Genetics reveals shifts in reproductive behaviour of the invasive bird parasite Philornis downsi collected from Darwin’s finch nests

Abstract

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.