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Pathogen adaptations during host-pathogen co-evolution can cause the host balance between immunity and immunopathology to rapidly shift. However, little is known in natural disease systems about the immunological pathways optimised through the trade-off between immunity and self-damage. The evolutionary interaction between the conjunctival bacterial infectionMycoplasma gallisepticum(MG) and its avian host, the house finch (Haemorhous mexicanus), can provide insights into such adaptations in immune regulation. Here we use experimental infections to reveal immune variation in conjunctival tissue for house finches captured from four distinct populations differing in the length of their co-evolutionary histories with MG and their disease tolerance (defined as disease severity per pathogen load) in controlled infection studies. To differentiate contributions of host versus pathogen evolution, we compared house finch responses to one of two MG isolates: the original VA1994 isolate and a more evolutionarily derived one, VA2013. To identify differential gene expression involved in initiation of the immune response to MG, we performed 3’-end transcriptomic sequencing (QuantSeq) of samples from the infection site, conjunctiva, collected 3-days post-infection. In response to MG, we observed an increase in general pro-inflammatory signalling, as well as T-cell activation and IL17 pathway differentiation, associated with a decrease in the IL12/IL23 pathway signalling. The immune response was stronger in response to the evolutionarily derived MG isolate compared to the original one, consistent with known increases in MG virulence over time. The host populations differed namely in pre-activation immune gene expression, suggesting population-specific adaptations. Compared to other populations, finches from Virginia, which have the longest co-evolutionary history with MG, showed significantly higher expression of anti-inflammatory genes and Th1 mediators. This may explain the evolution of disease tolerance to MG infection in VA birds. We also show a potential modulating role of BCL10, a positive B- and T-cell regulator activating the NFKB signalling. Our results illuminate potential mechanisms of house finch adaptation to MG-induced immunopathology, contributing to understanding of the host evolutionary responses to pathogen-driven shifts in immunity-immunopathology trade-offs.

 

Acute infections can alter foraging and movement behaviors relevant to sociality and pathogen spread. However, few studies have directly examined how acute infections caused by directly transmitted pathogens influence host social preferences. While infected hosts often express sickness behaviors (e.g., lethargy) that can reduce social associations with conspecifics, enhanced sociality during infection might be favored in some systems if social grouping improves host survival of infection. Directly assaying social preferences of infected hosts is needed to elucidate potential changes in social preferences that may act as a form of behavioral tolerance (defined as using behavior to minimize fitness costs of infection). We tested how infection alters sociality in juvenile house finches (Haemorhous mexicanus), which are both highly gregarious and particularly susceptible to infection by the bacterial pathogenMycoplasma gallisepticum(MG). We inoculated 33 wild‐caught but captive‐held juvenile house finches with MG or media (sham control). At peak infection, birds were given a choice assay to assess preference for associating near a flock versus an empty cage. We then repeated this assay after all birds had recovered from infection. Infected birds were significantly more likely than controls to spend time associating with, and specifically foraging near, the flock. However, after infected birds had recovered from MG infection, there were no significant differences in the amount of time birds in each treatment spent with the flock. These results indicate augmented social preferences during active infection, potentially as a form of behavioral tolerance. Notably, infected birds showed strong social preferences regardless of variation in disease severity or pathogen loads, with 14/19 harboring high loads (5–6 log₁₀copies of MG) at the time of the assay. Overall, our results show that infection with a directly transmitted pathogen can augment social preferences, with important implications for MG spread in natural populations.

 

Animal hosts can adapt to emerging infectious disease through both disease resistance, which decreases pathogen numbers, and disease tolerance, which limits damage during infection without limiting pathogen replication. Both resistance and tolerance mechanisms can drive pathogen transmission dynamics. However, it is not well understood how quickly host tolerance evolves in response to novel pathogens or what physiological mechanisms underlie this defense. Using natural populations of house finches ( Haemorhous mexicanus ) across the temporal invasion gradient of a recently emerged bacterial pathogen ( Mycoplasma gallisepticum ), we find rapid evolution of tolerance (<25 years). In particular, populations with a longer history of MG endemism have less pathology but similar pathogen loads compared with populations with a shorter history of MG endemism. Further, gene expression data reveal that more-targeted immune responses early in infection are associated with tolerance. These results suggest an important role for tolerance in host adaptation to emerging infectious diseases, a phenomenon with broad implications for pathogen spread and evolution. 

How directly transmitted pathogens benefit from harming hosts is key to understanding virulence evolution. It is recognized that pathogens benefit from high within-host loads, often associated with virulence. However, high virulence may also directly augment spread of a given amount of pathogen, here termed ‘spreadability’. We used house finches and the conjunctival pathogen Mycoplasma gallisepticum to test whether two components of virulence—the severity of conjunctival inflammation and behavioural morbidity produced—predict pathogen spreadability. We applied ultraviolet powder around the conjunctiva of finches that were inoculated with pathogen treatments of distinct virulence and measured within-flock powder spread, our proxy for ‘spreadability’. When compared to uninfected controls, birds infected with a high-virulence, but not low-virulence, pathogen strain, spread significantly more powder to flockmates. Relative to controls, high-virulence treatment birds both had more severe conjunctival inflammation—which potentially facilitated powder shedding—and longer bouts on feeders, which serve as fomites. However, food peck rates and displacements with flockmates were lowest in high-virulence treatment birds relative to controls, suggesting inflammatory rather than behavioural mechanisms likely drive augmented spreadability at high virulence. Our results suggest that inflammation associated with virulence can facilitate pathogen spread to conspecifics, potentially favouring virulence evolution in this system and others. 

DNA‐based methods to measure the abundance and relative abundance of bacterial taxa can be skewed by the presence of dead or transient bacteria. Consequently, the active, functional members of the community may be a small subset of the detected bacterial community. This mismatch can make inferences about the roles of communities in host health difficult and can be particularly problematic for low‐abundance microbiomes, such as those on conjunctival surfaces. In this study, we manipulated bacterial communities on bird conjunctiva with a bacteriostatic antibiotic, reducing bacterial activity while preserving viability, to identify the living and active conjunctival communities using comparisons of 16S ribosomal DNA and RNA in paired samples. DNA amplicons included many more sequence variants than RNA amplicons from the same communities, with consequent differences in diversity. While we found that changes in communities in DNA samples broadly represent shifts in the living (RNA‐amplicon) communities, assessments of community function may be better described by RNA samples, reducing background noise from dead cells. We further used these data to test RNA:DNA ratios, used in other microbiological contexts, to detect shifts in bacterial activity after antibiotic disruption but were unable to detect changes in bacterial activity with this method.

 

ABSTRACT Free-living hosts encounter pathogens at a wide range of frequencies and concentrations, including low doses that are largely aclinical, creating a varied landscape of exposure history and reinfection likelihood. While several studies show that higher priming doses result in stronger immunological protection against reinfection, it remains unknown how the reinfection challenge dose and priming dose interact to determine the likelihood and severity of reinfection. We manipulated both priming and challenge doses of Mycoplasma gallisepticum , which causes mycoplasmal conjunctivitis, in captive house finches ( Haemorhous mexicanus ), to assess reinfection probability and severity. We found a significant interaction between priming and challenge doses on reinfection probability, with the likelihood of reinfection by a high but not a low challenge dose decreasing exponentially at higher priming doses. While this interaction was likely driven by lower average infection probabilities for low-dose versus high-dose challenges, even the highest priming dose provided only negligible protection against reinfection from low-dose challenges. Similarly, pathogen loads during reinfection were significantly reduced with increasing priming doses only for birds reinfected at high but not low doses. We hypothesize that these interactions arise to some degree from fundamental differences in host immune responses across doses, with single low doses only weakly triggering host immune responses. Importantly, our results also demonstrate that reinfections can occur from a variety of exposure doses and across diverse degrees of standing immunity in this system. Overall, our study highlights the importance of considering both initial and subsequent exposure doses where repeated exposure to a pathogen is common in nature. 

Bacterial communities in and on wild hosts are increasingly appreciated for their importance in host health. Through both direct and indirect interactions, bacteria lining vertebrate gut mucosa provide hosts protection against infectious pathogens, sometimes even in distal body regions through immune regulation. In house finches ( Haemorhous mexicanus ), the bacterial pathogen Mycoplasma gallisepticum (MG) causes conjunctivitis, with ocular inflammation mediated by pro- and anti-inflammatory cytokines and infection triggering MG-specific antibodies. Here, we tested the role of gut bacteria in host responses to MG by using oral antibiotics to perturb bacteria in the gut of captive house finches prior to experimental inoculation with MG. We found no clear support for an impact of gut bacterial disruption on conjunctival pathology, MG load, or plasma antibody levels. However, there was a non-significant trend for birds with intact gut communities to have greater conjunctival pathology, suggesting a possible impact of gut bacteria on pro-inflammatory cytokine stimulation. Using 16S bacterial rRNA amplicon sequencing, we found dramatic differences in cloacal bacterial community composition between captive, wild-caught house finches in our experiment and free-living finches from the same population, with lower bacterial richness and core communities composed of fewer genera in captive finches. We hypothesize that captivity may have affected the strength of results in this experiment, necessitating further study with this consideration. The abundance of anthropogenic impacts on wildlife and their bacterial communities, alongside the emergence and spread of infectious diseases, highlights the importance of studies addressing the role of commensal bacteria in health and disease, and the consequences of gut bacterial shifts on wild hosts. 

ABSTRACT The commensal microbes inhabiting a host tissue can interact with invading pathogens and host physiology in ways that alter pathogen growth and disease manifestation. Prior work in house finches (Haemorhous mexicanus) found that resident ocular microbiomes were protective against conjunctival infection and disease caused by a relatively high dose of Mycoplasma gallisepticum. Here, we used wild-caught house finches to experimentally examine whether protective effects of the resident ocular microbiome vary with the dose of invading pathogen. We hypothesized that commensal protection would be strongest at low M. gallisepticum inoculation doses because the resident microbiome would be less disrupted by invading pathogen. Our five M. gallisepticum dose treatments were fully factorial with an antibiotic treatment to perturb resident microbes just prior to M. gallisepticum inoculation. Unexpectedly, we found no indication of protective effects of the resident microbiome at any pathogen inoculation dose, which was inconsistent with the prior work. The ocular bacterial communities at the beginning of our experiment differed significantly from those previously reported in local wild-caught house finches, likely causing this discrepancy. These variable results underscore that microbiome-based protection in natural systems can be context dependent, and natural variation in community composition may alter the function of resident microbiomes in free-living animals. 

Abstract An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution.