Diverse outcomes in cheese fungi domestication
Domestication of different varieties in the cheese-making fungus Geotrichum candidum
Recommendation: posted 23 March 2023, validated 24 March 2023
Domestication is a complex process that imprints the demography and the genomes of domesticated populations, enforcing strong selective pressures on traits favourable to humans, e.g. for food production . Domestication has been quite intensely studied in plants and animals, but less so in micro-organisms such as fungi, despite their assets (e.g. their small genomes and tractability in the lab). This elegant study by Bennetot and collaborators  on the cheese-making fungus Geotrichum candidum adds to the mounting body of studies in the genomics of fungi, proving they are excellent models in evolutionary biology for studying adaptation and drift in eukaryotes .
Bennetot et al. newly showed with whole genome sequences that all G. candidum strains isolated from cheese form a monophyletic clade subdivided into three genetically differentiated populations with several admixed strains, while the wild strains sampled from diverse geographic locations form a sister clade. This suggests the wild progenitor was not sampled in the present study and calls for future exciting work on the domestication history of the G. candidum fungus. The authors scanned the genomes for footprints of adaptation to the cheese environment and identified promising candidates, such as a gene involved in iron uptake (this element is limiting in cheese). Their functional genome analysis also provides evidence for higher contents of transposable elements in cheese-making strains, likely due to relaxed selection during the domestication process.
This paper is particularly impressive in that the authors complemented the population genomic approach with the phenotypic characterization of the strains and tested their ability to outcompete common fungal food spoilers. The authors convincingly showed that cheese-making strains display phenotypic differences relative to wild relatives for multiple traits such as slower growth, lower proteolysis activity and a greater amount of volatiles attractive to consumers, these phenotypes being beneficial for cheese making.
Finally, this work is particularly inspiring because it thoroughly discusses convergent evolution during domestication in different cheese-associated fungi. Indeed, studying populations experiencing similar environmental pressures is fundamental to understanding whether evolution is repeatable . For instance, all three cheese populations of G. candidum exhibit a lower genetic diversity than wild populations. However, only one population displays a stronger domestication syndrome, resembling the Penicillium camemberti situation . Furthermore, different cheese-making practices may have led to varying situations with clonal lineages in non-Roquefort P. roqueforti and P. camemberti [5, 6], while the cheese-making G. candidum populations still harbour some diversity. In a nutshell, Bennetot's study makes an important contribution to evolutionary biology and highlights the value of diversifying our model organisms toward under-represented clades.
 Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418: 700–707. https://doi.org/10.1038/nature01019
 Bennetot B, Vernadet J-P, Perkins V, Hautefeuille S, Rodríguez de la Vega RC, O’Donnell S, Snirc A, Grondin C, Lessard M-H, Peron A-C, Labrie S, Landaud S, Giraud T, Ropars J (2023) Domestication of different varieties in the cheese-making fungus Geotrichum candidum. bioRxiv, 2022.05.17.492043, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.05.17.492043
 Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, Rodríguez de la Vega RC, Branco S, Giraud T (2014) Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol. Ecol. 23: 753–773. https://doi.org/10.1111/mec.12631
 Bolnick DI, Barrett RD, Oke KB, Rennison DJ, Stuart YE (2018) (Non)Parallel evolution. Ann. Rev. Ecol. Evol. Syst. 49: 303–330. https://doi.org/10.1146/annurev-ecolsys-110617-062240
 Ropars J, Didiot E, Rodríguez de la Vega RC, Bennetot B, Coton M, Poirier E, Coton E, Snirc A, Le Prieur S, Giraud T (2020) Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties. Current Biol. 30: 4441–4453.e4. https://doi.org/10.1016/j.cub.2020.08.082
 Dumas, E, Feurtey, A, Rodríguez de la Vega, RC, Le Prieur S, Snirc A, Coton M, Thierry A, Coton E, Le Piver M, Roueyre D, Ropars J, Branca A, Giraud T (2020) Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol. 29: 2639–2660. https://doi.org/10.1111/mec.15359
Christelle Fraïsse (2023) Diverse outcomes in cheese fungi domestication. Peer Community in Evolutionary Biology, 100592. https://doi.org/10.24072/pci.evolbiol.100592
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.
This work was funded by the Artifice ANR-19-CE20-0006-01 ANR grant to J.R. In addition, a NSERC-Discovery Grant supported the scholarship of V.P and data generation, and is held by S. Labrie (RGPIN-2017-06388)
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.05.17.492043
Version of the preprint: 3
Author's Reply, 20 Feb 2023
Decision by Christelle Fraïsse, posted 21 Oct 2022, validated 26 Oct 2022
Thank you for your patience. Two reviewers have provided constructive and thorough comments on your preprint. Both agree that the study is of high quality, and after reading the manuscript, I agree with their statement. I especially appreciated that domestication was tackled from a phenotypic and genomic perspective – this represents an impressive amount of work. I am convinced that this work will interest the evolutionary biology community.
The reviewers made a number of helpful, often concordant, suggestions for improvements that must be addressed in a revision. In particular:
1) They criticize the interpretation of the data for the Cheese_2 population as revealing a more advanced stage of domestication. Evidence for human-mediated selection to be more substantial in that cheese population than others should be demonstrated more clearly. Moreover, Reviewer 1 suggests considering other forces than selection in the evolution of the cheese populations, including migration and genetic drift.
2) Another issue raised by the two reviewers is the under-sampling of the wild strains. This bias could have consequences for interpreting the data (in particular, if the wild strains were sampled in a single geographic area), so it should be handled with caution. Reviewer 2 noted that an outcome that could follow is the misinterpretation of the cheese clade as being derived from the wild clade (see their specific comments on that point). Determining if cheese-making practices (Reviewer 1) could explain the differentiation between the three cheese clades may help understand whether this genetic structure within cheese strains has pre-existed domestication.
3) Both reviewers note the difficulty of interpreting FST when measuring the extent of population divergence. Moreover, Reviewer 2 questions the method used to detect candidate regions under adaptation. Instead of considering the 5% most extreme values of Dxy and Pi, which is expected under neutrality, you could only consider those regions that pop up as extremes in both Dxy and Pi scans as candidates. Otherwise, I recommend running a method that scans for selective sweeps.
4) I agree with Reviewer 1 that the comparison with Penicillium should be better justified and moved into a single paragraph in the Discussion section. A more in-depth discussion of the convergence process would help clarify the importance of comparing with Penicillium.
5) Reviewer 2 suggests running a demographic analysis to test for an absence of a substantial bottleneck during the domestication of G. candidum. I think there is no need to run such a type of analysis; however, Tajima’s D could be calculated to clarify this claim.
I am looking forward to receiving your revised preprint.
With best regards,