Coordinated molecular and ecological adaptations underlie a highly successful parasitoid

Reviewer #1 (Public Review):

Summary:

Major findings or outcomes include a genome for the wasp, characterization of the venom constituents and teratocyte and ovipositor expression profiles, as well as information about Trichopria ecology and parasitism strategies. It was found that Trichopria cannot discriminate among hosts by age, but can identify previously parasitized hosts. The authors also investigated whether superparasitism by Trichopria wasps improved parasitism outcomes (it did), presumably by increasing venom and teratocyte concentrations/densities. Elegant use of Drosophila ectopic expression tools allowed for functional characterization of venom components (Timps), and showed that these proteins are responsible for parasitoid-induced delays in host development. After finding that teratocytes produce a large number of proteases, experiments showed that these contribute to digestion of host tissues for parasite consumption.
The discussion ties these elements together by suggesting that genes used for aiding in parasitism via different parts of the parasitism arsenal arise from gene duplication and shifts in tissue of expression (to venom glands or teratocytes).

Strengths:

The strength of this manuscript is that it describes the parasitism strategies used by Trichopria wasps at a molecular and behavioral level with broad strokes. It represents a large amount of work that in previous decades might have been published in several different papers. Including all of these data in a manuscript together makes for a comprehensive and interesting study.

Weaknesses:

The weakness is that the breadth of the study results in fairly shallow mechanistic or functional results for any given facet of Trichopria's biology. Although none of the findings are especially novel given results from other parasitoid species in previous publications, integrating results together provides significant information about Trichopria biology.

Reviewer #2 (Public Review):

Summary:

Key findings of this research include the sequencing of the wasp's genome, identification of venom constituents and teratocytes, and examination of Trichopria drosophilae (Td)'s ecology and parasitic strategies. It was observed that Td doesn't distinguish between hosts based on age but can recognize previously parasitized hosts. The study also explored whether multiple parasitisms by Td improved outcomes, which indeed it did, possibly by increasing venom and teratocyte levels. Utilizing Drosophila ectopic expression tools, the authors functionally characterized venom components, specifically tissue inhibitors of metalloproteinases (Timps), which were found to cause delays in host development. Additionally, experiments revealed that teratocytes produce numerous proteases, aiding in the digestion of host tissues for parasite consumption. The discussion suggests that genes involved in different aspects of parasitism may arise from gene duplication and shifts in tissue expression to venom glands or teratocytes.

Strengths:

This manuscript provides an in-depth and detailed depiction of the parasitic strategies employed by Td wasps, spanning both molecular and behavioral aspects. It consolidates a significant amount of research that, in the past, might have been distributed across multiple papers. By presenting all this data in a single manuscript, it delivers a comprehensive and engaging study that could help future developments in the field of biological control against a major insect pest.

Weaknesses:

While none of the findings are particularly groundbreaking, as similar results have been reported for other parasitoid species in prior research, the integration of these results into one comprehensive overview offers valuable biological insights into an interesting new potential biocontrol species.