Extreme heterogeneity in parasitism despite low population genetic structure among monarch butterflies inhabiting the Hawaiian Islands

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Pierce, Amanda A ^a   De Roode, Jacobus C ^a   Altizer, Sonia ^b   Bartel, Rebecca A ^b,c  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c Red Wolf Recovery Program   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL TISSUE; ARTICLE; BUTTERFLY; DANAUS PLEXIPPUS; ENVIRONMENTAL FACTOR; FEMALE; GENE FLOW; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; LANDSCAPE; MALE; NONHUMAN; OPHRYOCYSTIS ELEKTROSCIRRHA; PARASITE LOAD; PARASITE TRANSMISSION; PARASITISM; POPULATION DYNAMICS; POPULATION GENETICS; POPULATION STRUCTURE; PROTOZOON; SPECIES EXTINCTION; UNITED STATES; ANIMAL; GENETICS; HOST PARASITE INTERACTION; PARASITOLOGY; POPULATION MIGRATION; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL; TRANSMISSION;

MICROSATELLITE DNA;

ANIMAL MIGRATION; ANIMALS; BUTTERFLIES; FEMALE; GENETIC HETEROGENEITY; GENETIC VARIATION; GENETICS, POPULATION; HAWAII; HOST-PARASITE INTERACTIONS; MALE; MICROSATELLITE REPEATS; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL;

EID: 84902793223     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100061     Document Type: Article

References (57)

1. Ravensdale M, Nemri A, Thrall PH, Ellis JG, Dodds PN (2011) Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Molecular Plant Pathology 12: 93-102.
2. Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology & Evolution 20: 328-336. (Pubitemid 40772080)
3. Smith DL, Lucey B, Waller LA, Childs JE, Real LA (2002) Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. Proceedings of the National Academy of Sciences of the United States of America 99: 3668-3672. (Pubitemid 34252164)
4. Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17: 267-272. (Pubitemid 36234419)
5. Thrall PH, Antonovics J (1995) Theoretical and empirical studies of metapopulations-population and genetic dynamics of the silene-usfilago system. Canadian Journal of Botany-Revue Canadienne De Botanique 73: S1249-S1258. (Pubitemid 26452717)
6. Thrall PH, Burdon JJ (1997) Host-pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial. Journal of Ecology 85: 743-753. (Pubitemid 28000546)
7. Riley S (2007) Large-scale spatial-transmission models of infectious disease. Science 316: 1298-1301.
8. Cronin JT (2009) Habitat edges, within-patch dispersion of hosts, and parasitoid oviposition behavior. Ecology 90: 196-207.
9. Hassell MP, Comins HN, May RM (1991) Spatial structure and chaos in insect population-dynamics. Nature 353: 255-258. (Pubitemid 21896765)
10. Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331: 296-302.
11. Johnson TL, Cully JF, Collinge SK, Ray C, Frey CM, et al. (2011) Spread of Plague Among Black-Tailed Prairie Dogs Is Associated With Colony Spatial Characteristics. Journal of Wildlife Management 75: 357-368.
12. Folstad I, Nilssen AC, Halvorsen O, Andersen J (1991) Parasite avoidance: the cause of post-valing migrations in Rangifer? Canadian Journal of Zoology 69: 2423-2429.
13. Bartel RA, Oberhauser KS, de Roode JC, Altizer SM (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92: 342-351.
14. Carlsson-Graner U (2006) Disease dynamics, host specificity and pathogen persistence in isolated host populations. Oikos 112: 174-184.
15. Carlsson-Graner U, Thrall PH (2002) The spatial distribution of plant populations, disease dynamics and evolution of resistance. Oikos 97: 97-110. (Pubitemid 34589526)
16. Best A, Webb S, White A, Boots M (2011) Host resistance and coevolution in spatially structured populations. Proceedings of the Royal Society B-Biological Sciences 278: 2216-2222.
17. Ackery PR, Vane-Wright RI (1984) Milkweed Butterflies: their Cladistics and Biology. Ithaca, NY: Cornell University Press.
18. Urquhart FA, Urquhart NR (1978) 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. Canadian Journal of Zoology 56: 1759-1764.
19. Brower LP, Malcolm SB (1991) Animal migrations-endangered phenomena. American Zoologist 31: 265-276.
20. Zalucki MP, Clarke AR (2004) Monarchs across the Pacific: the Columbus hypothesis revisited. Biological Journal of the Linnean Society 82: 111-121. (Pubitemid 38653711)
21. Shephard JM, Hughes JM, Zalucki MP (2002) Genetic differentiation between Australian and North American populations of the monarch butterfly Danaus plexippus (L.) (Lepidoptera: Nymphalidae): an exploration using allozyme electrophoresis. Biological Journal of the Linnean Society 75: 437-452.
22. Altizer S, Davis AK (2010) Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology. Evolution 64: 1018-1028.
23. Lyons JI, Pierce AA, Barribeau SM, Sternberg ED, Mongue AJ, et al. (2012) Lack of genetic differentiation between monarch butterflies with divergent migration destinations. Molecular Ecology 21: 3433-3444.
24. 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. In press.
25. Leong KLH, Yoshimura MA, Kaya HK, Williams H (1997) Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. Journal of Invertebrate Pathology 69: 79-83. (Pubitemid 127346222)
26. Altizer SM, Oberhauser KS, Brower LP (2000) Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Entomology 25: 125-139. (Pubitemid 30301882)
27. Leong KLH, Yoshimura MA, Kaya HK (1997) Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies. Pan-Pacific Entomologist 73: 49-51. (Pubitemid 127033139)
28. 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. 203-218.
29. McLaughlin RE, Myers J (1970) Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of the monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. Journal of Protozoology 17: 300-&.
30. de Roode JC, Gold LR, Altizer S (2007) Virulence determinants in a natural butterfly-parasite system. Parasitology 134: 657-668. (Pubitemid 46841601)
31. Altizer SM, Oberhauser KS (1999) Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). Journal of Invertebrate Pathology 74: 76-88. (Pubitemid 129498901)
32. Bradley CA, Altizer S (2005) Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8: 290-300. (Pubitemid 40393914)
33. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53: 1259-1267. (Pubitemid 29416966)
34. Acevedo-Whitehouse K, Petetti L, Duignan P, Castinel A (2009) Hookworm infection, anaemia and genetic variability of the New Zealand sea lion. Proceedings of the Royal Society B-Biological Sciences 276: 3523-3529.
35. Smith EM, Hoffman JI, Green LE, Amos W (2012) Preliminary association of microsatellite heterozygosity with footrot in domestic sheep. Livestock Science 143: 293-299.
36. Whitehorn PR, Tinsley MC, Brown MJF, Darvill B, Goulson D (2011) Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proceedings of the Royal Society B-Biological Sciences 278: 1195-1202.
37. Zalucki MP, Kitching RL (1982) The analysis and description of movement in adult Danaus plexippus L (Lepidotera, Danaiae). Behaviour 80: 174-198.
38. Cockrell BJ, Malcolm SB, Brower LP (1993) Time, temperature, and latitudinal constraints on the annual recolonization of eastern North America by the monarch butterfly. Natural History Museum of Los Angeles County Science Series 0: 233-251. (Pubitemid 24409754)
39. de Roode JC, Chi J, Rarick RM, Altizer S (2009) Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus). Oecologia 161: 67-75.
40. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564-567.
41. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
42. Hood GM (2010) PopTools version 3.2.5.
43. Rousset F (2008) GENEPOP '007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103-106.
44. Szpiech Z, Jakobsson M, Rosenberg N (2008) ADZE: a rarefaction approach for counting alleles private to combinations of. Bioinformatics 24: 1367-4811.
45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959. (Pubitemid 30397141)
46. Vane-Wright RI (1993) The Columbus hypothesis: An explantation for the dramatic 19th century range expansion of the monarch butterfly. Natural History Museum of Los Angeles County Science Series 0: 179-187.
47. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.
48. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Molecular Ecology 11: 155-165. (Pubitemid 34140159)
49. Oksanen JF, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2011) vegan: Community Ecology Package. R package version 2.0-0. Available: http://CRANR-projectorg/package=vegan.
50. 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. 168-185.
51. Almberg ES, Cross PC, Smith DW (2010) Persistence of canine distemper virus in the Greater Yellowstone Ecosystem's carnivore community. Ecological Applications 20: 2058-2074.
52. Hess G, Randolph S, Arneberg P, Chemini C, Furlanello C, et al. (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. 102-119.
53. Hanski I, Gilpin M (1991) Metapopulation dynamics- brief history and conceptual domain. Biological Journal of the Linnean Society 42: 3-16.
54. Hess G (1996) Disease in metapopulation models: Implications for conservation. Ecology 77: 1617-1632.
55. McCallum H, Dobson A (2002) Disease, habitat fragmentation and conservation. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2041-2049. (Pubitemid 35177015)
56. Gog J, Woodroffe R, Swinton J (2002) Disease in endangered metapopulations: the importance of alternative hosts. Proceedings of the Royal Society B-Biological Sciences 269: 671-676. (Pubitemid 34407373)
57. Lindsey E, Altizer S (2009) Sex differences in immune defenses and response to parasitism in monarch butterflies. Evolutionary Ecology 23: 607-620.