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ABSTRACT Studies of symbiosis employ the term “parasitism” to connote different sorts of relationships. Within the context of mutualistic symbioses, parasites are otherwise cooperative individuals or strains that appropriate a disproportionate amount of the synergistic products. In the context of antagonistic symbioses, there is no pretence of cooperation, and instead parasites are defined as individuals or strains that derive fitness benefits at a fitness cost to their hosts. In both cases, parasitism is selected for at the lower level (that of the individual symbiont) but selected against at the higher level (the group of symbionts in a single host). Despite these similarities, these different sorts of parasitism likely evolve by different pathways. Once a host–symbiont relationship initiates, if functional synergy is lacking, the relationship will remain exploitative, although parasites may differ in their detrimental effects on the host and the higher‐level unit. If functional synergy is present, however, cooperation may develop with benefits for both host and symbionts (i.e. mutualism). Nevertheless, parasites may still evolve from within these incipient relationships when individuals or strains of symbionts act parasitically by defecting from the common good to further their selfish replication. Levels‐of‐selection dynamics thus underlie both forms of parasitism, but only in the case of latent functional synergy can true symbiotic complexity at the higher level emerge. 

Abstract Human activity changes multiple factors in the environment, which can have positive or negative synergistic 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 urban and non‐urban locations and then characterized nestling health, fledging success, diet, and gene expression patterns related to host defense. Fledging success of non‐parasitized nestlings from urban (79%) and non‐urban (75%) nests did not differ significantly. However, parasitized, non‐urban nestlings lost more blood, and fewer nestlings survived (8%) compared to urban nestlings (50%). Stable isotopic values (δ¹⁵N) from urban nestling feces were higher than those from 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 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.