Evolutionary footprints of a cold relic in a rapidly warming world

  1. Eva Wolf
  2. Emmanuel Gaquerel
  3. Mathias Scharmann
  4. Levi Yant
  5. Marcus A Koch

  • Curated by eLife

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    Evaluation Summary:

    This manuscript has the potential to be of broad interest to scientists seeking to understand the evolutionary dynamics of plants during past periods of rapid climate change. Specifically, within the target genus of Cochlearia, the results indicate increased rates of speciation and diversification in response to pronounced glacial cycles. Future work to establish more direct mechanistic links between the results and conclusions will improve our understanding of adaptation and speciation.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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Abstract

With accelerating global warming, understanding the evolutionary dynamics of plant adaptation to environmental change is increasingly urgent. Here, we reveal the enigmatic history of the genus Cochlearia (Brassicaceae) , a Pleistocene relic that originated from a drought-adapted Mediterranean sister genus during the Miocene. Cochlearia rapidly diversified and adapted to circum-Arctic regions and other cold-characterized habitat types during the Pleistocene. This sudden change in ecological preferences was accompanied by a highly complex, reticulate polyploid evolution, which was apparently triggered by the impact of repeated Pleistocene glaciation cycles. Our results illustrate that two early diversified Arctic-alpine diploid gene pools contributed differently to the evolution of this young polyploid genus now captured in a cold-adapted niche. Metabolomics revealed central carbon metabolism responses to cold in diverse species and ecotypes, likely due to continuous connections to cold habitats that may have facilitated widespread adaptation to alpine and subalpine habitats, and which we speculate were coopted from existing drought adaptations. Given the growing scientific interest in the adaptive evolution of temperature-related traits, our results provide much-needed taxonomic and phylogenomic resolution of a model system as well as first insights into the origins of its adaptation to cold.

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  1. Version published to 10.7554/elife.71572 on eLife
  2. eLife

    Author Response:

    Reviewer #1:

    For this manuscript, I focused on the metabolite analysis. The data is presented as supporting a common response based on shared selective histories if I'm understanding properly. However, primary metabolite data is hard to interpret in the same fashion as genetic data. This arises because of the high degree of pleiotropy wherein it is very hard to find a mutant or variant that doesn't alter primary metabolism. As such, it is possible that there is a common response less because of shared history and more because there is constraining selection that shapes what is the optimal primary metabolite response to cold in photosynthetic organisms. For example, in Arabidopsis, it has been found that accessions tend to have a highly similar primary metabolism but when they are crossed, the progeny have a vastly wider array of primary metabolism phenotypes, suggesting that the similarity in accessions is not shared genetics but constraining selection that forces compensatory variants. I don't think this detracts from the utility of including the primary metabolism but it would help to have more clarity in the strengths and weaknesses in using metabolite data to track theories and arguments that are largely genetic based.

    We fully agree with the reviewer. The idea of constraining selection is at least as interesting as our explanation, and should be in the forefront. Given this interesting idea of compensatory mutations that are private to each accession (or ‘lineage’ or ‘line’), in principle this idea also hints towards the parallel/convergent evolution (‘constraining selection’ in the reviewer’s words) of this important trait or trait complex. We re-phrased this within the manuscript and considered this comment seriously throughout. We also incorporate into our manuscript this interesting compensatory variant notion and metabolic network pleiotropy.

    One difference we would like to highlight still is that in our study (compared to Arabidopsis thaliana studies) we are comparing across many different species, ploidal levels, and varying species-level evolutionary histories. This makes our experiment different from Arabidopsis thaliana ecotype experiments and crossings; but indeed the reviewer is fully right that our results may also follow a similar evolutionary path as for Arabidopsis thaliana.

    Reviewer #2:

    Cochlearia, and other species that have rapidly evolved new ecological niches, represent excellent systems to study adaptation to past, present, future and changing environments. Furthermore, reticulate evolution within such groups offers a natural experiment to test hypotheses about the roles of hybridization, introgression, etc. on evolutionary dynamics, including pre-adaptation. However, there are also several significant challenges to using such systems, most crucially separating adaptation as the causal mechanism from the wide array of non-adaptive processes that could also cause the observed patterns. Overall, Wolf and colleagues do a nice job describing this complex taxonomic system and provide multiple lines of inquiry into how observed patterns may align with various adaptive scenarios. Despite the strong descriptive framework, I had trouble understanding exactly how causality could be assigned. Thus, the interpretation and discussion of the results felt speculative.

    Thank you for the encouraging comments. Yes, we agree: the points towards an important aspect of this kind of phylogenetic-systematic-evolutionary research, namely demonstrating causality. Honestly speaking, in such studies we are not able to show causality in its strict sense, and we think that the reviewer wants to claim this without using quite so strong wording. We considered this while re-phrasing respective paragraphs and also town down some speculative conclusion.

    Reviewer #3:

    There has been intense interest in how plants have responded during periods of rapid climate change in the past. Understanding these responses can increase our understanding of how plants might respond to rapidly accelerating anthropogenic climate shifts and help set conservation priorities. Many paleoecological studies have provided insight on how plants have migrated and persisted in suitable climate refugia (i.e. pockets of suitable habitat that exist even if regional climate is unfavorable for the persistence of a species) throughout glacial cycles, however there has been considerably less work that details the evolutionary dynamics of plants during these periods. This piece provides timely and valuable analyses illustrating the potential influence of pronounced climate change on the evolutionary dynamics of the genus Cochlearia.

    Thank you for the encouraging comments.

    The authors' use of cytogenetic analyses, organellar phylogenies, and demographic modeling allows for insights into the geographic patterns of diversity, speciation rates, and postglacial expansion scenarios of Cochlearia. Drawing unique conclusions from these different lines of evidence provides new understandings into the putative role of Pleistocene glacial cycles in driving evolutionary processes such as speciation. The study also aims to provide insight into the origins of the stated putative cold tolerance exhibited by Cochlearia by using a metabolomics approach; however, the framing and use of a single related outgroup (sister genus Ionopsidium) obfuscate the link between the results and stated conclusions.

    We appreciate this point, but indeed there is no other outgroup to be used. In this study we included all (both) genera with most of its species of tribe Cochlearieae. Within a family- wide phylogenetic context this tribe is placed along a polytomy (together with not well resolved other tribes) and stem group age of Cochlearieae is of appr. 18.9 million years ago (Walden et al., 2020). Therefore, for our research question additional outgroups from other tribes will not contribute any further information, because more basal splits are then nearly 20 million years ago (Early Miocene) with no biogeographic and environmentally defined scenarios that can be compared. 16-23 million years ago most tribes of evolutionary lineage II underwent an early radiation with highest net diversification rates (Walden et al. 2020) during this time. We included some of this information into the introduction.

    Specifically, regarding the approach that resulted in figure 4 which encompassed the metabolomics and related analyses, the initial climate groupings into 'climate ecotypes' would benefit from clarification and consideration of assignment methods. Typically, using the term ecotype invokes the idea of distinct forms of a species with phenotypic differences adapted to local conditions rather than groupings to those under broad climate regimes. While grouping populations according to climate origin can be useful, it is not clear how the final 9 WorldClim bioclimatic variables were selected (e.g. it is not apparent how importance of or correlations between climate variables, etc. were considered). Consequently, knowing this information would help understand the patterns in figure 4b, which seems to indicate that geographically distant populations experience very similar climate conditions (understanding that similarities can exist but variable selection can greatly influence these patterns).

    Thanks for this reminder to explaining selection and analyses of BioClim variables.

    As for the term “ecotype”: In plant taxonomy ecotypes are often referred to on subspecies level, in particular if environmental conditions are extremely different (e.g. heavy metal contaminated versus not-contaminated soils) and often these subspecies do not significantly differ in morphology (Noccaea caerulescens, Minuartia verna). In Cochlearia morphology is at best a morphospace which is more or less shared between all species in different ways. Species definition and taxonomy is based on a combination of largely overlapping morphospace, cytotype, ecotype and habitat types (bedrock; arctic, lowland to alpine; soil type and salt, life cycle) and distribution – often sole morphology is a bad species predictor (morphologically cryptic species – this is well-known also for some other arctic species such from the genus Draba). But the reviewer is fully right, that using the term ecotype here is somehow misleading. Our idea was to highlight that groups of taxa are combined by bioclimatic variables (and biomes or habitat types) while spanning the entire species/ecotype space of the genus – and this grouping follows also evolutionary meaningful cluster. We clarified this.

    As for selection of BioClim variables: we agree, indeed selection might have appeared arbitrary to the reader. Our original selection followed our field and cultivation experiences. However, structuring into four clusters as originally shown with the first submission is robust also when including all 19 BioClim variables. The same four cluster are retained in PCA, when temperature related BioClim variables are used only.

    Therefore, we added a Principal Component Analysis as starting point for Bioclim variable selection, secondly we added a PCA using temperature related BioClim variables 1-11 only. Built upon this we added a sentence why our nine selected variables were used to highlight the four groups in Fig. 4. The two PCA scree plots (including vector data) plus the correlation matrix and the results of a KMO test (Kaiser-Meyer-Olkin test: testing significant difference between the correlation matrix of variables and an identity matrix) are additionally provided with the Suppl. Material.

    The other concern is in regards to the framing and interpretation of these results. For instance, in the results (lines 329-330) and discussion (lines 419-423), the impression is given that experimental results here match those found in plants belonging to a different genus (i.e. Arabidopsis). However, rather than attributing this to more generally conserved mechanisms in response to considerable cold stress, the authors relate this to the unique history of Cochlearia (and its relationship to the drought adapted sister genus). The authors also note that surprisingly there was no demarcation of cold responses between the climate-defined groupings. Detailing why this is surprising given some of the other conclusion statements would be helpful. Some targeted revision to strengthen this link would be useful to bolster the inference of about the origins of cold tolerance in Cochlearia, rather than making it seem like this result could be expected in other taxa.

    Thank you for this. We agree that we did not explain our reasoning as well as we could and we now have reworked this. Original lines 329-330 simply refers to the (expected) and obvious general response to cold – some explanatory text has been added, e.g. such as at the end of the discussion and directly with the above-mentioned lines.

    Lastly, another area that would benefit from some clarification and tightening is revisiting the connection between the results and stated conclusions. For instance, some of the statements from the introduction and conclusions indicate the reader might expect explicit niche exploration analyses and more detailed genomic approaches. It is not abundantly clear for a general audience how these results definitively demonstrate how genetic diversity was rescued in reticulate and polyploid gene pools or species barriers were torn down. These are very specific, strong claims that do not appear to be explicitly discussed outside of the introduction/discussion or directly related to the results presented in this manuscript.

    Thank you for pointing out how this could be read in this way. We have revised this to indicate that agree: we do not think our data ‘definitively demonstrate’ (in the reviewer’s words, not our) this. We modify the text to avoid such interpretation.

    This is no way diminishes the considerable effort of the authors to conduct the informative array of presented analyses, but more closely aligning the conclusions within the scope of presented results (or providing direct links on how the results provide these insights) would help increase the effectiveness of this manuscript.

    Many thanks for this very encouraging note. We have worked to incorporate these thoughtful comments.

  3. eLife

    Evaluation Summary:

    This manuscript has the potential to be of broad interest to scientists seeking to understand the evolutionary dynamics of plants during past periods of rapid climate change. Specifically, within the target genus of Cochlearia, the results indicate increased rates of speciation and diversification in response to pronounced glacial cycles. Future work to establish more direct mechanistic links between the results and conclusions will improve our understanding of adaptation and speciation.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    For this manuscript, I focused on the metabolite analysis. The data is presented as supporting a common response based on shared selective histories if I'm understanding properly. However, primary metabolite data is hard to interpret in the same fashion as genetic data. This arises because of the high degree of pleiotropy wherein it is very hard to find a mutant or variant that doesn't alter primary metabolism. As such, it is possible that there is a common response less because of shared history and more because there is constraining selection that shapes what is the optimal primary metabolite response to cold in photosynthetic organisms. For example, in Arabidopsis, it has been found that accessions tend to have a highly similar primary metabolism but when they are crossed, the progeny have a vastly wider array of primary metabolism phenotypes, suggesting that the similarity in accessions is not shared genetics but constraining selection that forces compensatory variants. I don't think this detracts from the utility of including the primary metabolism but it would help to have more clarity in the strengths and weaknesses in using metabolite data to track theories and arguments that are largely genetic based.

  5. eLife

    Reviewer #2 (Public Review):

    Cochlearia, and other species that have rapidly evolved new ecological niches, represent excellent systems to study adaptation to past, present, future and changing environments. Furthermore, reticulate evolution within such groups offers a natural experiment to test hypotheses about the roles of hybridization, introgression, etc. on evolutionary dynamics, including pre-adaptation. However, there are also several significant challenges to using such systems, most crucially separating adaptation as the causal mechanism from the wide array of non-adaptive processes that could also cause the observed patterns. Overall, Wolf and colleagues do a nice job describing this complex taxonomic system and provide multiple lines of inquiry into how observed patterns may align with various adaptive scenarios. Despite the strong descriptive framework, I had trouble understanding exactly how causality could be assigned. Thus, the interpretation and discussion of the results felt speculative.

  6. eLife

    Reviewer #3 (Public Review):

    There has been intense interest in how plants have responded during periods of rapid climate change in the past. Understanding these responses can increase our understanding of how plants might respond to rapidly accelerating anthropogenic climate shifts and help set conservation priorities. Many paleoecological studies have provided insight on how plants have migrated and persisted in suitable climate refugia (i.e. pockets of suitable habitat that exist even if regional climate is unfavorable for the persistence of a species) throughout glacial cycles, however there has been considerably less work that details the evolutionary dynamics of plants during these periods. This piece provides timely and valuable analyses illustrating the potential influence of pronounced climate change on the evolutionary dynamics of the genus Cochlearia.

    The authors' use of cytogenetic analyses, organellar phylogenies, and demographic modeling allows for insights into the geographic patterns of diversity, speciation rates, and postglacial expansion scenarios of Cochlearia. Drawing unique conclusions from these different lines of evidence provides new understandings into the putative role of Pleistocene glacial cycles in driving evolutionary processes such as speciation. The study also aims to provide insight into the origins of the stated putative cold tolerance exhibited by Cochlearia by using a metabolomics approach; however, the framing and use of a single related outgroup (sister genus Ionopsidium) obfuscate the link between the results and stated conclusions.

    Specifically, regarding the approach that resulted in figure 4 which encompassed the metabolomics and related analyses, the initial climate groupings into 'climate ecotypes' would benefit from clarification and consideration of assignment methods. Typically, using the term ecotype invokes the idea of distinct forms of a species with phenotypic differences adapted to local conditions rather than groupings to those under broad climate regimes. While grouping populations according to climate origin can be useful, it is not clear how the final 9 WorldClim bioclimatic variables were selected (e.g. it is not apparent how importance of or correlations between climate variables, etc. were considered). Consequently, knowing this information would help understand the patterns in figure 4b, which seems to indicate that geographically distant populations experience very similar climate conditions (understanding that similarities can exist but variable selection can greatly influence these patterns). The other concern is in regards to the framing and interpretation of these results. For instance, in the results (lines 329-330) and discussion (lines 419-423), the impression is given that experimental results here match those found in plants belonging to a different genus (i.e. Arabidopsis). However, rather than attributing this to more generally conserved mechanisms in response to considerable cold stress, the authors relate this to the unique history of Cochlearia (and its relationship to the drought adapted sister genus). The authors also note that surprisingly there was no demarcation of cold responses between the climate-defined groupings. Detailing why this is surprising given some of the other conclusion statements would be helpful. Some targeted revision to strengthen this link would be useful to bolster the inference of about the origins of cold tolerance in Cochlearia, rather than making it seem like this result could be expected in other taxa.

    Lastly, another area that would benefit from some clarification and tightening is revisiting the connection between the results and stated conclusions. For instance, some of the statements from the introduction and conclusions indicate the reader might expect explicit niche exploration analyses and more detailed genomic approaches. It is not abundantly clear for a general audience how these results definitively demonstrate how genetic diversity was rescued in reticulate and polyploid gene pools or species barriers were torn down. These are very specific, strong claims that do not appear to be explicitly discussed outside of the introduction/discussion or directly related to the results presented in this manuscript. This is no way diminishes the considerable effort of the authors to conduct the informative array of presented analyses, but more closely aligning the conclusions within the scope of presented results (or providing direct links on how the results provide these insights) would help increase the effectiveness of this manuscript.

  7. Version published to 10.1101/2021.07.11.451959v1 on bioRxiv