological Sciences"},{"key":"ref17","unstructured":"Ackery PR, Vane-Wright RI (1984) Milkweed Butterflies: their Cladistics and Biology. Ithaca, NY: Cornell University Press."},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1759","DOI":"10.1139\/z78-240","article-title":"Autumnal migration routes of the eastern population of the monarch butterfly (<italic>Danaus p. plexippus<\/italic> L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico","volume":"56","author":"FA Urquhart","year":"1978","journal-title":"Canadian Journal of Zoology"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1093\/icb\/31.1.265","article-title":"Animal migrations-endangered phenomena","volume":"31","author":"LP Brower","year":"1991","journal-title":"American Zoologist"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1111\/j.1095-8312.2004.00322.x","article-title":"Monarchs across the Pacific: the Columbus hypothesis revisited","volume":"82","author":"MP Zalucki","year":"2004","journal-title":"Biological Journal of the Linnean Society"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1046\/j.1095-8312.2002.00034.x","article-title":"Genetic differentiation between Australian and North American populations of the monarch butterfly <italic>Danaus plexippus<\/italic> (L.) (Lepidoptera: Nymphalidae): an exploration using allozyme electrophoresis","volume":"75","author":"JM Shephard","year":"2002","journal-title":"Biological Journal of the Linnean Society"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1111\/j.1558-5646.2010.00946.x","article-title":"Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology","volume":"64","author":"S Altizer","year":"2010","journal-title":"Evolution"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"3433","DOI":"10.1111\/j.1365-294X.2012.05613.x","article-title":"Lack of genetic differentiation between monarch butterflies with divergent migration destinations","volume":"21","author":"JI Lyons","year":"2012","journal-title":"Molecular Ecology"},{"key":"ref24","unstructured":"Altizer S, De Roode JC (2013) Monarch defense against a debilitating parasite: resistance, immunity and self-medication. In: Oberhauser K, Altizer S, Nail KR, editors. Monarchs in a Changing World: Biology and Conservation of an Iconic Insect: Cornell University. pp. <italic>In press<\/italic>."},{"key":"ref25","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1006\/jipa.1996.4634","article-title":"Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha","volume":"69","author":"KLH Leong","year":"1997","journal-title":"Journal of Invertebrate Pathology"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1046\/j.1365-2311.2000.00246.x","article-title":"Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies","volume":"25","author":"SM Altizer","year":"2000","journal-title":"Ecological Entomology"},{"key":"ref27","first-page":"49","article-title":"Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies","volume":"73","author":"KLH Leong","year":"1997","journal-title":"Pan-Pacific Entomologist"},{"key":"ref28","unstructured":"Altizer SM, Oberhauser K, Geurts KA (2004) Transmission of the protozoan parasite, Ophryocystis elektroscirrha, in monarch butterfly populations. In: Solensky KOaM, editor. The Monarch Butterfly: Biology and Conservation. Ithaca, New York: Cornell University Press. 203\u2013218."},{"key":"ref29","doi-asserted-by":"crossref","unstructured":"McLaughlin RE, Myers J (1970) <italic>Ophryocystis elektroscirrha<\/italic> sp. n., a neogregarine pathogen of the monarch butterfly <italic>Danaus plexippus<\/italic> (L.) and the Florida queen butterfly <italic>D. gilippus berenice<\/italic> Cramer. Journal of Protozoology 17: 300-&amp;.","DOI":"10.1111\/j.1550-7408.1970.tb02375.x"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1017\/S0031182006002009","article-title":"Virulence determinants in a natural butterfly-parasite system","volume":"134","author":"JC de Roode","year":"2007","journal-title":"Parasitology"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1006\/jipa.1999.4853","article-title":"Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus)","volume":"74","author":"SM Altizer","year":"1999","journal-title":"Journal of Invertebrate Pathology"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1111\/j.1461-0248.2005.00722.x","article-title":"Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts","volume":"8","author":"CA Bradley","year":"2005","journal-title":"Ecology Letters"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.2307\/2640828","article-title":"Parasite-mediated selection against inbred Soay sheep in a free-living, island population","volume":"53","author":"DW Coltman","year":"1999","journal-title":"Evolution"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"3523","DOI":"10.1098\/rspb.2009.1001","article-title":"Hookworm infection, anaemia and genetic variability of the New Zealand sea lion","volume":"276","author":"K Acevedo-Whitehouse","year":"2009","journal-title":"Proceedings of the Royal Society B-Biological Sciences"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.livsci.2011.10.009","article-title":"Preliminary association of microsatellite heterozygosity with footrot in domestic sheep","volume":"143","author":"EM Smith","year":"2012","journal-title":"Livestock Science"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1098\/rspb.2010.1550","article-title":"Genetic diversity, parasite prevalence and immunity in wild bumblebees","volume":"278","author":"PR Whitehorn","year":"2011","journal-title":"Proceedings of the Royal Society B-Biological Sciences"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1163\/156853982X00346","article-title":"The analysis and description of movement in adult <italic>Danaus plexippus<\/italic> L (Lepidotera, Danaiae)","volume":"80","author":"MP Zalucki","year":"1982","journal-title":"Behaviour"},{"key":"ref38","first-page":"233","article-title":"Time, temperature, and latitudinal constraints on the annual recolonization of eastern North America by the monarch butterfly","volume":"0","author":"BJ Cockrell","year":"1993","journal-title":"Natural History Museum of Los Angeles County Science Series"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s00442-009-1361-6","article-title":"Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus)","volume":"161","author":"JC de Roode","year":"2009","journal-title":"Oecologia"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1111\/j.1755-0998.2010.02847.x","article-title":"Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows","volume":"10","author":"L Excoffier","year":"2010","journal-title":"Molecular Ecology Resources"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"223","DOI":"10.2307\/2409177","article-title":"Analyzing tables of statistical tests","volume":"43","author":"WR Rice","year":"1989","journal-title":"Evolution"},{"key":"ref42","unstructured":"Hood GM (2010) PopTools version 3.2.5."},{"key":"ref43","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1111\/j.1471-8286.2007.01931.x","article-title":"GENEPOP \u2018007: a complete re-implementation of the GENEPOP software for Windows and Linux","volume":"8","author":"F Rousset","year":"2008","journal-title":"Molecular Ecology Resources"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1093\/bioinformatics\/btn478","article-title":"ADZE: a rarefaction approach for counting alleles private to combinations of","volume":"24","author":"Z Szpiech","year":"2008","journal-title":"Bioinformatics"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1093\/genetics\/155.2.945","article-title":"Inference of population structure using multilocus genotype data","volume":"155","author":"JK Pritchard","year":"2000","journal-title":"Genetics"},{"key":"ref46","first-page":"179","article-title":"The Columbus hypothesis: An explantation for the dramatic 19th century range expansion of the monarch butterfly","volume":"0","author":"RI Vane-Wright","year":"1993","journal-title":"Natural History Museum of Los Angeles County Science Series"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1093\/genetics\/139.1.457","article-title":"A measure of population subdivision based on microsatellite allele frequencies","volume":"139","author":"M Slatkin","year":"1995","journal-title":"Genetics"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1046\/j.0962-1083.2001.01436.x","article-title":"The estimation of population differentiation with microsatellite markers","volume":"11","author":"F Balloux","year":"2002","journal-title":"Molecular Ecology"},{"key":"ref49","unstructured":"Oksanen JF, Blanchet FG, Kindt R, Legendre P, Minchin PR, <etal>et al<\/etal>.. (2011) vegan: Community Ecology Package. R package version 2.0-0. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/CRANR-projectorg\/package=vegan\" xlink:type=\"simple\">http:\/\/CRANR-projectorg\/package=vegan<\/ext-link>."},{"key":"ref50","unstructured":"Real LA, Childs JE (2005) Spatial-temporal dynamics of rabies in ecological communities. In: Ray SKCaC, editor. Disease Ecology: Community Structure and Pathogen Dynamics. Oxford: Oxford University Press. 168\u2013185."},{"key":"ref51","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.1890\/09-1225.1","article-title":"Persistence of canine distemper virus in the Greater Yellowstone Ecosystem\u2019s carnivore community","volume":"20","author":"ES Almberg","year":"2010","journal-title":"Ecological Applications"},{"key":"ref52","doi-asserted-by":"crossref","unstructured":"Hess G, Randolph S, Arneberg P, Chemini C, Furlanello C, <etal>et al<\/etal>.. (2002) Spatial aspects of disease dynamics. In: P. Hudson AR, B. T Grenfell, H Heesterbeek, and A. P Dobson, editor. Ecology of Wildlife Diseases. Oxford: Oxford University Press. 102\u2013119.","DOI":"10.1093\/oso\/9780198506201.003.0006"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/j.1095-8312.1991.tb00548.x","article-title":"Metapopulation dynamics- brief history and conceptual domain","volume":"42","author":"I Hanski","year":"1991","journal-title":"Biological Journal of the Linnean Society"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"1617","DOI":"10.2307\/2265556","article-title":"Disease in metapopulation models: Implications for conservation","volume":"77","author":"G Hess","year":"1996","journal-title":"Ecology"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"2041","DOI":"10.1098\/rspb.2002.2079","article-title":"Disease, habitat fragmentation and conservation","volume":"269","author":"H McCallum","year":"2002","journal-title":"Proceedings of the Royal Society of London Series B-Biological Sciences"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1098\/rspb.2001.1667","article-title":"Disease in endangered metapopulations: the importance of alternative hosts","volume":"269","author":"J Gog","year":"2002","journal-title":"Proceedings of the Royal Society B-Biological Sciences"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1007\/s10682-008-9258-0","article-title":"Sex differences in immune defenses and response to parasitism in monarch butterflies","volume":"23","author":"E Lindsey","year":"2009","journal-title":"Evolutionary Ecology"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0100061","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,27]],"date-time":"2024-05-27T18:51:58Z","timestamp":1716835918000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0100061"}},"subtitle":[],"editor":[{"given":"Patrick","family":"O\u2019Grady","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2014,6,13]]},"references-count":57,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2014,6,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0100061","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,6,13]]}}}