Determinants of population genetic structure in co-occurring freshwater snails
Connectivity and selfing drives population genetic structure in a patchy landscape: a comparative approach of four co-occurring freshwater snail species
Genetic diversity is a key aspect of biodiversity and has important implications for evolutionary potential and thereby the persistence of species. Improving our understanding of the factors that drive genetic structure within and between populations is, therefore, a long-standing goal in evolutionary biology. However, this is a major challenge, because of the complex interplay between genetic drift, migration, and extinction/colonization dynamics on the one hand, and the biology and ecology of species on the other hand (Romiguier et al. 2014, Ellegren and Galtier 2016, Charlesworth 2003).
Jarne et al. (2021) studied whether environmental and demographic factors affect the population genetic structure of four species of hermaphroditic freshwater snails in a similar way, using comparative analyses of neutral genetic microsatellite markers.
Specifically, they investigated microsatellite variability of Hygrophila in almost 280 sites in Guadeloupe, Lesser Antilles, as part of a long-term survey experiment (Lamy et al. 2013). They then modelled the influence of the mating system, local environmental characteristics and demographic factors on population genetic diversity.
Consistent with theoretical predictions (Charlesworth 2003), they detected higher genetic variation in two outcrossing species than in two selfing species, emphasizing the importance of the mating system in maintaining genetic diversity. The study further identified an important role of site connectivity, through its influences on effective population size and extinction/colonisation events. Finally, the study detects an influence of interspecific interactions caused by an ongoing invasion by one of the studied species on genetic structure, highlighting the indirect effect of changes in community composition and demography on population genetics.
Jarne et al. (2021) could address the extent to which genetic structure is determined by demographic and environmental factors in multiple species given the remarkable sampling available. Additionally, the study system is extremely suitable to address this hypothesis as species’ habitats are defined and delineated. Whilst the authors did attempt to test for across-species correlations, further investigations on this matter are required. Moreover, the effect of interactions between factors should be appropriately considered in any modelling between genetic structure and local environmental or demographic features.
The findings in this study contribute to improving our understanding of factors influencing population genetic diversity, and highlights the complexity of interacting factors, therefore also emphasizing the challenges of drawing general implications, additionally hampered by the relatively limited number of species studied. Jarne et al. (2021) provide an excellent showcase of an empirical framework to test determinants of genetic structure in natural populations. As such, this study can be an example for further attempts of comparative analysis of genetic diversity.
Charlesworth, D. (2003) Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358, 1051-1070. doi: https://doi.org/10.1098/rstb.2003.1296
Ellegren, H. and Galtier, N. (2016) Determinants of genetic diversity. Nature Reviews Genetics, 17, 422-433. doi: https://doi.org/10.1038/nrg.2016.58
Jarne, P., Lozano del Campo, A., Lamy, T., Chapuis, E., Dubart, M., Segard, A., Canard, E., Pointier, J.-P. and David, P. (2021) Connectivity and selfing drives population genetic structure in a patchy landscape: a comparative approach of four co-occurring freshwater snail species. HAL, hal-03295242, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://hal.archives-ouvertes.fr/hal-03295242
Lamy, T., Gimenez, O., Pointier, J. P., Jarne, P. and David, P. (2013). Metapopulation dynamics of species with cryptic life stages. The American Naturalist, 181, 479-491. doi: https://doi.org/10.1086/669676
Romiguier, J., Gayral, P., Ballenghien, M. et al. (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261-263. doi: https://doi.org/10.1038/nature13685
Trine Bilde and Matteo Fumagalli (2021) Determinants of population genetic structure in co-occurring freshwater snails. Peer Community in Evolutionary Biology, 100130. https://doi.org/10.24072/pci.evolbiol.100130
Revision round #227 Jul 2021
Decision round #2
Thank you for submitting the revised version of the manuscipt. We are satisfied with the responses to the reviewer comments, and we kindly ask you to make a few minor corrections before we make the final recommendation. Please see the comments here:
1. Pantel et al citation is still "submitted" in the text and bibliography while in the response the Author's say it has been published. Can references to this paper be updated?
2. The sentence “Two correlations were significant in cases in which we did not expect a correlation, specifically, a negative correlation between size and connectivity and a positive one between stability and the density of favorable habitats” should be rephrased. We suggest something like “We observed two unexpected significant correlations, namely between size and connectivity (negative) and between stability and the density of favorable habitats (positive).”
3. Reference Otto (2021) is alphabetically wrongly placed in the bibliography.
4. "recommander" should be "recommender" in Conflict of Interests statement
Matteo Fumagalli and Trine Bilde
Revision round #104 Jun 2021
Decision round #1
Dear Dr Jarne and co-authors
We are pleased that we have now received three reviews of your pre-print. The reviewers and we as co-handlers of your manuscript all enjoyed reading the pre-print, and that we would like to recommend minor revision.
All reviewers agree that your study is interesting and presents a very interesting and comprehensive study. The reviewers have provided several comments and useful suggestions on ways to improve the presentation. These mainly relate to improving clarity of various parts of the manuscript.
One potentially critical point was raised relating to the collinearity between predictors in some of the models, in addition to a question regarding whether an additional variable should be included in the analyses.
It should be fairly straightforward to address the comments in a revised version of the manuscript.
Matteo Fumagalli and Trine Bilde