Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade‐offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The ‘fecundity advantage hypothesis’ predicts female‐biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis‐causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in‐nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12‐year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host–parasite system.

The parasitic larvae of Philornis downsi Dodge & Aitken (Diptera: Muscidae) were first discovered in Darwin's finch nests on the Galápagos Islands in 1997. Larvae of P. downsi consume the blood and tissue of developing birds, causing high in-nest mortality in their Galápagos hosts. The fly has been spreading across the archipelago and is considered the biggest threat to the survival of Galápagos land birds. Here, we review (1) Philornis systematics and taxonomy, (2) discuss shifts in feeding habits across Philornis species comparing basal to more recently evolved groups, (3) report on differences in the ontogeny of wild and captive P. downsi larvae, (4) describe what is known about adult P. downsi behaviour, and (5) discuss changes in P. downsi behaviour since its discovery on the Galápagos Islands. From 1997 to 2010, P. downsi larvae have been rarely detected in Darwin's finch nests with eggs. Since 2012, P. downsi larvae have regularly been found in the nests of incubating Darwin's finches. Exploring P. downsi ontogeny and behaviour in the larger context of taxonomic relationships provides clues about the breadth of behavioural flexibility that may facilitate successful colonisation.

When different introduced species across trophic levels (parasite, predator) invade island systems, they may pose significant threats to nesting birds. In this study, we measure nesting height and infer causes of offspring mortality in the critically endangered Medium Tree Finch (Camarhynchus pauper), an island endemic restricted to Floreana Island on the Galápagos Archipelago. Considering all nests at which a male built a nest, sang and attempted to attract a female (n = 222 nests), only 10.4% of nests produced fledglings (5% of nests had total fledging success, 5.4% of nests had partial fledging success). Of the 123 nests chosen by a female, 18.7% produced fledglings and of 337 eggs laid, 13.4% produced fledglings. Pairing success was higher for older males, but male age did not predict nesting success. All nests with chicks were infested with avian vampire fly larvae (Philornis downsi). We attributed the cause of death to avian vampire fly if chicks were found dead in the nest with fly larvae or pupae (45%) present. We inferred avian (either Asio flammeus galapagoensis or Crotophaga ani) predation (24%) if the nest was empty but dishevelled; and black rat (Rattus rattus) predation (20%) if the nest was empty but undamaged. According to these criteria, the highest nests were depredated by avian predators, the lowest nests by rats, and intermediate nests failed because of avian vampire fly larvae. In conclusion, there is no safe nesting height on Floreana Island under current conditions of threats from two trophic levels (introduced parasitic dipteran, introduced mammalian/avian predators; with Galápagos Short-Eared Owls being the only native predator in the system).

In invasive parasites, generalism is considered advantageous during the initial phase of introduction. Thereafter, fitness costs to parasites, such as host-specific mortality, can drive parasites towards specialism to avoid costly hosts. It is important to determine changes in host specificity of invasive populations to understand host-parasite dynamics and their effects on vulnerable host populations. We examined changes in mortality in the introduced avian vampire fly (Philornis downsi) (Diptera: Muscidae), a generalist myasis-causing ectoparasite, between 2004 and 2020 on Floreana Island (Galápagos). Mortality was measured as the proportion of immature larvae found upon host nest termination. Over the time period, the avian vampire fly was most abundant and had low mortality in nests of the critically endangered medium tree finch (Camarhynchus pauper) and had the highest mortality in nests of hybrid tree finches (Camarhynchus spp.). Low larval mortality was also found in small tree (Camarhynchus parvulus) and small ground finch (Geospiza fuliginosa) nests. Selection could favour avian vampire flies that select medium tree finch nests and/or avoid hybrid nests. Overall, the finding of differences in avian vampire fly survival across host species is parsimonious with the idea that the introduced fly may be evolving towards host specialisation.

Due to novel or dynamic fluctuations in environmental conditions and resources, host and parasite relationships can be subject to diverse selection pressures that may lead to significant changes during and after invasion of a parasite. Genomic analyses are useful for elucidating evolutionary processes in invasive parasites following their arrival to a new area and host. Philornis downsi (Diptera: Muscidae), the avian vampire fly, was introduced to the Galápagos Islands circa 1964 and has since spread across the archipelago, feeding on the blood of developing nestlings of endemic land birds. Since its discovery, there have been significant changes to the dynamics of P. downsi and its novel hosts, such as shifting mortality rates and changing oviposition behaviour, however no temporal genetic studies have been conducted. We collected P. downsi from nests and traps from a single island population over a 14-year period, and genotyped flies at 469 single nucleotide polymorphisms (SNPs) using restriction-site associated DNA sequencing (RADSeq). Despite significant genetic differentiation (FST) between years, there was no evidence for genetic clustering within or across four sampling years between 2006 and 2020, suggesting a lack of population isolation. Sibship reconstructions from P. downsi collected from 10 Darwin’s finch nests sampled in 2020 showed evidence for shifts in reproductive behaviour compared to a similar genetic analysis conducted in 2004–2006. Compared with this previous study, females mated with fewer males, individual females oviposited fewer offspring per nest, but more unique females oviposited per nest. These findings are important to consider within reproductive control techniques, and have fitness implications for both parasite evolution and host fitness.