The pros and cons of mating with strangers
Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costly
Recommendation: posted 12 July 2017, validated 12 July 2017
Interspecific matings are by definition rare events in nature, but when they occur they can be very important, and not only because they might condition gene flow between species. Even when such matings have no genetic consequence, for instance if they do not yield any fertile hybrid offspring, they can still have an impact on the population dynamics of the species involved . Such atypical pairings between heterospecific partners are usually regarded as detrimental or undesired; as they interfere with the occurrence or success of intraspecific matings, they are expected to cause a decline in absolute fitness.
The story is not always so simple however, and it might all depend on the timing of events and on the identity of the partners. Using the herbivorous mite Tetranychus urticae as a model, Clemente et al.  experimentally arranged matings with two other Tetranychus species that commonly share the same host plants as T. urticae. They carefully controlled the history of events: heterospecific matings could occur just before, just after, 24h before, or 24h after, a conspecific mating. Interestingly, the oviposition rate (total fecundity) of females was increased when mating with a heterospecific individual. This suggests that heterospecic sperm can stimulate oogenesis just as conspecific sperm does. Such a positive effect was observed for matings involving T. ludeni females and T. urticae males, but a negative effect is found in the interaction with T. evansi. Sex-ratio (fertilization success in those species) could also be impacted but, unlike fertilization, this occurred when the mating events were distant in time. This is is at odds with what is observed in conspecific matings, where sperm displacement occurs only if mating events are temporally close. Overall, the effects of heterospecific mating were quite variable and it is challenging to predict a single, general, effect of interspecific matings. The net effect will likely be context-dependent, depending on the relative frequency of the difference mating sequences and on how fecundity and sex-ratio contribute to overall fitness, both aspect strongly influenced by the population dynamics and structure.
 Gröning J. & Hochkirch A. 2008. Reproductive interference between animal species. The Quarterly Review of Biology 83: 257-282. doi: 10.1086/590510
 Clemente SH, Santos I, Ponce AR, Rodrigues LR, Varela SAM & Magalhaes S. 2017 Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costly. bioRxiv 113274, ver. 4 of the 30th of June 2017. doi: 10.1101/113274
Vincent Calcagno (2017) The pros and cons of mating with strangers. Peer Community in Evolutionary Biology, 100025. 10.24072/pci.evolbiol.100025
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
Evaluation round #2
DOI or URL of the preprint: 10.1101/113274
Version of the preprint: 2
Author's Reply, 06 Jul 2017
Decision by Vincent Calcagno, posted 28 Jun 2017
Dear authors, Thank you for revising your preprint. The reviewers and I are satisfied with your revisions and by your response letter as well.
I am therefore willing to recommend your preprint for PCI Evol Biol, once you will have double-checked the statistical points that one reviewer has raised: please provide degrees of freedom wherever appropriate and make sure there are no errors in the statistics reported.
Reviewed by Michael D Greenfield, 26 Jun 2017
Reviewed by Joël Meunier, 22 Jun 2017
Evaluation round #1
DOI or URL of the preprint: 10.1101/113274
Version of the preprint: 1
Author's Reply, 09 Jun 2017
Decision by Vincent Calcagno, posted 04 May 2017
I have read your preprint manuscript with great interest. It reports some intriguing results, such as increased fecundity following heterospecific matings. I got it evaluated by two expert reviewers, and based on this I believe I could recommend your work on PCI Evol. Biol.. However this would require you to prepare and upload a revised version that addresses the following concerns.
First, it is not clear what is the realized or expected frequency in the wild of the different events you are experimentally considering, i.e. the different mating sequences. What are the existing premating barriers? What is the typical number of matings experienced by females? Such information should be very clearly provided to decide whether you are considering common events that have a fitness impact and whose frequency and consequences are potentially shaped by natural selection, or if you are considering more abstract postzygotic barriers and the level of isolation those species would experience in the case of hybridization.
Second, the reviewers, and I had the same impression, were puzzled by your use of a metaanalysis statistical pipeline at the end of your study. As one reviewer states this is atypical in this experimental context, but more importantly it is not clear at all what this brings on top of the previous statistical analyses you are conducting earlier in the manuscript. Reanalyzing the same data, or presenting two sets of analyses for the same data, is not a good idea. As I understand the main reason you would want to use this metanalysis package is to get an idea of “combined effects”. However, and I concur with reviewers on this point, it seems a bit artificial and akin to adding apples and oranges: brood size and sexratio are two distinct components that enter fitness in a complex (and certainly context-dependent) way, so it does not seem possible to simply add them up with a 1:1 weighting. This seems too naive in this context. Furthermore, you could discuss such combined effects based on the simpler analyzes, with no need to compute precise (and oversimplified) quantities. I would have the same critics regarding the computation of a summary estimate over the different types of matings: as we do not know what is their relative frequencies (see the previous point) in the wild, it makes no sense to combine them additively with equal weighting in some sort of average. In terms of formatting, the metaanalysis also looks like an additional layer added on top of everything at the very end: it may be redundant or unnecessary, but it surely lacks sufficient explanation/justification. I personally think you should drop this entire analysis, unless you substantially rewrite the article so that it becomes obvious why you need it and what it does exactly (in which case it would probably replace several earlier analyses presented).
One reviewer also brought up several other concerns about the statistical results and the overall presentation that you would want to address. If you are willing to revise your manuscript, I will be happy to consider it for recommendation, and in any case I hope you will find these reports useful.