The spatial dynamics of habitat fragmentation drives the evolution of dispersal and metapopulation persistence
Evolution of dispersal and the maintenance of fragmented metapopulations
Recommendation: posted 14 July 2023, validated 15 July 2023
The persistence of populations facing the destruction of their habitat is a multifaceted question that has mobilized theoreticians and empiricists alike for decades. As an ecological question, persistence has been studied as the spatial rescue of populations via dispersal into remaining suitable habitats. The spatial aggregation of habitat destruction has been a key component of these studies, and it has been applied to the problem of coexistence by integrating competition-colonization tradeoffs. There is a rich ecological literature on this topic, both from theoretical and field studies (Fahrig 2003). The relationship between life-history strategies of species and their resilience to spatially structured habitat fragmentation is also an important component of conservation strategies through the management of land use, networks of protected areas, and the creation of corridors. In the context of environmental change, the ability of species to adapt to changes in landscape configuration and availability can be treated as an eco-evolutionary process by considering the possibility of evolutionary rescue (Heino and Hanski 2001; Bell 2017). However, eco-evolutionary dynamics considering spatially structured changes in landscapes and life-history tradeoffs remains an outstanding question. Finand et al. (2023) formulate the problem of persistence in fragmented landscapes over evolutionary time scales by studying models for the evolution of dispersal in relation to habitat fragmentation and spatial aggregation. Their simulations were conducted on a spatial grid where individuals can colonize suitable patch as a function of their competitive rank that decreases as a function of their (ii) dispersal distance trait. Simulations were run under fixed habitat fragmentation (proportion of unsuitable habitat) and aggregation, and with an explicit rate of habitat destruction to study evolutionary rescue.
Their results reveal a balance between the selection for high dispersal under increasing habitat fragmentation and selection for lower dispersal in response to habitat aggregation. This balance leads to the coexistence of polymorphic dispersal strategies in highly aggregated landscapes with low fragmentation where high dispersers inhabit aggregated habitats while low dispersers are found in isolated habitats. The authors then integrate the spatial rescue mechanism to the problem of evolutionary rescue in response to temporally increasing fragmentation. There they show how rapid evolution allows for evolutionary rescue through the evolution of high dispersal. They also show the limits to this evolutionary rescue to cases where both aggregation and fragmentation are not too high. Interestingly, habitat aggregation prevents evolutionary rescue by directly affecting the evolutionary potential of dispersal. The study is based on simple scenarios that ignore the complexity of relationships between dispersal, landscape properties, and species interactions. This simplicity is the strength of the study, revealing basic mechanisms that can now be tested against other life-history tradeoffs and species interactions. Finand et al. (2023) provide a novel foundation for the study of eco-evolutionary dynamics in metacommunities exposed to spatially structured habitat destruction. They point to important assumptions that must be made along the way, including the relationships between dispersal distance and fecundity (they assume a positive relationship), and the nature of life-history tradeoffs between dispersal rate and local competitive abilities.
Bell, G. 2017. Evolutionary Rescue. Annual Review of Ecology, Evolution, and Systematics 48:605–627. https://doi.org/10.1146/annurev-ecolsys-110316-023011
Fahrig, L. 2003. Effects of Habitat Fragmentation on Biodiversity. Annual Review of Ecology, Evolution, and Systematics 34:487–515. https://doi.org/10.2307/30033784
Finand, B., T. Monnin, and N. Loeuille. 2023. Evolution of dispersal and the maintenance of fragmented metapopulations. bioRxiv, 2022.06.08.495260, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.06.08.495260
Heino, M., and I. Hanski. 2001. Evolution of Migration Rate in a Spatially Realistic Metapopulation Model. The American Naturalist 157:495–511. https://doi.org/10.1086/319927
Frédéric Guichard (2023) The spatial dynamics of habitat fragmentation drives the evolution of dispersal and metapopulation persistence. Peer Community in Ecology, 100426. 10.24072/pci.ecology.100426
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: https://doi.org/10.1101/2022.06.08.495260
Version of the preprint: 2
Author's Reply, 13 Jul 2023
Decision by Frédéric Guichard, posted 02 Jun 2023, validated 05 Jun 2023
I am almost ready to make my final recommendation. While I am finalizing it, I simply wanted the authors to consider the following suggestions:
1. Competition-colonization trade-off is a central ecological context for the study. Reviewers suggested a number of references that could help set that context. While I understand competition-colonization tradeoffs constitutes the context rather than the goal of the study, the fact that the study focuses on evolutionary process makes it all the more important to provide appropriate reference to the ecological literature that might be unfamiliar to evolutionary biologists.
2. L227-228: vague description of stationarity. Long term average and variance would be more specific and appropriate metrics. In any case, consider providing a more precise and repeatable description of your assessment of stationarity.
3. L458. Replace ‘is founded’ with ‘was funded’.
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.06.08.495260
Version of the preprint: 1
Author's Reply, 22 May 2023
Decision by Frédéric Guichard, posted 09 Sep 2022
All reviewers found the work novel and of general interest. I share that opinion. They also provided detailed comments and suggestions to improve the manuscript. Most major concerns converged among reviewers to questions of clarity/reproducilbility, reference to previous work, and interpretation of results. The detailed suggestions found in reviewers' reports will most certainly contribute to improving the manuscript. Reviewers were concerns the work would not be reproducible becasue of lack of details on the various packages and code used to run simulations. Most reviewers also raised concerns over some interpretations of results generated from a specific model. Part of the problem was a concern over the sensitivity of results to the specific model used. Some more specific potential issues were also suggested, such as the dependence of results on the asumed correlation between dispersal and fecundity, or the validity of concluding to lower competition in highly fragmented landscapes. Finally, all reviewers suggested additional references to previous work to better set the broader context for adding evolutionary dynamics to the study of extinctions in metapopulations with habilitat destruction. In my opinion, addressing these, and all other comments from reviewers, will increase the potential impact of this study.