Abstract
Among the most common parasites of Drosophila in nature are parasitoid wasps, which lay their eggs in fly larvae and pupae. D. melanogaster larvae can mount a cellular immune response against wasp eggs, but female wasps inject venom along with their eggs to block this immune response. Genetic variation in flies for immune resistance against wasps and genetic variation in wasps for virulence against flies largely determines the outcome of any fly-wasp interaction. Interestingly, up to 90% of the variation in fly resistance against wasp parasitism has been linked to a very simple mechanism: flies with increased constitutive blood cell (hemocyte) production are more resistant. However, this relationship has not been tested for Drosophila hosts outside of the melanogaster subgroup, nor has it been tested across a diversity of parasitoid wasp species and strains. We compared hemocyte levels in two fly species from different subgroups, D. melanogaster and D. suzukii, and found that D. suzukii constitutively produces up to five times more hemocytes than D. melanogaster. Using a panel of 24 parasitoid wasp strains representing fifteen species, four families, and multiple virulence strategies, we found that D. suzukii was significantly more resistant to wasp parasitism than D. melanogaster. Thus, our data suggest that the relationship between hemocyte production and wasp resistance is general. However, at least one sympatric wasp species was a highly successful infector of D. suzukii, suggesting specialists can overcome the general resistance afforded to hosts by excessive hemocyte production. Given that D. suzukii is an emerging agricultural pest, identification of the few parasitoid wasps that successfully infect D. suzukii may have value for biocontrol.
Highlights
Fruitflies of the genus Drosophila are regularly attacked by parasitoid wasps
The previous studies were limited to flies in the melanogaster subgroup and to a few wasp species/strains that represent only a small fraction of the diverse virulence strategies used by Drosophila parasitoid wasps
To determine if increased hemocyte production by flies is a panacea against wasp infection, we first compared hemocyte numbers between D. melanogaster and D. suzukii, a relative of D. melanogaster outside the melanogaster subgroup
Summary
Fruitflies of the genus Drosophila are regularly attacked by parasitoid wasps. In natural D. melanogaster populations, upwards of 50% of fly larvae are found to be infected by wasps, suggesting they exert extremely strong selection pressures on Drosophila populations in nature [1,2,3]. Fruitfly larvae mount an immune response against wasp eggs, termed melanotic encapsulation, that is thought to involve several steps [4,5]: The response begins when circulating, constitutively produced plasmatocytes recognize the wasp egg as foreign and signal to induce the differentiation of larger lamellocytes from pro-hemocytes in the lymph gland (the fly hematopoietic organ) and from other circulating plasmatocytes (via the intermediate podocyte form) [6,7] These newly derived lamellocytes migrate towards, and attach and spread around the wasp egg in a multi-layered capsule. There is both between and within species genetic variation in flies for resistance against wasps and among wasps for virulence against flies [8,9,10,11,12,13,14,15,16]
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