Adaptations of skin peptide defences and possible response to the amphibian chytrid fungus in populations of Australian green-eyed treefrogs, Litoria genimaculata

Douglas C. Woodhams, Nicole Kenyon, Sara C. Bell, Ross A. Alford, Shuo Chen, David D Billheimer, Yu Shyr, Louise A. Rollins-Smith

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Aim: Rapidly evolving pathogens may exert diversifying selection on genes involved in host immune defence including those encoding antimicrobial peptides (AMPs). Amphibian skin peptides are one important defence against chytridiomycosis, an emerging infectious disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd). We examined the population-level variation in this innate immune defence to understand its relationship with disease dynamics. Location: Queensland, Australia. Methods: We examined skin peptide defences in five geographically distinct populations of Australian green-eyed treefrogs, Litoria genimaculata. Skin peptide samples were collected from 52 frogs from three upland populations that previously declined as chytridiomycosis emerged, but subsequently recovered, and from 34 frogs in two lowland populations that did not decline. Historical samples of skin peptides preceding Bd emergence were not available from any population. Results: In general, lowland populations had more effective peptide defences than upland populations. Peptide profiles were similar among populations, although relative amounts of peptides expressed differed significantly among populations and were more variable in the uplands. Infected frogs in upland populations carried a significantly higher infection burden compared to lowland populations. The presence of effective AMPs in the skin of L. genimaculata does not eliminate infection; however, more effective peptide defences may limit infection intensity and the progression of disease. Main conclusions: The population bottleneck in upland populations caused by chytridiomycosis emergence did not appear to produce responses to selection for more effective peptide defences against chytridiomycosis compared to lowland populations of L. genimaculata. This does not exclude the possibility that current peptide defences have adapted in response to disease emergence. A suggestive (P < 0.10) interaction between infection status and population indicates that in lowland populations, infected individuals tend to be those with lower relative intensities of AMPs, whereas in the upland populations, infected and uninfected individuals are similar. Thus, both the AMPs and the environment may act to mediate resistance to Bd infection.

Original languageEnglish (US)
Pages (from-to)703-712
Number of pages10
JournalDiversity and Distributions
Volume16
Issue number4
DOIs
StatePublished - Jul 2010
Externally publishedYes

Fingerprint

Hylidae
skin (animal)
peptide
amphibian
amphibians
skin
fungus
peptides
fungi
highlands
antimicrobial peptides
lowlands
frog
frogs
Litoria
defence
infection
population bottleneck
infectious disease
emerging diseases

Keywords

  • Antimicrobial peptide
  • Batrachochytrium dendrobatidis
  • Chytridiomycosis
  • Innate immunity
  • MALDI mass spectrometry

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

Adaptations of skin peptide defences and possible response to the amphibian chytrid fungus in populations of Australian green-eyed treefrogs, Litoria genimaculata. / Woodhams, Douglas C.; Kenyon, Nicole; Bell, Sara C.; Alford, Ross A.; Chen, Shuo; Billheimer, David D; Shyr, Yu; Rollins-Smith, Louise A.

In: Diversity and Distributions, Vol. 16, No. 4, 07.2010, p. 703-712.

Research output: Contribution to journalArticle

Woodhams, Douglas C. ; Kenyon, Nicole ; Bell, Sara C. ; Alford, Ross A. ; Chen, Shuo ; Billheimer, David D ; Shyr, Yu ; Rollins-Smith, Louise A. / Adaptations of skin peptide defences and possible response to the amphibian chytrid fungus in populations of Australian green-eyed treefrogs, Litoria genimaculata. In: Diversity and Distributions. 2010 ; Vol. 16, No. 4. pp. 703-712.
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AU - Kenyon, Nicole

AU - Bell, Sara C.

AU - Alford, Ross A.

AU - Chen, Shuo

AU - Billheimer, David D

AU - Shyr, Yu

AU - Rollins-Smith, Louise A.

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N2 - Aim: Rapidly evolving pathogens may exert diversifying selection on genes involved in host immune defence including those encoding antimicrobial peptides (AMPs). Amphibian skin peptides are one important defence against chytridiomycosis, an emerging infectious disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd). We examined the population-level variation in this innate immune defence to understand its relationship with disease dynamics. Location: Queensland, Australia. Methods: We examined skin peptide defences in five geographically distinct populations of Australian green-eyed treefrogs, Litoria genimaculata. Skin peptide samples were collected from 52 frogs from three upland populations that previously declined as chytridiomycosis emerged, but subsequently recovered, and from 34 frogs in two lowland populations that did not decline. Historical samples of skin peptides preceding Bd emergence were not available from any population. Results: In general, lowland populations had more effective peptide defences than upland populations. Peptide profiles were similar among populations, although relative amounts of peptides expressed differed significantly among populations and were more variable in the uplands. Infected frogs in upland populations carried a significantly higher infection burden compared to lowland populations. The presence of effective AMPs in the skin of L. genimaculata does not eliminate infection; however, more effective peptide defences may limit infection intensity and the progression of disease. Main conclusions: The population bottleneck in upland populations caused by chytridiomycosis emergence did not appear to produce responses to selection for more effective peptide defences against chytridiomycosis compared to lowland populations of L. genimaculata. This does not exclude the possibility that current peptide defences have adapted in response to disease emergence. A suggestive (P < 0.10) interaction between infection status and population indicates that in lowland populations, infected individuals tend to be those with lower relative intensities of AMPs, whereas in the upland populations, infected and uninfected individuals are similar. Thus, both the AMPs and the environment may act to mediate resistance to Bd infection.

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KW - Innate immunity

KW - MALDI mass spectrometry

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