Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians

Arnaud BATAILLE, Jonathan J. FONG, Moonsuk CHA, Guinevere O. U. WOGAN, Hae Jun BAEK, Hang LEE, Mi-Sook MIN, Bruce WALDMAN

Research output: Journal PublicationsJournal Article (refereed)Researchpeer-review

66 Citations (Scopus)

Abstract

Population declines and extinctions of amphibians have been attributed to the chytrid fungus Batrachochytrium dendrobatidis (Bd), especially one globally emerging recombinant lineage (‘Bd-GPL’). We used PCR assays that target the ribosomal internal transcribed spacer region (ITS) of Bd to determine the prevalence and genetic diversity of Bd in South Korea, where Bd is widely distributed but is not known to cause morbidity or mortality in wild populations. We isolated Korean Bd strains from native amphibians with low infection loads and compared them to known worldwide Bd strains using 19 polymorphic SNP and microsatellite loci. Bd prevalence ranged between 12.5 and 48.0%, in 11 of 17 native Korean species, and 24.7% in the introduced bullfrog Lithobates catesbeianus . Based on ITS sequence variation, 47 of the 50 identified Korean haplotypes formed a group closely associated with a native Brazilian Bd lineage, separated from the Bd-GPL lineage. However, multilocus genotyping of three Korean Bd isolates revealed strong divergence from both Bd-GPL and the native Brazilian Bd lineages. Thus, the ITS region resolves genotypes that diverge from Bd-GPL but otherwise generates ambiguous phylogenies. Our results point to the presence of highly diversified endemic strains of Bd across Asian amphibian species. The rarity of Bd-GPL-associated haplotypes suggests that either this lineage was introduced into Korea only recently or Bd-GPL has been outcompeted by native Bd strains. Our results highlight the need to consider possible complex interactions among native Bd lineages, Bd-GPL and their associated amphibian hosts when assessing the spread and impact of Bd-GPL on worldwide amphibian populations.
Original languageEnglish
Pages (from-to)4196-4209
Number of pages14
JournalMolecular Ecology
Volume22
Issue number16
Early online date27 Jun 2013
DOIs
Publication statusPublished - Aug 2013
Externally publishedYes

Fingerprint

Chytridiomycota
Amphibians
amphibian
amphibians
Fungi
fungus
fungi
internal transcribed spacers
haplotypes
Lithobates catesbeianus
South Korea
rarity
morbidity
population decline
wild population
native species
genotyping
Korean Peninsula
phylogeny
genotype

Bibliographical note

The research was supported by the National Research Foundation of Korea (NRF), funded by the government of the Republic of Korea (MSIP) (grants 2010‐0002767, 2012R1A1A2044449 and 2012K1A2B1A03000496 to B.W., and KRF‐2007‐313‐C00503 and 2009‐0067686 to M.S.M.) and by Seoul National University (Brain Fusion Program, Brain Korea 21 Program, and New Faculty Resettlement Fund grants to B.W.).

Keywords

  • chytrid fungus
  • conservation
  • emerging infectious disease
  • endemism
  • frogs
  • host–parasite co-evolution
  • invasive species
  • population declines
  • prevalence
  • salamanders

Cite this

BATAILLE, Arnaud ; FONG, Jonathan J. ; CHA, Moonsuk ; WOGAN, Guinevere O. U. ; BAEK, Hae Jun ; LEE, Hang ; MIN, Mi-Sook ; WALDMAN, Bruce. / Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. In: Molecular Ecology. 2013 ; Vol. 22, No. 16. pp. 4196-4209.
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abstract = "Population declines and extinctions of amphibians have been attributed to the chytrid fungus Batrachochytrium dendrobatidis (Bd), especially one globally emerging recombinant lineage (‘Bd-GPL’). We used PCR assays that target the ribosomal internal transcribed spacer region (ITS) of Bd to determine the prevalence and genetic diversity of Bd in South Korea, where Bd is widely distributed but is not known to cause morbidity or mortality in wild populations. We isolated Korean Bd strains from native amphibians with low infection loads and compared them to known worldwide Bd strains using 19 polymorphic SNP and microsatellite loci. Bd prevalence ranged between 12.5 and 48.0{\%}, in 11 of 17 native Korean species, and 24.7{\%} in the introduced bullfrog Lithobates catesbeianus . Based on ITS sequence variation, 47 of the 50 identified Korean haplotypes formed a group closely associated with a native Brazilian Bd lineage, separated from the Bd-GPL lineage. However, multilocus genotyping of three Korean Bd isolates revealed strong divergence from both Bd-GPL and the native Brazilian Bd lineages. Thus, the ITS region resolves genotypes that diverge from Bd-GPL but otherwise generates ambiguous phylogenies. Our results point to the presence of highly diversified endemic strains of Bd across Asian amphibian species. The rarity of Bd-GPL-associated haplotypes suggests that either this lineage was introduced into Korea only recently or Bd-GPL has been outcompeted by native Bd strains. Our results highlight the need to consider possible complex interactions among native Bd lineages, Bd-GPL and their associated amphibian hosts when assessing the spread and impact of Bd-GPL on worldwide amphibian populations.",
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Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. / BATAILLE, Arnaud; FONG, Jonathan J.; CHA, Moonsuk; WOGAN, Guinevere O. U.; BAEK, Hae Jun; LEE, Hang; MIN, Mi-Sook; WALDMAN, Bruce.

In: Molecular Ecology, Vol. 22, No. 16, 08.2013, p. 4196-4209.

Research output: Journal PublicationsJournal Article (refereed)Researchpeer-review

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AU - BATAILLE, Arnaud

AU - FONG, Jonathan J.

AU - CHA, Moonsuk

AU - WOGAN, Guinevere O. U.

AU - BAEK, Hae Jun

AU - LEE, Hang

AU - MIN, Mi-Sook

AU - WALDMAN, Bruce

N1 - The research was supported by the National Research Foundation of Korea (NRF), funded by the government of the Republic of Korea (MSIP) (grants 2010‐0002767, 2012R1A1A2044449 and 2012K1A2B1A03000496 to B.W., and KRF‐2007‐313‐C00503 and 2009‐0067686 to M.S.M.) and by Seoul National University (Brain Fusion Program, Brain Korea 21 Program, and New Faculty Resettlement Fund grants to B.W.).

PY - 2013/8

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N2 - Population declines and extinctions of amphibians have been attributed to the chytrid fungus Batrachochytrium dendrobatidis (Bd), especially one globally emerging recombinant lineage (‘Bd-GPL’). We used PCR assays that target the ribosomal internal transcribed spacer region (ITS) of Bd to determine the prevalence and genetic diversity of Bd in South Korea, where Bd is widely distributed but is not known to cause morbidity or mortality in wild populations. We isolated Korean Bd strains from native amphibians with low infection loads and compared them to known worldwide Bd strains using 19 polymorphic SNP and microsatellite loci. Bd prevalence ranged between 12.5 and 48.0%, in 11 of 17 native Korean species, and 24.7% in the introduced bullfrog Lithobates catesbeianus . Based on ITS sequence variation, 47 of the 50 identified Korean haplotypes formed a group closely associated with a native Brazilian Bd lineage, separated from the Bd-GPL lineage. However, multilocus genotyping of three Korean Bd isolates revealed strong divergence from both Bd-GPL and the native Brazilian Bd lineages. Thus, the ITS region resolves genotypes that diverge from Bd-GPL but otherwise generates ambiguous phylogenies. Our results point to the presence of highly diversified endemic strains of Bd across Asian amphibian species. The rarity of Bd-GPL-associated haplotypes suggests that either this lineage was introduced into Korea only recently or Bd-GPL has been outcompeted by native Bd strains. Our results highlight the need to consider possible complex interactions among native Bd lineages, Bd-GPL and their associated amphibian hosts when assessing the spread and impact of Bd-GPL on worldwide amphibian populations.

AB - Population declines and extinctions of amphibians have been attributed to the chytrid fungus Batrachochytrium dendrobatidis (Bd), especially one globally emerging recombinant lineage (‘Bd-GPL’). We used PCR assays that target the ribosomal internal transcribed spacer region (ITS) of Bd to determine the prevalence and genetic diversity of Bd in South Korea, where Bd is widely distributed but is not known to cause morbidity or mortality in wild populations. We isolated Korean Bd strains from native amphibians with low infection loads and compared them to known worldwide Bd strains using 19 polymorphic SNP and microsatellite loci. Bd prevalence ranged between 12.5 and 48.0%, in 11 of 17 native Korean species, and 24.7% in the introduced bullfrog Lithobates catesbeianus . Based on ITS sequence variation, 47 of the 50 identified Korean haplotypes formed a group closely associated with a native Brazilian Bd lineage, separated from the Bd-GPL lineage. However, multilocus genotyping of three Korean Bd isolates revealed strong divergence from both Bd-GPL and the native Brazilian Bd lineages. Thus, the ITS region resolves genotypes that diverge from Bd-GPL but otherwise generates ambiguous phylogenies. Our results point to the presence of highly diversified endemic strains of Bd across Asian amphibian species. The rarity of Bd-GPL-associated haplotypes suggests that either this lineage was introduced into Korea only recently or Bd-GPL has been outcompeted by native Bd strains. Our results highlight the need to consider possible complex interactions among native Bd lineages, Bd-GPL and their associated amphibian hosts when assessing the spread and impact of Bd-GPL on worldwide amphibian populations.

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KW - conservation

KW - emerging infectious disease

KW - endemism

KW - frogs

KW - host–parasite co-evolution

KW - invasive species

KW - population declines

KW - prevalence

KW - salamanders

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