Early-life parasitism can negatively impact the growth, development, and survival of animal hosts. Parasitism can also positively influence developmental processes that increase host resistance, fecundity, and survival. Established processes include the development of resistance barriers, immune priming and training, acquired resistance, and behavior. However, few studies have calculated the overall, net effect of early-life parasitism on host fitness, and instead have focused on a particular life stage or just the cause (e.g., immune response) or consequence (e.g., survival). Indeed, several challenges prevent progress, including immune response specificity, dose-dependent immune responses, logistical feasibility, and analyzing imperfect datasets. Going forward, an integrative approach is needed to address the roadblocks that the field is currently facing.

Invasive parasites are a major threat to naive, island hosts, who often deal with multiple parasite taxa (hereon, co-parasitism). These parasite taxa can positively or negatively affect each other through the host’s immune system, which can depend on the order of exposure (i.e., priority effects). Several parasite taxa, such as the avian vampire fly (Philornis downsi) and avian pox virus, were introduced to the Galápagos Islands and negatively affect endemic birds, such as Darwin’s finches. Although finches can be parasitized by both taxa, the effect of co-parasitism on finches and the dynamics between parasite taxa are unknown. For our study, we experimentally manipulated vampire fly abundance in the nests of small ground finch (Geospiza fuliginosa), then determined the effect of treatment on the prevalence of avian pox in nestlings. We also determined whether nestlings parasitized by flies and/or pox differed in body condition, hemoglobin levels (proxy for blood loss), and survival. We found that nestlings from fly-parasitized nests were less likely to test positive for pox than nestlings from nests with flies. Additionally, nestlings with low (0) and high (>40) fly abundances were more likely to test positive for pox compared to nestlings with intermediate abundances (10-30). Although co-parasitism did not affect nestling condition and survival, co-parasitized nestlings had lower hemoglobin levels than nestlings with no or only one parasite taxa. Overall, our study supports the presence of priority effects, in which flies help nestlings resist pox infection until fly numbers are too high for nestlings to defend themselves.

The gut microbiome regulates multiple aspects of host health, including metabolism and the development of the immune system. Despite this, we still know relatively little about how the gut microbiome influences host responses to parasitism in wild organisms, particularly whether interactions between gut microbiota and host physiology contribute to variation in parasitism across host species. The goal of this study was to determine the role of gut microbiota in shaping how birds respond to nest parasites and investigate whether this relationship varies between host species. Both eastern bluebirds (Sialia sialis) and tree swallows (Tachycineta bicolor) are parasitized by blow flies (Protocalliphora sialia) which produce larvae that feed on nestlings’ blood. We experimentally manipulated the gut microbiota of nestling bluebirds and tree swallows by dosing nestlings with an oral antibiotic or sterile water as a control. We then quantified nestling physiology (hemoglobin, glucose, parasite specific IgY antibodies), body morphometrics, and survival until fledging, as well as nest parasite abundance and size. We found that an experimental disruption of nestling gut microbiota increased parasite abundance in tree swallows, but decreased parasite abundance in bluebirds. Treatment with antibiotics was associated with delayed parasite development, including reduced pupation volume of parasites found as larvae in bluebird nests. Similarly, antibiotic treatment was associated with larger size differences in pupal volume between parasites found as larvae and pupae in swallow nests. Both antibiotic treatment and parasite abundance had variable effects on nestling body morphometrics and physiology across the two host species. Together, these results suggest that gut microbiota contribute to host differences in resistance to P. sialia and can influence host-parasite interactions.

Host-associated microbiota can be affected by factors related to environmental change, such as urbanization and invasive species. For example, urban areas often affect food availability for animals, which can change their gut microbiota. Invasive parasites can also influence microbiota through either competition or indirectly through a change in the host immune response. These interacting factors can have complex effects on host fitness, but few studies have disentangled the relationship between urbanization and parasitism on an organism’s gut microbial composition. To address this gap in knowledge, we investigated the effects of urbanization and parasitism by the invasive avian vampire fly (Philornis downsi) on the gut microbiota of nestling small ground finches (Geospiza fuliginosa) on San Cristóbal Island, Galápagos. We conducted a factorial study in which we experimentally manipulated parasite presence in an urban and non-urban area. Feces were then collected when nestlings to characterize the gut microbiota (i.e., alpha and beta diversity, community composition). Although we did not find an interactive effect of urbanization and parasitism on the microbiota, we did find main effects of each variable. Urban and parasitized nestlings had lower bacterial diversity and differences in relative abundance of bacterial phyla and genera compared to non-urban non-parasitized nestlings, respectively. Overall, this study advances our understanding of the complex effects of anthropogenic stressors on the gut microbiota of birds.