Ecoimmunity in Darwin's finches: invasive parasites trigger acquired immunity in the medium ground finch (Geospiza fortis).

Sarah K Huber,Dale H Clayton,B Rosemary Grant,Peter R Grant,Jennifer A H Koop,Marisa O King,Jeb P Owen

doi:10.1371/journal.pone.0008605

Sarah K Huber, Dale H Clayton + Show 5 more

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https://doi.org/10.1371/journal.pone.0008605

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Abstract

BackgroundInvasive parasites are a major threat to island populations of animals. Darwin's finches of the Galápagos Islands are under attack by introduced pox virus (Poxvirus avium) and nest flies (Philornis downsi). We developed assays for parasite-specific antibody responses in Darwin's finches (Geospiza fortis), to test for relationships between adaptive immune responses to novel parasites and spatial-temporal variation in the occurrence of parasite pressure among G. fortis populations.Methodology/Principal FindingsWe developed enzyme-linked immunosorbent assays (ELISAs) for the presence of antibodies in the serum of Darwin's finches specific to pox virus or Philornis proteins. We compared antibody levels between bird populations with and without evidence of pox infection (visible lesions), and among birds sampled before nesting (prior to nest-fly exposure) versus during nesting (with fly exposure). Birds from the Pox-positive population had higher levels of pox-binding antibodies. Philornis-binding antibody levels were higher in birds sampled during nesting. Female birds, which occupy the nest, had higher Philornis-binding antibody levels than males. The study was limited by an inability to confirm pox exposure independent of obvious lesions. However, the lasting effects of pox infection (e.g., scarring and lost digits) were expected to be reliable indicators of prior pox infection.Conclusions/SignificanceThis is the first demonstration, to our knowledge, of parasite-specific antibody responses to multiple classes of parasites in a wild population of birds. Darwin's finches initiated acquired immune responses to novel parasites. Our study has vital implications for invasion biology and ecological immunology. The adaptive immune response of Darwin's finches may help combat the negative effects of parasitism. Alternatively, the physiological cost of mounting such a response could outweigh any benefits, accelerating population decline. Tests of the fitness implications of parasite-specific immune responses in Darwin's finches are urgently needed.

Highlights

Invasive parasites pose a serious threat to native animal populations, because hosts with no history of exposure may lack effective immune defenses
When we compared Philornis-specific antibody levels in adult birds sampled before nesting with a different set of individuals sampled during the nesting period, we found significantly greater levels of Philornis-specific antibodies during the nesting period
We found no sex difference in pox-specific antibody levels, suggesting equal exposure of males and females to pox virus

Summary

Introduction

Invasive parasites pose a serious threat to native animal populations, because hosts with no history of exposure may lack effective immune defenses. Darwin’s finches have recently been exposed to two introduced parasites of high conservation priority: avian pox virus (Poxvirus avium) and the nest fly Philornis downsi (Figure 1A, 1B) [1,2]. Both of these parasites have been shown to have negative effects on host fitness of Galapagos birds [5,6,7,8,9,10]. The physiological costs of an induced immune response to these parasites may exceed the benefits of mitigating parasite damage and contribute to negative fitness consequences. We developed assays for parasite-specific antibody responses in Darwin’s finches (Geospiza fortis), to test for relationships between adaptive immune responses to novel parasites and spatial-temporal variation in the occurrence of parasite pressure among G. fortis populations

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