Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.

Dramatic declines of native Hawaiian avifauna due to the human-mediated emergence of avian malaria and pox prompted an examination of whether island taxa share a common altered immunological signature, potentially driven by reduced genetic diversity and reduced exposure to parasites. We tested this...

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Main Authors: Jon S Beadell, Colm Atkins, Erin Cashion, Michelle Jonker, Robert C Fleischer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-09-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0000896
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spelling doaj-178eb8a066cf414ebc15c31ef7a68b3a2021-03-03T19:55:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032007-09-0129e89610.1371/journal.pone.0000896Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.Jon S BeadellColm AtkinsErin CashionMichelle JonkerRobert C FleischerDramatic declines of native Hawaiian avifauna due to the human-mediated emergence of avian malaria and pox prompted an examination of whether island taxa share a common altered immunological signature, potentially driven by reduced genetic diversity and reduced exposure to parasites. We tested this hypothesis by characterizing parasite prevalence, genetic diversity and three measures of immune response in two recently-introduced species (Neochmia temporalis and Zosterops lateralis) and two island endemics (Acrocephalus aequinoctialis and A. rimitarae) and then comparing the results to those observed in closely-related mainland counterparts. The prevalence of blood parasites was significantly lower in 3 of 4 island taxa, due in part to the absence of certain parasite lineages represented in mainland populations. Indices of genetic diversity were unchanged in the island population of N. temporalis; however, allelic richness was significantly lower in the island population of Z. lateralis while both allelic richness and heterozygosity were significantly reduced in the two island-endemic species examined. Although parasite prevalence and genetic diversity generally conformed to expectations for an island system, we did not find evidence for a pattern of uniformly altered immune responses in island taxa, even amongst endemic taxa with the longest residence times. The island population of Z. lateralis exhibited a significantly reduced inflammatory cell-mediated response while levels of natural antibodies remained unchanged for this and the other recently introduced island taxon. In contrast, the island endemic A. rimitarae exhibited a significantly increased inflammatory response as well as higher levels of natural antibodies and complement. These measures were unchanged or lower in A. aequinoctialis. We suggest that small differences in the pathogenic landscape and the stochastic history of mutation and genetic drift are likely to be important in shaping the unique immunological profiles of small isolated populations. Consequently, predicting the impact of introduced disease on the many other endemic faunas of the remote Pacific will remain a challenge.https://doi.org/10.1371/journal.pone.0000896
collection DOAJ
language English
format Article
sources DOAJ
author Jon S Beadell
Colm Atkins
Erin Cashion
Michelle Jonker
Robert C Fleischer
spellingShingle Jon S Beadell
Colm Atkins
Erin Cashion
Michelle Jonker
Robert C Fleischer
Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
PLoS ONE
author_facet Jon S Beadell
Colm Atkins
Erin Cashion
Michelle Jonker
Robert C Fleischer
author_sort Jon S Beadell
title Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
title_short Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
title_full Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
title_fullStr Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
title_full_unstemmed Immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
title_sort immunological change in a parasite-impoverished environment: divergent signals from four island taxa.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2007-09-01
description Dramatic declines of native Hawaiian avifauna due to the human-mediated emergence of avian malaria and pox prompted an examination of whether island taxa share a common altered immunological signature, potentially driven by reduced genetic diversity and reduced exposure to parasites. We tested this hypothesis by characterizing parasite prevalence, genetic diversity and three measures of immune response in two recently-introduced species (Neochmia temporalis and Zosterops lateralis) and two island endemics (Acrocephalus aequinoctialis and A. rimitarae) and then comparing the results to those observed in closely-related mainland counterparts. The prevalence of blood parasites was significantly lower in 3 of 4 island taxa, due in part to the absence of certain parasite lineages represented in mainland populations. Indices of genetic diversity were unchanged in the island population of N. temporalis; however, allelic richness was significantly lower in the island population of Z. lateralis while both allelic richness and heterozygosity were significantly reduced in the two island-endemic species examined. Although parasite prevalence and genetic diversity generally conformed to expectations for an island system, we did not find evidence for a pattern of uniformly altered immune responses in island taxa, even amongst endemic taxa with the longest residence times. The island population of Z. lateralis exhibited a significantly reduced inflammatory cell-mediated response while levels of natural antibodies remained unchanged for this and the other recently introduced island taxon. In contrast, the island endemic A. rimitarae exhibited a significantly increased inflammatory response as well as higher levels of natural antibodies and complement. These measures were unchanged or lower in A. aequinoctialis. We suggest that small differences in the pathogenic landscape and the stochastic history of mutation and genetic drift are likely to be important in shaping the unique immunological profiles of small isolated populations. Consequently, predicting the impact of introduced disease on the many other endemic faunas of the remote Pacific will remain a challenge.
url https://doi.org/10.1371/journal.pone.0000896
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