Human activity changes multiple factors in the environment, which can have additive or neutralizing effects on organisms. However, few studies have explored the causal effects of multiple anthropogenic factors, such as urbanization and invasive species, on animals, and the mechanisms that mediate these interactions. This study examines the influence of urbanization on the detrimental effect of invasive avian vampire flies (Philornis downsi) on endemic Darwin's finches in the Galapagos Islands. We experimentally manipulated nest fly abundance in an urban and non-urban area and then characterized nestling health, survival, diet, and gene expression patterns related to host defense. Survival of non-parasitized nestlings from urban (85%) and non-urban (78%) nests did not differ significantly. However, parasitized, non-urban nestlings lost more blood and had lower survival (7%) compared to urban nestlings (50%). Stable isotopic values (δ15N) from nestling feces revealed that diet differed between urban and non-urban nestlings. δ15N values correlated negatively with parasite abundance, which suggests that diet might influence host defenses (e.g., tolerance and resistance). Parasitized urban nestlings differentially expressed genes within pathways associated with red blood cell production (tolerance) and pro-inflammatory response (innate immunological resistance), compared to parasitized non-urban nestlings. In contrast, parasitized non-urban nestlings differentially expressed genes within pathways associated with immunoglobulin production (adaptive immunological resistance). Our results suggest that urban nestlings are investing more in pro-inflammatory responses to resist parasites, but also recovering more blood cells to tolerate blood loss. Although non-urban nestlings are mounting an adaptive immune response, it is likely a last effort by the immune system rather than an effective defense against avian vampire flies since few nestlings survived.
Hosts have developed or evolved defense strategies, including tolerance and resistance, to reduce damage caused by parasites. Environmental factors, such as elevated temperature, can influence the effectiveness of these different host defenses but also can directly affect parasite fitness. Therefore, the net effect of elevated temperature on host-parasite relationships are determined by its direct effects on the host and the parasite. Furthermore, because host species can defend themselves differently against their parasites, the net effect of temperature might differ across each hosts interaction with the same parasite. Few studies have determined the net effects of temperature on both host defenses and parasites in a multi-host system. To address this gap, we experimentally manipulated temperature and parasite presence in the nests of two host species who defend themselves differently to the same parasitic nest fly (Protocalliphora sialia). Specifically, we conducted a factorial experiment by increasing temperature (or not) and removing all parasitic nest flies (or not) in the nests of tolerant eastern bluebirds (Sialia sialis) and resistant tree swallows (Tachycineta bicolor). We then quantified parasite load in nests and measured nestling body size metrics, blood loss, and survival. If temperature predominately affected parasite fitness, then elevated temperature would cause similar directional effects on parasite abundance across species. If temperature has different effects on hosts, then parasite abundance would differ in response to elevated temperature across host species. In contrast to previous years, we found that bluebird nests had half as many parasites as compared to swallow nests. Elevated temperature affected parasite abundance differently in each host species. Swallows from heated nests had fewer parasites compared to non-heated nests, suggesting that they were more resistant to the parasites. Interestingly, swallows from heated nests were also more tolerant to the effects of parasites than controls. In contrast, bluebirds from heated nests had more parasites and lower body mass compared to controls, suggesting that they lost tolerance, and resistance, to the parasites. Our results suggest that a changing climate could have complex net effects on host-parasite interactions, including on host defenses, with implications for host health and parasite survival.
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