Extreme Heterogeneity in Parasitism Despite Low Population Genetic Structure among Monarch Butterflies Inhabiting the Hawaiian Islands

Host movement and spatial structure can strongly influence the ecology and evolution of infectious diseases, with limited host movement potentially leading to high spatial heterogeneity in infection. Monarch butterflies (Danaus plexippus) are best known for undertaking a spectacular long-distance migration in eastern North America; however, they also form non-migratory populations that breed year-round in milder climates such as Hawaii and other tropical locations. Prior work showed an inverse relationship between monarch migratory propensity and the prevalence of the protozoan parasite, Ophryocystis elektroscirrha. Here, we sampled monarchs from replicate sites within each of four Hawaiian Islands to ask whether these populations show consistently high prevalence of the protozoan parasite as seen for monarchs from several other non-migratory populations. Counter to our predictions, we observed striking spatial heterogeneity in parasite prevalence, with infection rates per site ranging from 4–85%. We next used microsatellite markers to ask whether the observed variation in infection might be explained by limited host movement and spatial sub-structuring among sites. Our results showed that monarchs across the Hawaiian Islands form one admixed population, supporting high gene flow among sites. Moreover, measures of individual-level genetic diversity did not predict host infection status, as might be expected if more inbred hosts harbored higher parasite loads. These results suggest that other factors such as landscape-level environmental variation or colonization-extinction processes might instead cause the extreme heterogeneity in monarch butterfly infection observed here.

[1]  Seth M. Barribeau,et al.  Lack of genetic differentiation between monarch butterflies with divergent migration destinations , 2012, Molecular ecology.

[2]  L. Green,et al.  Preliminary association of microsatellite heterozygosity with footrot in domestic sheep , 2012 .

[3]  S. Webb,et al.  Host resistance and coevolution in spatially structured populations , 2011, Proceedings of the Royal Society B: Biological Sciences.

[4]  D. Goulson,et al.  Genetic diversity, parasite prevalence and immunity in wild bumblebees , 2011, Proceedings of the Royal Society B: Biological Sciences.

[5]  J. Cully,et al.  Spread of Plague Among Black-Tailed Prairie Dogs is Associated with Colony Spatial Characteristics , 2011 .

[6]  S. Altizer,et al.  Monarch butterfly migration and parasite transmission in eastern North America , 2011, Ecology.

[7]  Barbara A. Han,et al.  Animal Migration and Infectious Disease Risk , 2011, Science.

[8]  P. Cross,et al.  Persistence of canine distemper virus in the Greater Yellowstone ecosystem's carnivore community. , 2010, Ecological applications : a publication of the Ecological Society of America.

[9]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[10]  A. K. Davis,et al.  Populations of Monarch butterflies with different migratory behaviors show divergence in wing morphology. , 2010, Evolution; international journal of organic evolution.

[11]  P. Duignan,et al.  Hookworm infection, anaemia and genetic variability of the New Zealand sea lion , 2009, Proceedings of the Royal Society B: Biological Sciences.

[12]  S. Altizer,et al.  Sex differences in immune defenses and response to parasitism in monarch butterflies , 2009, Evolutionary Ecology.

[13]  S. Altizer,et al.  Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus) , 2009, Oecologia.

[14]  Noah A. Rosenberg,et al.  ADZE: a rarefaction approach for counting alleles private to combinations of populations , 2008, Bioinform..

[15]  Xia Li,et al.  Towards patterns tree of gene coexpression in eukaryotic species , 2008, Bioinform..

[16]  F. Rousset genepop’007: a complete re‐implementation of the genepop software for Windows and Linux , 2008, Molecular ecology resources.

[17]  C. O'Brien Disease Ecology: Community Structure and Pathogen Dynamics , 2007 .

[18]  S. Riley Large-Scale Spatial-Transmission Models of Infectious Disease , 2007, Science.

[19]  S. Altizer,et al.  Virulence determinants in a natural butterfly-parasite system , 2006, Parasitology.

[20]  R. Ostfeld,et al.  Spatial epidemiology: an emerging (or re-emerging) discipline. , 2005, Trends in ecology & evolution.

[21]  S. Altizer,et al.  Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts , 2005 .

[22]  Karen S. Oberhauser,et al.  The Monarch Butterfly: Biology and Conservation , 2004 .

[23]  A. Clarke,et al.  Monarchs across the Pacific: the Columbus hypothesis revisited , 2004 .

[24]  A. Dobson,et al.  Disease, habitat fragmentation and conservation , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  J. Gog,et al.  Disease in endangered metapopulations: the importance of alternative hosts , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  M. Zalucki,et al.  Genetic differentiation between Australian and North American populations of the monarch butterfly Danaus plexippus (L.) (Lepidoptera: Nymphalidae): an exploration using allozyme electrophoresis , 2002 .

[27]  P. Thrall,et al.  The spatial distribution of plant populations, disease dynamics and evolution of resistance , 2002 .

[28]  David L Smith,et al.  Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  F. Balloux,et al.  The estimation of population differentiation with microsatellite markers , 2002, Molecular ecology.

[30]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[31]  S. Altizer,et al.  Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies , 2000 .

[32]  D. Coltman,et al.  PARASITE‐MEDIATED SELECTION AGAINST INBRED SOAY SHEEP IN A FREE‐LIVING ISLAND POPULATON , 1999, Evolution; international journal of organic evolution.

[33]  S. Altizer,et al.  Effects of the protozoan parasite ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus) , 1999, Journal of invertebrate pathology.

[34]  J. Burdon,et al.  Host-pathogen dynamics in a metapopulation context:the ecological and evolutionary consequences of being spatial , 1997 .

[35]  G. Hess Disease in Metapopulation Models: Implications for Conservation , 1996 .

[36]  P. Thrall,et al.  Theoretical and empirical studies of metapopulations: population and genetic dynamics of the Silene–Ustilago system , 1995 .

[37]  Michael P. Hassell,et al.  Spatial structure and chaos in insect population dynamics , 1991, Nature.

[38]  I. Folstad,et al.  Parasite avoidance: the cause of post-calving migrations in Rangifer? , 1991 .

[39]  Lincoln P. Brower,et al.  Animal Migrations: Endangered Phenomena , 1991 .

[40]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[41]  R. Vane‐Wright,et al.  Milkweed Butterflies: Their Cladistics and Biology , 1984 .

[42]  F. A. Urquhart,et al.  Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico , 1978 .

[43]  J. Myers,et al.  Ophryocystis elektroscirrha sp. n., a Neogregarine Pathogen of the Monarch Butterfly Danaus plexippus (L.) and the Florida Queen Butterfly D. gilippus berenice Cramer1 , 1970 .

[44]  P. Dodds,et al.  Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. , 2011, Molecular plant pathology.

[45]  ichard,et al.  THE EFFECT OF FOREST FRAGMENTATION ON LYME DISEASE RISK , 2011 .

[46]  J. Cronin Habitat edges, within-patch dispersion of hosts, and parasitoid oviposition behavior. , 2009, Ecology.

[47]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[48]  S. Altizer,et al.  Transmission of the Protozoan Parasite Ophryocystis elektroscirrha in Monarch Butterfly Populations : Implications for Prevalence and Population-Level Impacts , 2007 .

[49]  U. Carlsson-Granér Disease dynamics, host specificity and pathogen persistence in isolated host populations , 2006 .

[50]  Sharon K. Collinge,et al.  Spatial-temporal dynamics of rabies in ecological communities. , 2006 .

[51]  Peter J. Hudson,et al.  The ecology of wildlife diseases , 2002 .

[52]  H. Kaya,et al.  Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. , 1997, Journal of invertebrate pathology.

[53]  H. Kaya,et al.  Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies , 1997 .

[54]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[55]  R. Vane-Wright,et al.  The Columbus hypothesis: an explanation for the dramatic 19th century range expansion of the monarch butterfly , 1993 .

[56]  L. Brower,et al.  Time, temperature, and latitudinal constraints on the annual recolonization of eastern North America by the monarch butterfly , 1993 .

[57]  M. Gilpin,et al.  Metapopulation dynamics: a brief his-tory and conceptual domain , 1991 .

[58]  Myron P. Zalucki,et al.  The Analysis and Description of Movement in Adult Danaus Plexippus L. (Lepidoptera: Danainae) , 1982 .