Abstract
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.
Highlights
Emerging disease in wildlife is an important force driving the decline and extinction of threatened populations [1,2,3] and may pose a threat to worldwide biodiversity [4]
While host species that have been introduced to Hawaii from continental sources over the last several centuries are largely unaffected by avian malaria, endemic species may exhibit mortalities ranging as high as 100% [10, summary in 11]
High susceptibility of island endemics to infectious disease has been proposed as a component of an ‘‘island syndrome’’ [12,13], which seeks to codify typical changes observed in body size [14], life history traits such as survival and fecundity [15,16] and other features associated with insular organisms [17]
Summary
Emerging disease in wildlife is an important force driving the decline and extinction of threatened populations [1,2,3] and may pose a threat to worldwide biodiversity [4]. While host species that have been introduced to Hawaii from continental sources over the last several centuries are largely unaffected by avian malaria, endemic species may exhibit mortalities ranging as high as 100% [10, summary in 11]. This suggests that the introduced strain of malaria is not unusually virulent; instead, it appears that at least some long-term island residents are unusually susceptible to this parasite. Given the physiological costs associated with developing, maintaining, and using an immune system [24,25,26,27,28], in a parasite-impoverished environment, selection should favor birds that maximize fitness by allocating resources away from costly components of the immune system and perhaps towards other fitness-related traits such as reproductive effort
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