Abstract
The recent emergence of the poultry bacterial pathogen Mycoplasma gallisepticum (MG) in free-living house finches (Haemorhous mexicanus), which causes mycoplasmal conjunctivitis in this passerine bird species, resulted in a rapid coevolutionary arms-race between MG and its novel avian host. Despite extensive research on the ecological and evolutionary dynamics of this host–pathogen system over the past two decades, the immunological responses of house finches to MG infection remain poorly understood. We developed seven new probe-based one-step quantitative reverse transcription polymerase chain reaction assays to investigate mRNA expression of house finch cytokine genes (IL1B, IL6, IL10, IL18, TGFB2, TNFSF15, and CXCLi2, syn. IL8L). These assays were then used to describe cytokine transcription profiles in a panel of 15 house finch tissues collected at three distinct time points during MG infection. Based on initial screening that indicated strong pro-inflammatory cytokine expression during MG infection at the periorbital sites in particular, we selected two key house finch tissues for further characterization: the nictitating membrane, i.e., the internal eyelid in direct contact with MG, and the Harderian gland, the secondary lymphoid tissue responsible for regulation of periorbital immunity. We characterized cytokine responses in these two tissues for 60 house finches experimentally inoculated either with media alone (sham) or one of two MG isolates: the earliest known pathogen isolate from house finches (VA1994) or an evolutionarily more derived isolate collected in 2006 (NC2006), which is known to be more virulent. We show that the more derived and virulent isolate NC2006, relative to VA1994, triggers stronger local inflammatory cytokine signaling, with peak cytokine expression generally occurring 3–6 days following MG inoculation. We also found that the extent of pro-inflammatory interleukin 1 beta signaling was correlated with conjunctival MG loads and the extent of clinical signs of conjunctivitis, the main pathological effect of MG in house finches. These results suggest that the pathogenicity caused by MG infection in house finches is largely mediated by host pro-inflammatory immune responses, with important implications for the dynamics of host–pathogen coevolution.
Highlights
Emerging infectious diseases apply novel and powerful selection pressures on wildlife host immune responses
Spleen was included in further analysis as a standardly investigated lymphatic tissue for the purpose of comparison. For these seven selected tissues, we analyzed the expression of all seven investigated cytokine genes in four control individuals and four NC2006-infected individuals at DPI 6 to identify the genes differentially expressed in individual tissues during Mycoplasma gallisepticum (MG) infection
The cytokine standardized relative quantity data show significant differential expression of IL1B in brain, conjunctiva, Harderian gland (HG) and internal eyelid, of IL6 in conjunctiva and internal eyelid, of IL10 in conjunctiva, HG and internal eyelid, and of CXCLi2 and TNFSF15 in conjunctiva and internal eyelid (Figure 2; see Figure S2 and Tables S5 and S6 in Supplementary Material for analogous results obtained based on Absolute quantity (aQ) data, A)
Summary
Emerging infectious diseases apply novel and powerful selection pressures on wildlife host immune responses. There is a growing list of examples of wildlife hosts that have rapidly evolved resistance or tolerance to recently emerged infectious diseases [e.g., rabbits and myxoma virus [1]; amphibians and chytridiomycosis [2]; bats and white-nose syndrome [3]; and house finches and mycoplasmal conjunctivitis [4]]. There have been few opportunities to experimentally characterize how pathogen evolution following initial disease emergence has altered the immune responses of natural wildlife hosts to infection [8, 9]. We use a well-studied and recently emerged wildlife disease system—the bacterium Mycoplasma gallisepticum (MG) and its novel songbird host, the house finch—to characterize cytokine responses during in vivo infection, and to understand how cytokine responses differ for birds inoculated with an original versus evolved pathogen isolate. While original isolates (e.g., VA1994) produce moderately severe but often self-healing disease in captivity, evolutionarily derived isolates (e.g., NC2006) are more likely to cause severe and/or chronic infection and disease [9, 19]
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