Urban living can rescue Darwin’s finches from the lethal effects of invasive vampire flies

Abstract

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 Galápagos 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 fumigated nestlings from urban and non-urban nests did not differ significantly. However, sham-fumigated, non-urban nestlings lost more blood and few nestlings survived compared to urban nestlings. Stable isotopic values (δ¹⁵N) from urban nestling feces were higher than non-urban nestlings, suggesting that urban nestlings are consuming more protein. 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 sham-fumigated non-urban nestlings. In contrast, sham-fumigated 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.