Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird.

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.

Let's stick together: Infection enhances preferences for social grouping in a songbird species.

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 pathogen Mycoplasma 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 log10 copies 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.

EFFECTS OF MYCOPLASMA GALLISEPTICUM INFECTION ON PREENING BEHAVIORS AND FEATHER QUALITY IN HOUSE FINCHES (HAEMORHOUS MEXICANUS).

Infections can have far-reaching sublethal effects on wildlife, including reduced maintenance of external structures. For many wildlife taxa, daily maintenance of external structures (termed preening in birds) is critical to fitness, but few studies have examined how infections alter such maintenance. Mycoplasma gallisepticum is a common pathogen in free-living House Finches (Haemorhous mexicanus), where it causes mycoplasmal conjunctivitis. Despite documented behavioral changes associated with M. gallisepticum infections in finches, no studies have examined how preening behavior may change with infection and how potential differences in preening may affect feather quality. To test this, we experimentally inoculated captive House Finches with M. gallisepticum or a control treatment, and we collected behavioral and feather quality data to detect potential changes in feather maintenance due to infection. We found that finches infected with M. gallisepticum preened significantly less often, and within the infected treatment, birds with the highest conjunctivitis severity preened the least often. However, there was no difference in the quality scores for secondary flight feathers collected from control versus infected birds. We also assayed feather water retention and found that the degree of water retention correlated with our feather quality scores, such that feathers with poor scores retained more water. However, as with quality scores, feather water retention did not differ with infection; this may be due to the controlled environment that the birds experienced while in captivity. Our data suggest that, in addition to sickness behaviors previously observed in finches, M. gallisepticum infection decreases other behaviors critical to survival, such as preening. While the consequences of reduced preening on feather maintenance were not apparent in captive conditions, further work is needed to determine whether House Finches in the wild that are infected with M. gallisepticum experience a fitness cost, such as increases in ectoparasite loads, due to this reduced feather maintenance.

Antibiotic perturbation of gut bacteria does not significantly alter host responses to ocular disease in a songbird species.

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.