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 ~17% P. downsi mortality in host nests with 55 ± 6.2 % host mortality, and a trend of ~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 ~32%, and male (~6%) and female adult size (~11%) decreased. Notably, females had ~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.

In this study we use nine years of field data spanning a 12-year period to examine changes in body size (an indirect measure of fecundity) in the dipteran ectoparasite, P. downsi, in response to the increasingly earlier death of its host. We monitored 116 Darwin’s finch nests for nesting outcome using our well-established field protocols. Upon nesting termination (fledging or death of the last nestling), each nest was collected in a sealed plastic bag, and all P. downsi larvae, pupae, empty puparia and adult flies were counted within 1-24 hours of collection. All P. downsi samples were stored in 90% ethanol immediately after counting. Philornis downsi intensity in the nest was measured as the total number of larvae, pupae, puparia and adult flies present upon collection of the nest. The sample size per year and host genus (Camarhynchus, Geospiza) is provided in Table S1.

We placed a total of 114 McPhail Traps in the lowlands and highlands of Santa Cruz and Floreana Island to sample adult P. downsi flies in the years 2004, 2005, 2012, 2013 and 2014 (for details see Table S1). The McPhail traps were baited with a liquid lure of blended papaya, water and white sugar (following trapping protocol developed by P. Lincango and C. Causton) that was replaced every 7 days. Traps were hung in trees along 4 x 90m transects and flies were collected twice per week and stored in ethanol. In 2014 on Floreana Island, we placed 28 McPhail traps along four transects, seven traps per transect, at heights of 2 to 7 metres. In other years and locations, traps were placed ad hoc every 50 m within 100 m x 200 m plots spanning a 2 km transect within study sites. We analysed data from 46 lowland traps and 68 highland traps (Table S1).

Mass (g), length and width (mm) were measured for each pupa, as these measurements are known to be highly correlated with adult fly size and can therefore be an indirect indicator of an individuals' fecundity upon maturity. Pupae cannot be sexed, therefore these data could not be used for sexual dimorphism analysis but are useful when looking at general temporal shifts in body size in the P. downsi population. All pupae were removed from ethanol and placed on filter paper to dry for 30 seconds before taking measurements. We measured the total mass of all intact pupae per nest and divided this by the number of pupae to calculate average pupa mass. The pupae were weighed to the nearest 0.001 g using an A&D HR-200 Digital Analytical Balance. The length (mm) and width (mm) of the largest pupa per nest was measured using digital callipers. For analysis we used the average mass per nest. Pupa mass was measured from the nests of 19 C. parvulus (268 pupae), 10 hybrid Camarhynchus tree finch (55 pupae), 25 C. pauper (332 pupae), 57 Geospiza fuliginosa (816 pupae) and 5 G. fortis (52 pupae) (Table S1).