Glacial Refugia in Pathogens: European Genetic Structure of Anther Smut Pathogens on and

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Climate warming is predicted to increase the frequency of invasions by pathogens and to cause the large-scale redistribution of native host species, with dramatic consequences on the health of domesticated and wild populations of plants and animals. The study of historic range shifts in response to climate change, such as during interglacial cycles, can help in the prediction of the routes and dynamics of infectious diseases during the impending ecosystem changes. Here we studied the population structure in Europe of two Microbotryum species causing anther smut disease on the plants Silene latifolia and Silene dioica. Clustering analyses revealed the existence of genetically distinct groups for the pathogen on S. latifolia, providing a clear-cut example of European phylogeography reflecting recolonization from southern refugia after glaciation. The pathogen genetic structure was congruent with the genetic structure of its host species S. latifolia, suggesting dependence of the migration pathway of the anther smut fungus on its host. The fungus, however, appeared to have persisted in more numerous and smaller refugia than its host and to have experienced fewer events of large-scale dispersal. The anther smut pathogen on S. dioica also showed a strong phylogeographic structure that might be related to more northern glacial refugia. Differences in host ecology probably played a role in these differences in the pathogen population structure. Very high selfing rates were inferred in both fungal species, explaining the low levels of admixture between the genetic clusters. The systems studied here indicate that migration patterns caused by climate change can be expected to include pathogen invasions that follow the redistribution of their host species at continental scales, but also that the recolonization by pathogens is not simply a mirror of their hosts, even for obligate biotrophs, and that the ecology of hosts and pathogen mating systems likely affects recolonization patterns.

Vyšlo v časopise: Glacial Refugia in Pathogens: European Genetic Structure of Anther Smut Pathogens on and. PLoS Pathog 6(12): e32767. doi:10.1371/journal.ppat.1001229
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001229

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Zdroje

1. AndersonPK

CunninghamAA

PatelNG

MoralesFJ

EpsteinPR

2004 Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19 535 544

2. HarvellCD

MitchellCE

WardJR

AltizerS

DobsonAP

2002 Climate warming and disease risks for terrestrial and marine biota. Science 296 2158 2162

3. Desprez-LoustauM

RobinC

BueeM

CourtecuisseR

GarbayeJ

2007 The fungal dimension of biological invasions. Trends Ecol Evol 22 472 480

4. GiraudT

GladieuxP

GavriletsS

2010 Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 25 387 395

5. FisherMC

KoenigGL

WhiteTJ

TaylorJW

2000 Pathogenic clones versus environmentally driven population increase: Analysis of an epidemic of the human fungal pathogen Coccidioides immitis. J Clin Microbiol 38 807 813

6. KiddSE

HagenF

TscharkeRL

HuynhM

BartlettKH

2004 A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci USA 101 17258 17263

7. DattaK

BartlettKH

BaerR

ByrnesE

GalanisE

2009 Spread of Cryptococcus gattii into Pacific Northwest Region of the United States. Emerg Infect Dis 15 1185 1191

8. BrooksDR

HobergEP

2007 How will global climate change affect parasite-host assemblages? Trends Parasitol 23 571 574

9. HewittGM

1996 Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58 247 276

10. HewittGM

2004 Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc London Biol 359 183 195

11. HewittG

2003 Ice ages: their impact on species distributions and evolution.

RotschildL

ListerA

Evolution on Planet Earth Academic press 339 361

12. KingRA

FerrisC

1998 Chloroplast DNA phylogeography of Alnus glutinosa (L.) Gaertn. Mol Ecol 7 1151 1161

13. TaberletP

FumagalliL

Wust-SaucyAG

CossonJF

1998 Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7 453 464

14. HewittG

2000 The genetic legacy of quaternary ice ages. Nature 405 907 913

15. PalmeAE

VendraminGG

2002 Chloroplast DNA variation, postglacial recolonization and hybridization in hazel, Corylus avellana. Mol Ecol 11 1769 1780

16. PetitRJ

BrewerS

BordacsS

BurgK

CheddadiR

2002 Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Manag 156 49 74

17. FrancoisO

BlumMGB

JakobssonM

RosenbergNA

2008 Demographic history of European populations of Arabidopsis thaliana. PLoS Genet 4 e1000075

18. IbrahimKM

NicholsRA

HewittGM

1996 Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77 282 291

19. PetitRJ

PineauE

DemesureB

BacilieriR

DucoussoA

1997 Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci USA 94 9996 10001

20. WidmerA

LexerC

2001 Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends Ecol Evol 16 267 269

21. ExcoffierL

FollM

PetitRJ

2008 Genetic Consequences of Range Expansions. Ann Rev Ecol Syst 40 481 501

22. NieberdingCM

Durette-DessetMC

VanderpoortenA

CasanovaJC

RibasA

2008 Geography and host biogeography matter for understanding the phylogeography of a parasite. Mol Phylogenet Evol 47 538 554

23. RichKA

ThompsonJN

FernandezCC

2008 Diverse historical processes shape deep phylogeographical divergence in the pollinating seed parasite Greya politella. Mol Ecol 17 2430 2448

24. AmicoGC

NickrentDL

2009 Population structure and phylogeography of the mistletoes Tristerix corymbosus and T. aphyllus (Loranthaceae) using chloroplast DNA sequence variation. Am J Bot 96 1571 1580

25. NakaoM

XiaoN

OkamotoM

YanagidaT

SakoY

2009 Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitol Int 58 384 389

26. ThrallPH

BurdonJJ

1999 The spatial scale of pathogen dispersal: Consequences for disease dynamics and persistence. Evol Ecol Res 1 681 701

27. GrenfellBT

PybusOG

GogJR

WoodJLN

DalyJM

2004 Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303 327 332

28. MiuraO

TorchinME

KurisAM

HechingerRF

ChibaS

2006 Introduced cryptic species of parasites exhibit different invasion pathways. Proc Natl Acad Sci USA 103 19818 19823

29. ReedDL

SmithVS

HammondSL

RogersAR

ClaytonDH

2004 Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biol 2 e340

30. WhitemanNK

ParkerPG

2005 Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation 8 175 181

31. WirthT

MeyerA

AchtmanM

2005 Deciphering host migrations and origins by means of their microbes. Mol Ecol 14 3289 3306

32. CriscioneCD

CooperB

BlouinMS

2006 Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87 823 828

33. NieberdingCM

OlivieriI

2007 Parasites: proxies for host genealogy and ecology? Trends Ecol Evol 22 156 165

34. WhitemanNK

KimballRT

ParkerPG

2007 Co-phylogeography and comparative population genetics of the threatened Galapagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Mol Ecol 16 4759 4773

35. BlakesleeAMH

ByersJE

LesserMP

2008 Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea's North American origin. Mol Ecol 17 3684 3696

36. BruyndonckxN

IsabelleH

PhilippeC

GeraldK

2009 Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechstein is shaped by its own demography and the social system of its bat host. Mol Ecol 18 3581 3592

37. BruyndonckxN

BiollazF

DubeyS

GoudetJ

ChristeP

2010 Mites as biological tags of their hosts. Mol Ecol 19 2770 2778

38. BarrettLG

ThrallPH

BurdonJJ

LindeCC

2008 Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 23 678 685

39. HoodME

Mena-AlíJI

GibsonAK

OxelmanB

GiraudT

2010 Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. New Phytologist 187 217 229

40. FargetteD

KonateG

FauquetC

MullerE

PeterschmittM

2006 Molecular ecology and emergence of tropical plant viruses. Ann Rev Phytopathol 44 235 260

41. WilsonDJ

FalushD

McVeanG

2005 Germs, genomes and genealogies. Trends Ecol Evol 20 39 45

42. DelmotteF

BucheliE

ShykoffJA

1999 Host and parasite population structure in a natural plant-pathogen system. Heredity 82 300 308

43. LutzM

GokerM

PiatekM

KemlerM

BegerowD

2005 Anther smuts of Caryophyllaceae: molecular characters indicate host-dependent species delimitation. Mycol Prog 4 225 238

44. KemlerM

GokerM

OberwinklerF

BegerowD

2006 Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evol Biol 6 35

45. Le GacM

HoodME

GiraudT

2007 Evolution of reproductive isolation within a parasitic fungal complex. Evolution 61 1781 1787

46. Le GacM

HoodME

FournierE

GiraudT

2007 Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61 15 26

47. RefrégierG

Le GacM

JabbourF

WidmerA

HoodME

2008 Cophylogeny of the anther smut fungi and their Caryophyllaceous hosts: Prevalence of host shifts and Importance of delimiting parasite species. BMC Evol Biol 8 100

48. SloanD

GiraudT

HoodM

2008 Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts. J Evol Biol 21 1544 1554

49. de VienneDM

RefrégierG

HoodM

GuigueA

DevierB

2009 Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. J Evol Biol 22 683 698

50. de VienneDM

HoodME

GiraudT

2009 Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol 22 2532 2541

51. DenchevC

GiraudT

HoodM

2009 Three new species of anthericolous smut fungi on Caryophyllaceae. Mycologia Balcanica 6 79 84

52. GladieuxP

VerckenE

FontaineM

HoodME

JonotO

2010 Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol. In press

53. ThrallP

JaroszA

1994 Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. II. Experimental tests on theoretical models. J Ecol 82 561 570

54. ThrallP

JaroszA

1994 Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. I. Ecological and genetic determinants of disease spread. J Ecol 82 549 559

55. BernasconiG

AntonovicsJ

BiereA

CharlesworthD

DelphL

2009 Silene as a model system in ecology and evolution. Heredity 103 5 14

56. TaylorD

KellerS

2007 Historical range expansion determined the phylogenetic diversity introduced during contemporary species invasion. Evolution 61 334 345

57. HathawayL

MalmJU

PrenticeHC

2009 Geographically congruent large-scale patterns of plastid haplotype variation in the European herbs Silene dioica and S. latifolia (Caryophyllaceae). Bot J Linn Soc 161 153 170

58. PrenticeHC

MalmJU

HathawayL

2008 Chloroplast DNA variation in the European herb Silene dioica (red campion): postglacial migration and interspecific introgression. Plant Syst Evol 272 23 37

59. FriedrichH

1979 Caryophyllaceae.

RechingerKH

Illustrierte Flora von Mitteleuropa Hamburg Parey 763 1182

60. BakerHG

1947 Melandrium album (Mill) Garcke. J Ecol 35 274 282

61. BakerHG

1947 Melandrium dioicum (L. Emend) Coss. & Germ. J Ecol 35 283 292

62. KarrenbergS

FavreA

2008 Genetic and ecological differenciation in hybridizing campions Silene dioica and S. latifolia. Evolution 62 763 773

63. BucheliE

GautschiB

ShykoffJA

2001 Differences in population structure of the anther smut fungus Microbotryum violaceum on two closely related host species, Silene latifolia and S. dioica. Mol Ecol 10 285 294

64. DurandE

JayF

GaggiottiOE

FrancoisO

2009 Spatial Inference of Admixture Proportions and Secondary Contact Zones. Mol Biol Evol 26 1963 1973

65. VekemansX

HardyOJ

2004 New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13 921 35

66. SunJX

MullikinJC

PattersonN

ReichDE

2009 Microsatellites Are Molecular Clocks That Support Accurate Inferences about History. Mol Biol Evol 26 1017 1027

67. GiraudT

YocktengR

Lopez-VillavicencioM

RefregierG

HoodME

2008 Mating system of the anther smut fungus, Microbotryum violaceum: selfing under heterothallism. Eukaryotic Cell 7 765 775

68. GranbergA

Carlsson-GranerU

ArnqvistP

GilesBE

2008 Variation in breeding system traits within and among populations of Microbotryum violaceum on Silene dioica. Int J Plant Sci 169 293 303

69. HoodME

AntonovicsJ

2000 Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum ( = Ustilago violacea). Heredity 85 231 241

70. GiraudT

JonotO

ShykoffJA

2005 Selfing propensity under choice conditions in a parasitic fungus, Microbotryum violaceum, and parameters influencing infection success in artificial inoculations. Int J Plant Sci 166 649 657

71. HoodME

AntonovicsJA

2004 Mating within the meiotic tetrad and the maintenance of genomic heterozygosity. Genetics 166 1751 1759

72. CharlesworthD

2003 Effects of inbreeding on the genetic diversity of populations. Phil Trans R Soc London Biol 358 1051 1070

73. PannellJR

CharlesworthB

2000 Effects of metapopulation processes on measures of genetic diversity. Phil Trans R Soc London Biol 355 1851 1864

74. ThrallPH

AntonovicsJ

1995 Theoretical and empirical studies of metapopulations: population and genetic dynamics of the Silene - Ustilago system. Can J Bot 73 S1249 S1258

75. GilesBE

GoudetJ

1997 Genetic differentiation in Silene dioica metapopulations: Estimation of spatiotemporal effects in a successional plant species. Am Nat 149 507 526

76. AntonovicsJ

2004 Long term study of a plant-pathogen metapopulation.

HanskiI

GaggiottiO

Ecology, Genetics, and Evolution of Metapopulations Amsterdam Academic Press 471 488

77. GiraudT

2004 Patterns of within population dispersal and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia. Heredity 93 559 65

78. WillisKJ

van AndelTH

2004 Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quat Sci Rev 23 2369 2387

79. DeffontaineV

LiboisR

KotlikP

SommerR

NieberdingC

2005 Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol Ecol 14 1727 39

80. KotlikP

DeffontaineV

MascherettiS

ZimaJ

MichauxJ

2006 A northern glacial refugium for bank voles (Clethrionomys glareolus). Proc Natl Acad Sci USA 103 14860 14864

81. BhagwatSA

WillisKJ

2008 Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? J Biogeography 35 464 482

82. ProvanJ

BennettK

2008 Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23 564 571

83. BinneyHA

WillisKJ

EdwardsME

BhagwatSA

AndersonPM

2009 The distribution of late-Quaternary woody taxa in northern Eurasia: evidence from a new macrofossil database. Quat Sci Rev 28 2445 2464

84. StewartJR

ListerAM

BarnesI

DalenL

2010 Refugia revisited: individualistic responses of species in space and time. Proc R Soc B 277 661 671

85. WillisKJ

NiklasKJ

2004 The role of Quaternary environmental change in plant macroevolution: the exception or the rule? Phil Trans R Soc London Biol 359 159 172

86. AspockH

2008 Postglacial formation and fluctuations of the biodiversity of Central Europe in the light of climate change. Parasitol Res 103 S7 S10

87. GómezA

LuntD

2007 Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula.

WeissS

FerrandN

Phylogeography of Southern European Refugia Dordrecht, The Netherlands Springer 155 188

88. UrsenbacherS

SchweigerS

TomovicL

Crnobrnja-IsailovicJ

FumagalliL

2008 Molecular phylogeography of the nose-horned viper (Vipera ammodytes, Linnaeus (1758)): Evidence for high genetic diversity and multiple refugia in the Balkan peninsula. Mol Phylogenet Evol 46 1116 1128

89. DeffontaineV

RenaudS

FontaineM

QuéréJ

LiboisR

2009 A relic bank vole lineage in the French Basque country highlights the biogeographical history of Pyrenean mountains in Europe. Mol Ecol 18 2489 2502

90. GrillA

AmoriG

AloiseG

LisiI

TosiG

2009 Molecular phylogeography of European Sciurus vulgaris: refuge within refugia? Mol Ecol 18 2687 2699

91. PrevisicA

WaltonC

KucinicM

MitrikeskiPT

KerovecM

2009 Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol Ecol 18 634 647

92. PetitRJ

AguinagaldeI

de BeaulieuJL

BittkauC

BrewerS

2003 Glacial refugia: Hotspots but not melting pots of genetic diversity. Science 300 1563 1565

93. HickersonMJ

StahlEA

LessiosHA

2006 Test for simultaneous divergence using approximate Bayesian computation. Evolution 60 2435 53

94. GiraudT

RefregierG

de VienneDM

Le GacMA

HoodME

2008 Speciation in fungi. Fungal Genet Biol 45 791 802

95. TatarenkovA

GaoH

MackiewiczM

TaylorDS

TurnerBJ

2007 Strong population structure despite evidence of recent migration in a selfing hermaphroditic vertebrate, the mangrove killifish (Kryptolebias marmoratus). Mol Ecol 16 2701 2711

96. BoileauMG

HebertPDN

SchwartzSS

1992 Non-equilibrium gene frequency divergence: persistent founder effects in natural populations. J Evol Biol 5 25 39

97. AntonovicsJ

HoodME

ThrallPH

AbramsJY

DuthieGM

2003 Herbarium studies on the distribution of anther-smut fungus (Microbotryum violaceum) and Silene species (Caryophyllaceae) in the eastern United States. Am J Bot 90 1522 1531

98. HoodME

AntonovicsJ

HeishmanH

2003 Karyotypic similarity identifies multiple host-shifts of a pathogenic fungus in natural populations. Infect Genet Evol 2 167 172

99. SlippersB

StenlidJ

WingfieldMJ

2005 Emerging pathogens: fungal host jumps following anthropogenic introduction. Trends Ecol Evol 20 420 421

100. TellierA

de VIenneDM

GiraudT

HoodME

RefrégierG

2010 Theory and examples of reciprocal influence between hosts and pathogens, from short-term to long term interactions: coevolution, cospeciation and pathogen speciation following host shifts. In: Host-Pathogen Interactions: Genetics, Immunology and Physiology. 37-77 NY Nova Science Publishers

101. Lopez-VillavicencioM

JonotO

CoanticA

HoodME

EnjalbertJ

2007 Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathogens 3 e176

102. BucheliE

GautschiB

ShykoffJA

1998 Isolation and characterization of microsatellite loci in the anther smut fungus Microbotryum violaceum. Mol Ecol 7 665 666

103. GiraudT

YocktengR

MartheyS

ChiapelloH

JonotO

2008 Isolation of 60 polymorphic microsatellite loci in EST libraries of four sibling species of the phytopathogenic fungal complex Microbotryum. Mol Ecol Res 8 387 392

104. RefrégierG

HoodME

GiraudT

2010 No evidence of reproductive character displacement between two sister fungal species causing anther smut disease in Silene. Int J Plant Sci 171 847 859

105. van PuttenWF

BiereA

van DammeJM

2005 Host-related genetic differentiation in the anther smut fungus Microbotryum violaceum in sympatric, parapatric and allopatric populations of two host species Silene latifolia and S. dioica. J Evol Biol 18 203 12

106. GoudetJ

2001 FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm

107. RaymondM

RoussetF

1995 GENEPOP (Version 1.2): Population genetics software for exact tests and eucumenism. J Hered 86 248 249

108. RoussetF

2008 genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8 103 106

109. BelkhirK

BorsaP

ChikhiL

RaufasteN

BonhommeF

2001 Genetix 4.02, Logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, population, interaction, CNRS UMR 5000, Université de Montpellier II (France)

110. PritchardJK

StephensM

DonnellyP

2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959

111. FalushD

StephensM

PritchardJ

2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 1567 1587

112. GaoH

WilliamsonS

BustamanteCD

2007 A Markov Chain Monte Carlo Approach for Joint Inference of Population Structure and Inbreeding Rates From Multilocus Genotype Data. Genetics 176 1635 1651

113. FrancoisO

AnceletS

GuillotG

2006 Bayesian clustering using hidden Markov random fields in spatial population genetics. Genetics 174 805 816

114. ChenC

DurandE

ForbesF

FrancoisO

2007 Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7 747 756

115. JakobssonM

RosenbergNA

2007 CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23 1801 6

116. RosenbergN

2004 DISTRUCT: a program for graphical display for population structure. Mol Ecol Notes 4 137 138

117. PritchardJK

WenW

2004 Documentation for Structure software: Version 2

118. SpiegelhalterDJ

BestNG

CarlinBP

LindeAVD

2002 Bayesian measures of model complexity and fit. J Roy Stat Soc B 64 583 639

119. JombartT

2010 Package ‘adegenet’. a R package for the multivariate analysis of genetic markers. http://cran.r-project.org/web/packages/adegenet/index.html

120. ChesselD

DufourA

DrayS

2009 Package ‘ade4’. Analysis of Ecological Data: Exploratory and Euclivian methods in Environmental sciences. http://cran.r-project.org/web/packages/ade4/index.html

121. R Development Core Team 2010 R: A Language and Environment for Statistical Computing

122. NeiM

TajimaF

TatenoY

1983 Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19 153 170

123. ChakrabortyR

JinL

1993 Determination of relatedness between individuals using DNA fingerprinting. Hum Biol 65 875 895

124. BowcockAM

Ruiz-linaresA

TomfohrdeJ

MinchE