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Dear Dr. Jandausch and colleagues:
Thanks for revising your manuscript based on the concerns raised by the reviewers. I now believe that your manuscript is suitable for publication. Congratulations! I look forward to seeing this work in print, and I anticipate it being an important resource for groups studying strepsipteran biology. Thanks again for choosing PeerJ to publish such important work.
Best,
-joe
[# PeerJ Staff Note - this decision was reviewed and approved by Michael Wink, a PeerJ Section Editor covering this Section #]
Dear Dr. Jandausch and colleagues:
Thanks for submitting your manuscript to PeerJ. I have now received three independent reviews of your work, and as you will see, the reviewers raised some minor concerns about the manuscript. Despite this, these reviewers are highly optimistic about your work and the potential impact it will lend to research on strepsipteran biology. Thus, I encourage you to revise your manuscript, accordingly, taking into account all of the concerns raised by the reviewers.
While the concerns of the reviewers are relatively minor, this is a major revision to ensure that the original reviewers have a chance to evaluate your responses to their concerns.
Please note that reviewers 1 and 2 have included marked-up versions of your manuscript.
Importantly, please add the references considered by the reviewers to be important for placing your study within the full context of the system. Please also ensure that access to all supporting material is available.
I look forward to seeing your revision, and thanks again for submitting your work to PeerJ.
Good luck with your revision,
Best,
-joe
[# PeerJ Staff Note: It is PeerJ policy that additional references suggested during the peer-review process should only be included if the authors are in agreement that they are relevant and useful #]
[# PeerJ Staff Note: Please ensure that all review and editorial comments are addressed in a response letter and any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate. #]
BASIC REPORTING Clear, professional English language used throughout. Relevant literature is lacking. The structure conforms to PeerJ standards. High quality figures, well labelled. Raw data supplied.
EXPERIMENTAL DESIGN Original primary research within Scope of the journal. Research question in Stylops well defined, not equally in Xenos. High technical & ethical standard. Methods detailed.
VALIDITY OF THE FINDINGS High impact and novelty. Literature is clearly stated for Stylops but incomplete for Xenos. Data are robust and statistically controlled. Conclusions support results.
General comments, criticisms and suggestions
INTRODUCTION
Abstract is perfect, while Introduction could be shortened to be more effective. For example, omit any information on Mengenillidae (lines 50-52, 77-78, 82-83, 111-113).
Given the topic – traumatic insemination - I suggest avoiding the term “copulate” (76), “copulation” (90), “copulate” (311), sensu Eberhard (1995, p.69): “copulation (genitalic coupling of male and female) is not equivalent to insemination.”
89-90: “the secondary copulation opening”: unclear. Do you mean that this opening “is used in most species for insemination” (93-94)? My suggestion is to quote and discuss a study on Xenos vesparum in which this alternative sperm routes have been described, besides traumatic insemination. This study describes - with scanning and transmission electron microscopy - two routes by which sperm cells can reach the hemocoel, hypodermic insemination and/or extragenital insemination via ventral canal (compare Fig.5 with Fig.2B in this ms).
Beani, L., Giusti, F., Mercati, D., Lupetti, P., Paccagnini, E., Turillazzi, S., & Dallai, R. (2005). Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. Journal of Morphology, 265(3), 291-303.
MATERIAL AND METHODS
161-163: preference of Xenos vesparum for Campsis radicans has been described in detail in a recent study. Add this reference, please, and briefly comment the altered feeding of parasitized wasps. I wonder if Andrena vaga bees change their behavior if parasitized as well as X. vesparum, for example if they aggregate and thus facilitate parasite’s mating.
Beani, L., Cappa, F., Manfredini, F., & Zaccaroni, M. (2018). Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite. PloS one, 13(10), e0205201.
I appreciated the integrated methods used in this study, both observational and experimental: confocal laser scanning microscope, micro-indentation experiments, scanning electron microscopy, attraction experiments, specimen identification, mating experiments, X-ray computed tomography, 3D-reconstruction. I wonder if reading this beautiful research could be facilitated by transferring the very technical paragraphs “geometric morphometrics, landmarks and image processing” in Supplementary Methods, since “the males’ intromittent organs of S. ovinae and X. vesparum vary to a similar extent.” (549-552).
RESULTS and DISCUSSION
The main results of this study are the thicker resilin-rich integument and the higher forces required to penetrate in areas where traumatic insemination takes place rather than in control areas, either in Stylops or in Xenos, although the latter is less sclerotized. Co-evolution of the penises with the females’ paragenital organs in Stylops is a further intriguing result, as well as the alternative hypothesis that Strepsiptera have evolved tolerance rather than resistance against traumatic insemination: lower risk of integument rupture, sealing of the copulation wounds and reduced haemolymph loss (504-505).
As regards Attraction and Mating experiments in Stylops, you could quote similar field observations carried out in X. vesparum: five volant X. vesparum males, one mating on a leaf 20 cm from an aggregation and seven males close to a caged receptive female.
Hughes, D. P., Kathirithamby, J., Turillazzi, S., & Beani, L. (2004). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology, p.1042.
Again, in lab we described the direct approach by a male towards a receptive female, host interference by wings and legs movements, quick mating, and subsequent death of the male.
Beani et al. (2005). Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited (p.297)
Moreover, wasps parasitized by one or two X. vesparum females, individually enclosed into vials covered with a mesh, attracted male parasites inside the vials.
Beani et al. (2018). Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum.
Another original information is the sympatric occurrence of congeneric species, which increased interspecific competition (506-517) in Stylops but not in X. vesparum, released “over a period of several weeks” (518-519). More exactly, males emerge from mid-July until mid-August, the peak of the mating period, as indicated by the maximum number of empty puparia.
Hughes et al. (2004). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology. Fig.2, p.1039.
According with Kathyrithamby (2015), females of Strepsiptera produce species-specific pheromones to attract conspecific and to exclude heterospecific males (526-527). Although further prezygotic barriers may reduce heterospecific mating (527-545), I think that you could describe the Nassonow’s gland, which opens behind the brood canal up to the neck region. Dallai, R., Lupetti, P., Giusti, F., Mercati, D., Paccagnini, E., Turillazzi, S., Beani, L., Kathirithamby, J. (2004). Fine structure of the Nassonow’s gland in the neotenic endoparasitic of female Xenos vesparum (Rossi) (Strepsiptera, Insecta). Tissue and Cell, p.214.
Comments by Laura Beani
good; see attached file for suggested English improvements
good, answering more questions than the title suggests.....see attached review
Discussion is cautious....at the discretion of the authors could be expanded.
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This is a rare case that I had no specific comments. The paper was interesting and similar results as in other systems.
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