Are all the roads leading to Rome?
Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal
Recommendation: posted 18 February 2019, validated 20 February 2019
Blanchet, S. (2019) Are all the roads leading to Rome?. Peer Community in Ecology, 100011. 10.24072/pci.ecology.100011
Identifying the factors which favour the establishment and spread of non-native species in novel environments is one of the keys to predict - and hence prevent or control - biological invasions. This includes biological factors (i.e. factors associated with the invasive species themselves), and one of the prevailing hypotheses is that some species traits may explain their impressive success to establish and spread in novel environments . In animals, most research studies have focused on traits associated with fecundity, age at maturity, level of affiliation to humans or dispersal ability for instance. The “composite picture” of the perfect (i.e. successful) invader that has gradually emerged is a small-bodied animal strongly affiliated to human activities with high fecundity, high dispersal ability and a super high level of plasticity. Of course, the story is not that simple, and actually a perfect invader sometimes – if not often- takes another form… Carrying on to identify what makes a species a successful invader or not is hence still an important research axis with major implications.
In this manuscript, Charbonnel and collaborators  provide an interesting opportunity to gain novel insights into our understanding of (the) traits underlying invasion success. They nicely combine the power of Next-Generation Sequencing (NGS) with a clever comparative approach of two closely-related invasive rodents (the house mouse Mus musculus and the black rat Rattus rattus) in a common environment. They use this experimental design to test the appealing hypothesis that pathogens may be actors of the story, and may indirectly explain why some non-native species are so successful in invading novel habitats.
It is generally assumed that the community of pathogens encountered by non-native species in novel environments is different from that of their native area. On the one hand (the enemy-release hypothesis), it can be hypothesized that non-native species, when they arrive into a novel environment, will be relaxed from the pressure imposed by their native pathogens because local pathogens are not adapted (and hence do not infect) to this novel host. Because immune defence against pathogens is highly costly, non-native species establishing into a novel environment could hence reallocate these costs to other functions such as fecundity or dispersal apparatus. This scenario has been termed the “evolution of increased competitive ability” (EICA) hypothesis . On the other hand (the EICA-refined hypothesis ), one can assume that invaders will encounter new pathogens in newly established areas, and will allocate energy toward cost-effective immune pathways to permit allocating a non-negligible amount of energy toward other functions. Finally, a last hypothesis (the “immune protection” hypothesis) assumes major changes in pathogen composition between native and invaded areas, which should lead to an overall increase in immune investment by the native species to successfully invade novel environments . This last hypothesis suggests that only non-native species being able to take up the associated costs of immunity will be successful invaders.
The role of immunity in invasion success has yet been poorly investigated, mainly because of the difficulty to simultaneously analyse multiple immune pathways . Charbonnel and collaborators  overpass this difficulty by screening all genes expressed (using a whole RNA sequencing approach) in an immune tissue: the spleen. They do so along the invasion routes of two sympatric invasive rodents in Africa and compare anciently and newly invaded areas (respectively). For one of the two species (the house mouse), they found a high number of immune-related genes to be up-regulated in newly invaded areas compared to anciently invaded areas. All categories of immune pathways (costly and cost-effective) were up-regulated, suggesting an overall increase in immune investment in the mouse, which corroborates the “immune protection” hypothesis. For the black rat, patterns of gene expression were somewhat different, with much less pronounced differentiation in gene expression between newly and anciently invaded areas. Among the few differentiated genes, a few were associated to immune responses and some of theses genes were even down-regulated in the newly invaded areas. This pattern may actually corroborate the EICA hypothesis, although it could alternatively suggest that stochastic processes (drift) associated to recent decrease in population size (which is expected during a colonisation event) are more important than selection imposed by pathogens in shaping patterns of immune gene expression.
Overall, this study  suggests (i) that immune-related traits are important in predicting invasion success and (ii) that two successful species with a similar invasion history and living in similar environments can use different life-history strategies to reach the same success. This later finding is particularly relevant and intriguing as it suggests that the traits and strategies deployed by species to colonise new habitats might actually be idiosyncratic, and that, if general trends actually emerge in regards of traits predicting the success of invaders, the devil might actually be into the details. Comparative studies are extremely important to identify the general rules and the specificities sustaining actual patterns, but these approaches are yet poorly used in biological invasions (at least empirically). The work presented by Charbonnel and colleagues  calls for future comparative studies performed at multiple spatial scales (native vs. non-native areas, anciently vs. recently invaded areas), multiple taxonomic resolutions and across multiple traits (to search for trade-offs), so that the success of invasive species can be properly understood and predicted.
 Jeschke, J. M., & Strayer, D. L. (2006). Determinants of vertebrate invasion success in Europe and North America. Global Change Biology, 12(9), 1608-1619. doi: 10.1111/j.1365-2486.2006.01213.x
 Blossey, B., & Notzold, R. (1995). Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5), 887-889. doi: 10.2307/2261425
 Charbonnel, N., Galan, M., Tatard, C., Loiseau, A., Diagne, C. A., Dalecky, A., Parrinello, H., Rialle, S., Severac, D., & Brouat, C. (2019). Differential immune gene expression associated with contemporary range expansion of two invasive rodents in Senegal. bioRxiv, 442160, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/442160
 Lee, K. A., & Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology & Evolution, 19(10), 523-529. doi: 10.1016/j.tree.2004.07.012
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. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #2
DOI or URL of the preprint: 10.1101/442160
Version of the preprint: 3
Author's Reply, 13 Feb 2019
Decision by Simon Blanchet, posted 12 Feb 2019
I have now read the new version of the MS and your replies to the referees' comments. You've done a very good job and all comments were very well accounted for. My opinion is that there is no need to send the MS back to the referees. Nonetheless, I have attached an edited copy of the MS in which I have provided some change from place to place; these changes are suggestions, so feel free to accept them or not. Moreover, I still have a series of comments (comments 3 to 5) that are all related to the hypotheses being tested and their expectations. More specifically, I still have a problem with expectations regarding the EICA hypothesis. You mention in the Introduction that the EICA hypothesis is related to the enemy release hypothesis and that -because of that- the energy allocated to immunity should be released (an I agree). According to this statement, I would expect that the expression of immune genes is not different between newly and anciently invaded sites as both types of sites are in the non-native area and should be both "enemy free". On the contrary you mention p 5-6 that according to this hypothesis you expect an overall higher immune gene expression in recently invaded sites than in anciently invaded sites. I think that I disagree with this expectation, and I also have the feeling that is is in contradiction with what you said in the previous pages and in pages 12 (see comment 5). If I'm correct I think you should clarify this issue.
Once done, I'll be happy to recommend this very nice piece of work.
Simon BlanchetDownload recommender's annotations
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/442160
Version of the preprint: 2
Author's Reply, 05 Feb 2019
Decision by Simon Blanchet, posted 27 Nov 2018
Two reviewers have now read you contribution to PCI and have raised some comments. The two reviewers are specialists in the fields of invasion biology and genomics, and they both appreciated your manuscript. They especially like the way genome-wide patterns of gene expression were used to test clear and specific hypotheses related to invasion success in animals. They also highlight the facts that the studies was replicated both spatially and taxonomically, which is highly original and strong.
As you will see, they raised several comments, and my feeling is that all these comments should improve the general value of this manuscript. I therefore encourage you to update a new version of your manuscript that would take into account the comments both reviewers have made.
As you will see I have also uploaded an annotated pdf file with some comments I had.
Simon BlanchetDownload recommender's annotations