Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin’s finches

Abstract

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.

Effect of an introduced parasite in natural and anthropogenic habitats on the breeding success of the endemic little vermilion flycatcher Pyrocephalus nanus in the Galápagos

“…Long term studies on Darwin's finches showed that in recent years P. downsi infests nests earlier in the breeding cycle of the hosts (Cimadom et al ) and thus leads also to earlier host death. Interestingly, a recent study suggests that earlier host death due to P. downsi selects for faster pupation and thereby for smaller body size and hence lower fecundity in female adult flies (Common et al ), which over time could ease harm of P. downsi to Galápagos landbirds.…”

Female in-nest attendance predicts the number of ectoparasites in Darwin's finch species

“…Since 2004, there have been measurable shifts in P. downsi and host behaviour on both islands. Philornis downsi oviposition and hatching have shifted towards earlier in the host incubation period on Santa Cruz Island, whereas P. downsi hatching (and perhaps oviposition) occurs during chick feeding on Floreana [ 35 , 52 , 88 ]. On Floreana Island, the proportion of hybrid tree finches in the population increased to 55% in 2006 and has since remained at approximately 40% [ 43 , 45 ], and higher admixture (e.g.…”

“…Once the nesting event had finished (i.e. the offspring had died or fledged), as confirmed by our routine nest monitoring, the nest was immediately collected from the field, stored in a plastic bag and transported to our on-site laboratory later in the day to count the number of P. downsi larvae, pupae and puparia [ 52 ]. Generally, all P. downsi were counted within 6 h and a maximum of 24 h post-nest collection.…”

“…The P. downsi specimens from each nest were preserved in separate tubes containing 70% ethanol. We recorded the number of P. downsi per instar phase, though first and second instar were confirmed later with a microscope [ 52 , 53 ]. Here, we analysed the total number of P. downsi per nest as our main variable of interest and in relation to chick age at the time of nesting termination.…”

Shifting microbiomes complement life stage transitions and diet of the bird parasite Philornis downsi from the Galapagos Islands

“…Flexible associations may evolve distinct functional roles that eventually support speciation, as presumably in Drosophila flies and Cephalodia beetles, where specific microbial communities are associated with host species in ways that support exclusive dietary niches (Martinson et al, 2017;Blankenchip et al, 2018). Similarly, the parasitic habit of P. downsi is an evolved trait that is thought to be derived from ancestral saprophagy, where larvae developed by scavenging on excrement and organic debris in avian nests, (Couri et al, 2007;Dudaniec and Kleindorfer, 2016;Common et al, 2020). Radiation into this new dietary niche probably required the adoption of and adaptation to a new set of gut bacteria, which may have eventually contributed to S8).…”