Local adaptation shall occur whenever selective pressures vary across space and overwhelm the effects of gene flow and local extinctions (Kawecki and Ebert 2004). Because the intimate interaction that characterizes their relationship exerts a strong selective pressure on both partners, host-parasite systems represent a classical example in which local adaptation is expected from rapidly evolving parasites adapting to more evolutionary constrained hosts (Kaltz and Shykoff 1998). Such systems indeed represent a large proportion of the study-cases in local adaptation research (Runquist et al. 2020). Biotic interactions intervene in many environment-related societal challenges, so that understanding when and how local adaptation arises is important not only for understanding evolutionary dynamics but also for more applied questions such as the control of agricultural pests, biological invasions, or pathogens (Parker and Gilbert 2004).
The exact conditions under which local adaptation does occur and can be detected is however still the focus of many theoretical, methodological and empirical studies (Blanquart et al. 2013, Hargreaves et al. 2020, Hoeksema and Forde 2008, Nuismer and Gandon 2008, Richardson et al. 2014). A recent review that evaluates investigations that examined the combined influence of biotic and abiotic factors on local adaptation reaches partial conclusions about their relative importance in different contexts and underlines the many traps that one has to avoid in such studies (Runquist et al. 2020). The authors of this review emphasize that one should evaluate local adaptation using wild-collected strains or populations and over multiple generations, on environmental gradients that span natural ranges of variation for both biotic and abiotic factors, in a theory-based hypothetico-deductive framework that helps interpret the outcome of experiments. These multiple targets are not easy to reach in each local adaptation experiment given the diversity of systems in which local adaptation may occur. Improving research practices may also help better understand when and where local adaptation does occur by adding controls over p-hacking, HARKing or publication bias, which is best achieved when hypotheses, date collection and analytical procedures are known before the research begins (Chambers et al. 2014). In this regard, the route taken by Olvera-Vazquez et al. (2021) is interesting. They propose to investigate whether the rosy aphid (Dysaphis plantaginea) recently adapted to its cultivated host, the apple tree (Malus domestica), and chose to pre-register their hypotheses and planned experiments on PCI Ecology (Peer Community In 2020). Though not fulfilling all criteria mentioned by Runquist et al. (2020), they clearly state five hypotheses that all relate to the local adaptation of this agricultural pest to an economically important fruit tree, and describe in details a powerful, randomized experiment, including how data will be collected and analyzed. The experimental set-up includes comparisons between three sites located along a temperature transect that also differ in local edaphic and biotic factors, and contrasts wild and domesticated apple trees that originate from the three sites and were both planted in the local, sympatric site, and transplanted to allopatric sites. Beyond enhancing our knowledge on local adaptation, this experiment will also test the general hypothesis that the rosy aphid recently adapted to Malus sp. after its domestication, a question that population genetic analyses was not able to answer (Olvera-Vazquez et al. 2020).
Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecology Letters, 16, 1195–1205. https://doi.org/10.1111/ele.12150
Briscoe Runquist RD, Gorton AJ, Yoder JB, Deacon NJ, Grossman JJ, Kothari S, Lyons MP, Sheth SN, Tiffin P, Moeller DA (2019) Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis. The American Naturalist, 195, 412–431. https://doi.org/10.1086/707322
Chambers CD, Feredoes E, Muthukumaraswamy SD, Etchells PJ, Chambers CD, Feredoes E, Muthukumaraswamy SD, Etchells PJ (2014) Instead of “playing the game” it is time to change the rules: Registered Reports at <em>AIMS Neuroscience</em> and beyond. AIMS Neuroscience, 1, 4–17. https://doi.org/10.3934/Neuroscience.2014.1.4
Hargreaves AL, Germain RM, Bontrager M, Persi J, Angert AL (2019) Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes. The American Naturalist, 195, 395–411. https://doi.org/10.1086/707323
Hoeksema JD, Forde SE (2008) A Meta‐Analysis of Factors Affecting Local Adaptation between Interacting Species. The American Naturalist, 171, 275–290. https://doi.org/10.1086/527496
Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity, 81, 361–370. https://doi.org/10.1046/j.1365-2540.1998.00435.x
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x
Nuismer SL, Gandon S (2008) Moving beyond Common‐Garden and Transplant Designs: Insight into the Causes of Local Adaptation in Species Interactions. The American Naturalist, 171, 658–668. https://doi.org/10.1086/587077
Olvera-Vazquez SG, Remoué C, Venon A, Rousselet A, Grandcolas O, Azrine M, Momont L, Galan M, Benoit L, David G, Alhmedi A, Beliën T, Alins G, Franck P, Haddioui A, Jacobsen SK, Andreev R, Simon S, Sigsgaard L, Guibert E, Tournant L, Gazel F, Mody K, Khachtib Y, Roman A, Ursu TM, Zakharov IA, Belcram H, Harry M, Roth M, Simon JC, Oram S, Ricard JM, Agnello A, Beers EH, Engelman J, Balti I, Salhi-Hannachi A, Zhang H, Tu H, Mottet C, Barrès B, Degrave A, Razmjou J, Giraud T, Falque M, Dapena E, Miñarro M, Jardillier L, Deschamps P, Jousselin E, Cornille A (2020) Large-scale geographic survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa. bioRxiv, 2020.12.11.421644. https://doi.org/10.1101/2020.12.11.421644
Olvera-Vazquez S.G., Alhmedi A., Miñarro M., Shykoff J. A., Marchadier E., Rousselet A., Remoué C., Gardet R., Degrave A. , Robert P. , Chen X., Porcher J., Giraud T., Vander-Mijnsbrugge K., Raffoux X., Falque M., Alins, G., Didelot F., Beliën T., Dapena E., Lemarquand A. and Cornille A. (2021) Experimental test for local adaptation of the rosy apple aphid (Dysaphis plantaginea) to its host (Malus domestica) and to its climate in Europe. In principle recommendation by Peer Community In Ecology. https://forgemia.inra.fr/amandine.cornille/local_adaptation_dp, ver. 4.
Parker IM, Gilbert GS (2004) The Evolutionary Ecology of Novel Plant-Pathogen Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 675–700. https://doi.org/10.1146/annurev.ecolsys.34.011802.132339
Peer Community In. (2020, January 15). Submit your preregistration to Peer Community In for peer review. https://peercommunityin.org/2020/01/15/submit-your-preregistration-to-peer-community-in-for-peer-review/
Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology & Evolution, 29, 165–176. https://doi.org/10.1016/j.tree.2014.01.002
All reviewers agree upon the fact that you satisfactorily addressed their main comments and questions.
Please however consider the following additional comments before I can recommend your preprint:
- your reference list has not been updated so that many papers you cite in the revised version of your preprint cannot be found in the reference list; it seems also that some of the papers that are cited in the reference list do not correspond to citations (different years for instance) ;
- lines 150-155: please rephrase to make your argument easier to follow. The rosy apple aphid is widely distributed all across the range of its domesticated host in Eurasia, also covering the distribution of its wild contributors (M. sieversii and M. sylvestris). Your population genetic study of the aphid, though quite extensive, did not address the question of its relationships with M. sieversii. It seems thus difficult to exclude that this parasite did not follow the domestication of apple trees before they were introgressed with M. sylvestris and other wild relatives (see Cornille et al. 2012 Plos Genet);
- line 296: do you really mean "conformed"? See also "by12";
- Table 3: please make column headers correspond to the columns of the Table (3 column headers for 4 columns);
- Fig. 1: the red dot is not placed on Asturia, the green one is not close to Angers, and the blue one is in France, not in Belgium;
- Fig. 3: the legend and the figure overlap.
all reviewers and I agree that this preprint provides a fair report of a well designed and powerful local adaptation experiment. The reviewers however underline some weaknesses. Please try to address those as it will help you improve your experimental setup and the planned data analyses. Altogether, this will lead to a more robust experiment and stronger conclusions. In particular, the reviewers noted: (1) a lack of consistency in the way the words genotype, cultivar and variety are used; (2) a possible confounding effect of site with climatic variables; (3) that the way fitness will be measured needs further explanation; (4) that you should consider systemic apple tree responses, and the way domestication may have altered these and more specific responses to aphids; (5) misspecifications of statistical models.
I appreciate you submitted your preprint to PCI and I look forward to reading you revised version soon.