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04 Sep 2019
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Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals

Transcriptomics of thermal stress response in corals

Recommended by based on reviews by Mar Sobral

Climate change presents a challenge to many life forms and the resulting loss of biodiversity will critically depend on the ability of organisms to timely respond to a changing environment. Shifts in ecological parameters have repeatedly been attributed to global warming, with the effectiveness of these responses varying among species [1, 2]. Organisms do not only have to face a global increase in mean temperatures, but a complex interplay with another crucial but largely understudied aspect of climate change: thermal fluctuations. Understanding the mechanisms underlying adaptation to thermal fluctuations is thus a timely and critical challenge.
Coral reefs are among the most threaten ecosystems in the context of current global changes [3]. Brener-Raffalli and colleagues [4] provided a very complete study digging into the physiological, symbiont-based and transcriptomic mechanisms underlying response of corals to temperature changes. They used an experimental approach, following the heat stress response of coral colonies from different species of the genus Pocillopora. While the symbiont community composition did not significantly change facing exposure to warmer temperatures, the authors provided evidence for transcriptomic changes especially linked to stress response genes that may underlie plastic responses to heat stress.
The authors furthermore investigated the thermal stress response of corals originating from two sites differing in their natural thermal regimes, and found that they differ in the extent and nature of plastic response, including the expression of gene regulation factors and the basal expression level of some genes. These two sites also differ in a variety of aspects, including the focal coral species, which precludes from concluding about the role of thermal regime adaptation into the differences observed. However, these results still highlight a very interesting and important direction deserving further investigation [5], and point out the importance of variability in thermal stress response among localities [6] that might potentially mediate global warming consequences on coral reefs.

References

[1] Parmesan, C., & Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421(6918), 37–42. doi: 10.1038/nature01286
[2] Menzel, A., Sparks, T. H., Estrella, N., Koch, E., Aasa, A., Ahas, R., … Zust, A. (2006). European phenological response to climate change matches the warming pattern. Global Change Biology, 12(10), 1969–1976. doi: 10.1111/j.1365-2486.2006.01193.x
[3] Bellwood, D. R., Hughes, T. P., Folke, C., & Nyström, M. (2004). Confronting the coral reef crisis. Nature, 429(6994), 827–833. doi: 10.1038/nature02691
[4] Brener-Raffalli, K., Vidal-Dupiol, J., Adjeroud, M., Rey, O., Romans, P., Bonhomme, F., Pratlong, M., Haguenauer, A., Pillot, R., Feuillassier, L., Claereboudt, M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D., Mitta, G. and Toulza, E. (2019). Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals. BioRxiv, 398602, ver 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/398602
[5] Kenkel, Carly D., and Matz, M. V. (2017). Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology and Evolution, 1(1), 0014. doi: 10.1038/s41559-016-0014
[6] Kenkel, C. D., Meyer, E., and Matz, M. V. (2013). Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Molecular Ecology, 22(16), 4322–4334. doi: 10.1111/mec.12390

Gene expression plasticity and frontloading promote thermotolerance in Pocillopora coralsK. Brener-Raffalli, J. Vidal-Dupiol, M. Adjeroud, O. Rey, P. Romans, F. Bonhomme, M. Pratlong, A. Haguenauer, R. Pillot, L. Feuillassier, M. Claereboudt, H. Magalon, P. Gélin, P. Pontarotti, D. Aurelle, G. Mitta, E. Toulza<p>Ecosystems worldwide are suffering from climate change. Coral reef ecosystems are globally threatened by increasing sea surface temperatures. However, gene expression plasticity provides the potential for organisms to respond rapidly and effect...Climate change, Evolutionary ecology, Marine ecology, Molecular ecology, Phenotypic plasticity, SymbiosisStaffan Jacob2018-08-29 10:46:55 View
05 Feb 2020
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A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding

A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding

Recommended by ORCID_LOGO based on reviews by Tiago Pereira and 1 anonymous reviewer

High-throughput sequencing-based techniques such as DNA metabarcoding are increasingly advocated as providing numerous benefits over morphology‐based identifications for biodiversity inventories and ecosystem biomonitoring [1]. These benefits are particularly apparent for highly-diversified and/or hardly accessible aquatic and marine environments, where simple water or sediment samples could already produce acceptably accurate biodiversity estimates based on the environmental DNA present in the samples [2,3]. However, sequence-based characterization of biodiversity comes with its own challenges. A major one resides in the capacity to disentangle true biological diversity (be it taxonomic or genetic) from artefactual diversity generated by sequence-errors accumulation during PCR and sequencing processes, or from the amplification of non-target genes (i.e. pseudo-genes). On one hand, the stringent elimination of sequence variants might lead to biodiversity underestimation through the removal of true species, or the clustering of closely-related ones. On the other hand, a more permissive sequence filtering bears the risks of biodiversity inflation. Recent studies have outlined an excellent methodological framework for addressing this issue by proposing bioinformatic tools that allow the amplicon-specific error-correction as alternative or as complement to the more arbitrary approach of clustering into Molecular Taxonomic Units (MOTUs) based on sequence dissimilarity [4,5]. But to date, the relevance of amplicon-specific error-correction tools has been demonstrated only for a limited set of taxonomic groups and gene markers.
The study of Brandt et al. [6] successfully builds upon existing methodological frameworks for filling this gap in current literature. By proposing a bioinformatic pipeline combining Amplicon Sequence Variants (ASV) curation with MOTU clustering and additional post-clustering curation, the authors show that contrary to previous recommendations, ASV-based curation alone does not represent an adequate approach for DNA metabarcoding-based inventories of metazoans. Metazoans indeed, do exhibit inherently higher intra-specific and intra-individual genetic variability, necessarily leading to biased biodiversity estimates unbalanced in favor of species with higher intraspecific diversity in the absence of MOTU clustering. Interestingly, the positive effect of additional clustering showed to be dependent on the target gene region. Additional clustering had proportionally higher effect on the more polymorphic mitochondrial COI region (as compared to the 18S ribosomal gene). Thus, the major advantage of the study lies in the provision of optimal curation parameters that reflect the best possible balance between minimizing the impact of PCR/sequencing errors and the loss of true biodiversity across markers with contrasting levels of intragenomic variation. This is important as combining multiple markers is increasingly considered for improving the taxonomic coverage and resolution of data in DNA metabarcoding studies.
Another critical aspect of the study is the taxonomic assignation of curated OTUs (which is also the case for the majority of DNA metabarcoding-based biodiversity assessments). Facing the double challenge of focusing on taxonomic groups that are both highly diverse and poorly represented in public sequence reference databases, the authors failed to obtain high-resolution taxonomic assignments for several of the most closely-related species. As a result, taxa with low divergence levels were clustered as single taxonomic units, subsequently leading to underestimation of true biodiversity present. This finding adds to the argument that in order to be successful, sequence-based techniques still require the availability of comprehensive, high-quality reference databases.
Perhaps the only regret we might have with the study is the absence of mock community validation for the prokaryotes compartment. Even though the analyses of natural samples seem to suggest a positive effect of the curation pipeline, the concept of intra- versus inter-species variation in naturally occurring prokaryote communities remains at best ambiguous. Of course, constituting a representative sample of taxonomically-resolved prokaryote taxa from deep-sea habitats does not come without difficulties but has the benefit of opening opportunities for further studies on the matter.

References

[1] Porter, T. M., and Hajibabaei, M. (2018). Scaling up: A guide to high-throughput genomic approaches for biodiversity analysis. Molecular Ecology, 27(2), 313–338. doi: 10.1111/mec.14478
[2] Valentini, A., Taberlet, P., Miaud, C., Civade, R., Herder, J., Thomsen, P. F., … Dejean, T. (2016). Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Molecular Ecology, 25(4), 929–942. doi: 10.1111/mec.13428
[3] Leray, M., and Knowlton, N. (2015). DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proceedings of the National Academy of Sciences, 112(7), 2076–2081. doi: 10.1073/pnas.1424997112
[4] Callahan, B. J., McMurdie, P. J., and Holmes, S. P. (2017). Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME Journal, 11(12), 2639–2643. doi: 10.1038/ismej.2017.119
[5] Edgar, R. C. (2016). UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257. doi: 10.1101/081257
[6] Brandt, M. I., Trouche, B., Quintric, L., Wincker, P., Poulain, J., and Arnaud-Haond, S. (2020). A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding. BioRxiv, 717355, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/717355

A flexible pipeline combining clustering and correction tools for prokaryotic and eukaryotic metabarcoding Miriam I Brandt, Blandine Trouche, Laure Quintric, Patrick Wincker, Julie Poulain, Sophie Arnaud-Haond<p>Environmental metabarcoding is an increasingly popular tool for studying biodiversity in marine and terrestrial biomes. With sequencing costs decreasing, multiple-marker metabarcoding, spanning several branches of the tree of life, is becoming ...Biodiversity, Community ecology, Marine ecology, Molecular ecologyStefaniya Kamenova2019-08-02 20:52:45 View
20 Oct 2021
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Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline

Doomed by your partner: when mutualistic interactions are like an evolutionary millstone around a species’ neck

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Mutualistic interactions are the weird uncles of population and community ecology. They are everywhere, from the microbes aiding digestion in animals’ guts to animal-pollination services in ecosystems; They increase productivity through facilitation; They fascinate us when small birds pick the teeth of a big-mouthed crocodile. Yet, mutualistic interactions are far less studied and understood than competition or predation. Possibly because we are naively convinced that there is no mystery here: isn’t it obvious that mutualistic interactions necessarily facilitate species coexistence? Since mutualistic species benefit from one another, if one species evolves, the other should just follow, isn’t that so?

It is not as simple as that, for several reasons. First, because simple mutualistic Lotka-Volterra models showed that most of the time mutualistic systems should drift to infinity and be unstable (e.g. Goh 1979). This is not what happens in natural populations, so something is missing in simple models. At a larger scale, that of communities, this is even worse, since we are still far from understanding the link between the topology of mutualistic networks and the stability of a community. Second, interactions are context-dependent: mutualistic species exchange resources, and thus from the point of view of one species the interaction is either beneficial or not, depending on the net gain of energy (e.g. Holland and DeAngelis 2010). In other words, considering interactions as mutualistic per se is too caricatural. Third, since evolution is blind, the evolutionary response of a species to an environmental change can have any effect on its mutualistic partner, and not necessarily a neutral or positive effect. This latter reason is particularly highlighted by the paper by A. Weinbach et al. (2021).

Weinbach et al. considered a simple two-species mutualistic Lotka-Volterra model and analyzed the evolutionary dynamics of a trait controlling for the rate of interaction between the two species by using the classical Adaptive Dynamics framework. They showed that, depending on the form of the trade-off between this interaction trait and its effect on the intrinsic growth rate, several situations can occur at evolutionary equilibrium: species can stably coexist and maintain their interaction, or the interaction traits can evolve to zero where species can coexist without any interactions.

Weinbach et al. then investigated the fate of the two-species system if a partner species is strongly affected by environmental change, for instance, a large decrease of its growth rate. Because of the supposed trade-off between the interaction trait and the growth rate, the interaction trait in the focal species tends to decrease as an evolutionary response to the decline of the partner species. If environmental change is too large, the interaction trait can evolve to zero and can lead the partner species to extinction. An “evolutionary murder”.

Even though Weinbach et al. interpreted the results of their model through the lens of plant-pollinators systems, their model is not specific to this case. On the contrary, it is very general, which has advantages and caveats. By its generality, the model is informative because it is a proof of concept that the evolution of mutualistic interactions can have unexpected effects on any category of mutualistic systems. Yet, since the model lacks many specificities of plant-pollinator interactions, it is hard to evaluate how their result would apply to plant-pollinators communities.

I wanted to recommend this paper as a reminder that it is certainly worth studying the evolution of mutualistic interactions, because i) some unexpected phenomenons can occur, ii) we are certainly too naive about the evolution and ecology of mutualistic interactions, and iii) one can wonder to what extent we will be able to explain the stability of mutualistic communities without accounting for the co-evolutionary dynamics of mutualistic species.

References

Goh BS (1979) Stability in Models of Mutualism. The American Naturalist, 113, 261–275. http://www.jstor.org/stable/2460204.

Holland JN, DeAngelis DL (2010) A consumer–resource approach to the density-dependent population dynamics of mutualism. Ecology, 91, 1286–1295. https://doi.org/10.1890/09-1163.1

Weinbach A, Loeuille N, Rohr RP (2021) Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population decline. bioRxiv, 570580, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/570580

Eco-evolutionary dynamics further weakens mutualistic interaction and coexistence under population declineAvril Weinbach, Nicolas Loeuille, Rudolf P. Rohr<p style="text-align: justify;">With current environmental changes, evolution can rescue declining populations, but what happens to their interacting species? Mutualistic interactions can help species sustain each other when their environment wors...Coexistence, Eco-evolutionary dynamics, Evolutionary ecology, Interaction networks, Pollination, Theoretical ecologySylvain Billiard2019-09-05 11:29:45 View
09 Nov 2023
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Mark loss can strongly bias estimates of demographic rates in multi-state models: a case study with simulated and empirical datasets

Marks lost in action, biased estimations

Recommended by ORCID_LOGO based on reviews by Olivier Gimenez, Devin Johnson and 1 anonymous reviewer

Capture-Mark-Recapture (CMR) data are commonly used to estimate ecological variables such as abundance, survival probability, or transition rates from one state to another (e.g. from juvenile to adult, or migration from one site to another). Many studies have shown how estimations can be affected by neglecting one aspect of the population under study (e.g. the heterogeneity in survival between individuals) or one limit of the methodology itself (e.g. the fact that observers might not detect an individual although it is still alive). Strikingly, very few studies have yet assessed the robustness of one fundamental assumption of all CMR-based inferences: marks are supposed definitive and immutable. If they are not, how are estimations affected? Addressing this issue is the main goal of the paper by Touzalin et al. (2023), and they did a very nice work. But, because the answer is not that simple, it also calls for further investigations.

When and why would mark loss bias estimation? In at least two situations. First, when estimating survival rates: if an individual loses its mark, it will be considered as dead, hence death rates will be overestimated. Second, more subtly, when estimating transition rates: if one individual loses its mark at the specific moment where its state changes, then a transition will be missed in data. The history of the marked individual would then be split into two independent CMR sequences as if there were two different individuals, including one which died.

Touzalin et al. (2023) thoroughly studied these two situations by estimating ecological parameters on 1) well-thought simulated datasets, that cover a large range of possible situations inspired from a nice compilation of hundreds of estimations from fish and bats studies, and 2) on their own bats dataset, for which they had various sources of information about mark losses, i.e. different mark types on the same individuals, including mark based on genotypes, and marks found on the soil in the place where bats lived. Their main findings from the simulated datasets are that there is a general trend for underestimation of survival and transition rates if mark loss is not accounting for in the model, as it would be intuitively expected. However, they also showed from the bats dataset that biases do not show any obvious general trend, suggesting complex interactions between different ecological processes and/or with the estimation procedure itself.

The results by Touzalin et al. (2023) strongly suggest that mark loss should systematically be included in models estimating parameters from CMR data. In addition to adapt the inferential models, the authors also recommend considering either a double marking, or even a single but ‘permanent’ mark such as one based on the genotypes. However, the potential gain of a double marking or of the use of genotypes is still to be evaluated both in theory and practice, and it seems to be not that obvious at first sight. First because double marking can be costly for experimenters but also for the marked animals, especially as several studies showed that marks can significantly affect survival or recapture rates. Second because multiple sources of errors can affect genotyping, which would result in wrong individual assignations especially in populations with low genetic diversity or high inbreeding, or no individual assignation at all, which would increase the occurrence of missing data in CMR datasets. Touzalin et al. (2023) supposed in their paper that there were no genotyping errors, but one can doubt it to be true in most situations. They have now important and interesting other issues to address.

References

Frédéric Touzalin, Eric J. Petit, Emmanuelle Cam, Claire Stagier, Emma C. Teeling, Sébastien J. Puechmaille (2023) Mark loss can strongly bias demographic rates in multi-state models: a case study with simulated and empirical datasets. BioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.03.25.485763

Mark loss can strongly bias estimates of demographic rates in multi-state models: a case study with simulated and empirical datasetsFrédéric Touzalin, Eric J. Petit, Emmanuelle Cam, Claire Stagier, Emma C. Teeling, Sébastien J. Puechmaille<p style="text-align: justify;">1. The development of methods for individual identification in wild species and the refinement of Capture-Mark-Recapture (CMR) models over the past few decades have greatly improved the assessment of population demo...Conservation biology, DemographySylvain Billiard2022-04-12 18:49:34 View
05 Jun 2024
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Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off

Plant-herbivore-pollinator ménage-à-trois: tell me how well they match, and I'll tell you if it's made to last

Recommended by ORCID_LOGO based on reviews by Marcos Mendez and Yaroslav Ispolatov

How would a plant trait evolve if it is involved in interacting with both a pollinator and an herbivore species? The answer by Yacine and Loeuille is straightforward: it is not trivial, but it can explain many situations found in natural populations.

Yacine and Loeuille applied the well-known Adaptive Dynamics framework to a system with three interacting protagonists: a herbivore, a pollinator, and a plant. The evolution of a plant trait is followed under the assumption that it regulates the frequency of interaction with the two other species. As one can imagine, that is where problems begin: interacting more with pollinators seems good, but what if at the same time it implies interacting more with herbivores? And that's not a silly idea, as there are many cases where herbivores and pollinators share the same cues to detect plants, such as colors or chemical compounds.

They found that depending on the trade-off between the two types of interactions and their density-dependent effects on plant fitness, the possible joint ecological and evolutionary outcomes are numerous. When herbivory prevails, evolution can make the ménage-à-trois ecologically unstable, as one or even two species can go extinct, leaving the plant alone. Evolution can also make the coexistence of the three species more stable when pollination services prevail, or lead to the appearance of a second plant species through branching diversification of the plant trait when herbivory and pollination are balanced.

Yacine and Loeuille did not only limit themselves to saying "it is possible," but they also did much work evaluating when each evolutionary outcome would occur. They numerically explored in great detail the adaptive landscape of the plant trait for a large range of parameter values. They showed that the global picture is overall robust to parameter variations, strengthening the plausibility that the evolution of a trait involved in antagonistic interactions can explain many of the correlations between plant and animal traits or phylogenies found in nature.

Are we really there yet? Of course not, as some assumptions of the model certainly limit its scope. Are there really cases where plants' traits evolve much faster than herbivores' and pollinators' traits? Certainly not, but the model is so general that it can apply to any analogous system where one species is caught between a mutualistic and a predator species, including potential species that evolve much faster than the two others. And even though this limitation might cast doubt on the generality of the model's predictions, studying a system where a species' trait and a preference trait coevolve is possible, as other models have already been studied (see Fritsch et al. 2021 for a review in the case of evolution in food webs). We can bet this is the next step taken by Yacine and Loeuille in a similar framework with the same fundamental model, promising fascinating results, especially regarding the evolution of complex communities when species can accumulate after evolutionary branchings.

Relaxing another assumption seems more challenging as it would certainly need to change the model itself: interacting species generally do not play fixed roles, as being mutualistic or antagonistic might generally be density-dependent (Holland and DeAngelis 2010). How would the exchange of resources between three interacting species evolve? It is an open question.

References

Fritsch, C., Billiard, S., & Champagnat, N. (2021). Identifying conversion efficiency as a key mechanism underlying food webs adaptive evolution: a step forward, or backward? Oikos, 130(6), 904-930.
https://doi.org/10.1111/oik.07421
 
Holland, J. N., & DeAngelis, D. L. (2010). A consumer-resource approach to the density‐dependent population dynamics of mutualism. Ecology, 91(5), 1286-1295.
https://doi.org/10.1890/09-1163.1

Yacine, Y., & Loeuille, N. (2024) Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off. bioRxiv 2021.12.02.470900; doi: https://doi.org/10.1101/2021.12.02.470900

Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-offYoussef Yacine, Nicolas Loeuille<p style="text-align: justify;">Many plant traits are subject to an ecological trade-off between attracting pollinators and escaping herbivores. The interplay of both plant-animal interaction types determines their evolution. As most studies focus...Eco-evolutionary dynamics, Herbivory, Pollination, Theoretical ecologySylvain Billiard2023-03-21 14:23:12 View
24 Apr 2025
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Evolutionary rescue in a mixed beech-fir forest: insights from a quantitative-genetics approach in a process-based model

Integrating evolution and ecology in forests: insights from a multi species demogenetic model

Recommended by ORCID_LOGO based on reviews by Silvio Shueler and 3 anonymous reviewers

The study of eco-evolutionary dynamics, i.e. of the inter-twinning between ecological and evolutionary processes when they occur at comparable time scales, is of growing interest in the current context of global change (Carroll, Hendry, Reznick, & Fox, 2007; Govaert et al., 2019). Demo-genetic agent-based models (DG-ABMs) have gained popularity to address this issue because of their abilities to consider feedback loops between ecological and evolutionary processes and to track populations of interacting individuals with adaptive traits variations (Berzaghi et al., 2019; Lamarins et al., 2022). This type of individual- and process-based simulation modelling where interindividual variation in fitness and hence opportunities for selection emerge from demography, which in turn affects the genetic composition of the population over successive generations (feedback loop), is only beginning to be applied to forest trees (Oddou-Muratorio, Hendrik, & Lefèvre, 2020). Examples include studies investigating the dispersal capacity of transgenes in forest landscapes using spatially explicit DG-ABMs with different demographic rates for transgenic and wild-type trees (DiFazio, Slavov, Burczyk, Leonardi, & Strauss, 2004; Kuparinen & Schurr, 2007), the effect of assortative mating and selection on genetic and plastic differentiation along environmental gradients (Soularue et al., 2023) or the interactions and feedback between tree thinning, genetic evolution, and forest stand dynamics, eventually in the context of drought-induced disturbances (Fririon, Davi, Oddou‐Muratorio, Ligot, & Lefèvre, 2024; Godineau et al., 2023).

In this study, Devresse et al. (2025) extend the current DG-ABM framework for forest trees by incorporating interspecific interactions within diverse, uneven-aged forests. To this end, they adapted an existing multi-species, process-based forest dynamics model—ForCEEPS (Morin et al., 2021)—enabling the evolution of selected tree functional traits across generations. Their work focuses on three quantitative traits: drought tolerance, shade tolerance, and maximal growth rate. Using this enhanced DG-ABM, the authors investigate the conditions under which evolutionary rescue might occur in a mixed beech-fir forest facing climate change. Their results demonstrate that greater trait variability and higher heritability can mitigate short-term (century-scale) forest cover loss under climate warming. The study also shows that assisted gene flow facilitates species adaptation to climate change, while the introduction of pre-adapted species (assisted migration) may enhance post-disturbance recovery but simultaneously constrain the evolutionary rescue of local species.

This work represents a major interdisciplinary advancement in forest ecology and nicely illustrates how integrating evolutionary processes into ecology-focused models can offer novel insights into forest dynamics. The implementation of genetic variability and inheritance via the infinitesimal model of quantitative genetics, along with its limitations, is described in detail, and the various research questions explored using the coupled DG‑ABM are presented as proof of concept for this successful integration. Beyond its methodological contribution, the study highlights the importance of more integrated approaches to understanding forest responses to climate change—approaches that account for both within- and between-species diversity and that promote nature-based solutions. It also underscores the urgent need for experimental studies exploring the genetic variation and architecture of adaptive traits in forest species to better anticipate and support their adaptive potential in a rapidly changing environment.

 

References

Berzaghi, F., Wright, I. J., Kramer, K., Oddou-Muratorio, S., Bohn, F. J., Reyer, C. P. O., … Hartig, F. (2019). Towards a new generation of trait-flexible vegetation models. Trends in Ecology & Evolution, 35(3), 191–205. https://doi.org/10.1016/j.tree.2019.11.006

Carroll, S. P., Hendry, A. P., Reznick, D. N., & Fox, C. W. (2007). Evolution on ecological time-scales. Functional Ecology, 21(3), 387–393. https://doi.org/10.1111/j.1365-2435.2007.01289.x

Devresse, L., Way, F., Postic, T., de Coligny, F. & Morin, X. (2025) Evolutionary rescue in a mixed beech-fir forest: insights from a quantitative-genetics approach in a process-based model. HAL, ver.4 peer-reviewed and recommended by PCI Ecology. https://hal.science/hal-04575070

DiFazio, S. P., Slavov, G. T., Burczyk, J., Leonardi, S., & Strauss, S. H. (2004). Gene flow from tree plantations and implications for transgenic risk assessment. In Plantation Forest Biotechnology for the 21st Century (pp. 405–422). https://doi.org/10.1016/j.diagmicrobio.2009.10.017

Fririon, V., Davi, H., Oddou‐Muratorio, S., Ligot, G., & Lefèvre, F. (2024). Can Thinning Foster Forest Genetic Adaptation to Drought? A Demo‐Genetic Modelling Approach With Disturbance Regimes. Evolutionary Applications, 17(12). https://doi.org/10.1111/eva.70051

Godineau, C., Fririon, V., Beudez, N., de Coligny, F., Courbet, F., Ligot, G., … Lefèvre, F. (2023). A demo-genetic model shows how silviculture reduces natural density-dependent selection in tree populations. Evolutionary Applications, (March), 1–15. https://doi.org/10.1111/eva.13606

Govaert, L., Fronhofer, E. A., Lion, S., Eizaguirre, C., Bonte, D., Egas, M., … Matthews, B. (2019). Eco-evolutionary feedbacks—Theoretical models and perspectives. Functional Ecology, 33(1), 13–30. https://doi.org/10.1111/1365-2435.13241

Kuparinen, A., & Schurr, F. M. (2007). A flexible modelling framework linking the spatio-temporal dynamics of plant genotypes and populations: Application to gene flow from transgenic forests. Ecological Modelling, 202(3–4), 476–486. https://doi.org/10.1016/j.ecolmodel.2006.11.015

Lamarins, A., Fririon, V., Folio, D., Vernier, C., Daupagne, L., Labonne, J., … Oddou-Muratorio, S. (2022). Importance of interindividual interactions in eco-evolutionary population dynamics: The rise of demo-genetic agent-based models. Evolutionary Applications, 15(12), 1988–2001. https://doi.org/10.1111/eva.13508

Morin, X., Bugmann, H., de Coligny, F., Martin-StPaul, N., Cailleret, M., Limousin, J. M., … Guillemot, J. (2021). Beyond forest succession: A gap model to study ecosystem functioning and tree community composition under climate change. Functional Ecology, 35(4), 955–975. https://doi.org/10.1111/1365-2435.13760

Oddou-Muratorio, S., Hendrik, D., & Lefèvre, F. (2020). Integrating evolutionary, demographic and ecophysiological processes to predict the adaptive dynamics of forest tree populations under global change. Tree Genetics & Genomes, 16(5), 1–22. https://doi.org/10.1007/s11295-020-01451-1

Soularue, J. P., Firmat, C., Caignard, T., Thöni, A., Arnoux, L., Delzon, S., … Kremer, A. (2023). Antagonistic Effects of Assortative Mating on the Evolution of Phenotypic Plasticity along Environmental Gradients. American Naturalist, 202(1), 18–39. https://doi.org/10.1086/724579

Evolutionary rescue in a mixed beech-fir forest: insights from a quantitative-genetics approach in a process-based modelLouis Devresse, Freya Way, Tanguy Postic, François de Coligny, Xavier Morin<p>Questions have been raised about the ability of long-lived organisms, such as trees, to adapt to rapid climate change, and to what extent forest management actions influence the evolutionary responses of tree species. Given the life history of ...Community ecology, Competition, Eco-evolutionary dynamics, Ecosystem functioning, Evolutionary ecology, Theoretical ecologySylvie Oddou-Muratorio2024-05-17 19:33:41 View
16 Sep 2019
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Blood, sweat and tears: a review of non-invasive DNA sampling

Words matter: extensive misapplication of "non-invasive" in describing DNA sampling methods, and proposed clarifying terms

Recommended by based on reviews by 2 anonymous reviewers

The ability to successfully sequence trace quantities of environmental DNA (eDNA) has provided unprecedented opportunities to use genetic analyses to elucidate animal ecology, behavior, and population structure without affecting the behavior, fitness, or welfare of the animal sampled. Hair associated with an animal track in the snow, the shed exoskeleton of an insect, or a swab of animal scat are all examples of non-invasive methods to collect eDNA. Despite the seemingly uncomplicated definition of "non-invasive" as proposed by Taberlet et al. [1], Lefort et al. [2] highlight that its appropriate application to sampling methods in practice is not so straightforward. For example, collecting scat left behind on the forest floor by a mammal could be invasive if feces is used by that species to mark territorial boundaries. Other collection strategies such as baited DNA traps to collect hair, capturing and handling an individual to swab or stimulate emission of a body fluid, or removal of a presumed non essential body part like a feather, fish scale, or even a leg from an insect are often described as "non-invasive" sampling methods. However, such methods cannot be considered truly non-invasive. At a minimum, attracting or capturing and handling an animal to obtain a DNA sample interrupts its normal behavioral routine, but additionally can cause both acute and long-lasting physiological and behavioral stress responses and other effects. Even invertebrates exhibit long-term hypersensitization after an injury, which manifests as heightened vigilance and enhanced escape responses [3-5].
Through an extensive analysis of 380 papers published from 2013-2018, Lefort et al. [2] document the widespread misapplication of the term "non-invasive" to methods used to sample DNA. An astonishing 58% of these papers employed the term incorrectly. A big part of the problem is that "non-invasive" is usually used by authors in the medical or veterinary sense of not breaking the skin or entering the body [6], rather than in the broader, ecological sense of Taberlet et al. [1]. The authors argue that correct use of the term matters, because it may lead naive readers – one can imagine students, policy makers, and the general public – to incorrectly assume a particular method is safe to use in a situation where disturbing the animal could affect experimental results or raise animal welfare concerns. Such assumptions can affect experimental design, as well as interpretations of one's own or others' data.
The importance of the Lefort et al. [2] paper lies in part on the authors' call for the research community to be much more careful when applying the term "non-invasive" to methods of DNA sampling. This call cannot be shrugged off as a minor problem in a few papers – as their literature review demonstrates, "non-invasive" is being applied incorrectly more often than not. The authors recognize that not all DNA sampling must be non-invasive to be useful or ethical. Examples include taking samples for DNA extraction from museum specimens, or opportunistically from carcasses of animals hunted either legally or seized by authorities from poachers. In many cases, there may be no viable non-invasive method to obtain DNA, but a researcher strives to collect samples using methods that, although they may involve taking a sample directly from the animal's body, do not disrupt, or only slightly disrupt behavior, fitness, or welfare of the animal. Thus, the other important contribution by Lefort et al. [2] is to propose the terms "non-disruptive" and "minimally-disruptive" to describe such sampling methods, which are not strictly non-invasive. While gray areas undoubtedly remain, as acknowledged by the authors, answering the call for correct use of "non-invasive" and applying the proposed new terms for certain types of invasive sampling with a focus on level of disruption, will go a long way in limiting misconceptions and misinterpretations caused by the current confusion in terminology.

References

[1] Taberlet P., Waits L. P. and Luikart G. 1999. Noninvasive genetic sampling: look before you leap. Trends Ecol. Evol. 14: 323-327. doi: 10.1016/S0169-5347(99)01637-7
[2] Lefort M.-C., Cruickshank R. H., Descovich K., Adams N. J., Barun A., Emami-Khoyi A., Ridden J., Smith V. R., Sprague R., Waterhouse B. R. and Boyer S. 2019. Blood, sweat and tears: a review of non-invasive DNA sampling. bioRxiv, 385120, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/385120
[3] Khuong T. M., Wang Q.-P., Manion J., Oyston L. J., Lau M.-T., Towler H., Lin Y. Q. and Neely G. G. 2019. Nerve injury drives a heightened state of vigilance and neuropathic sensitization in Drosophila. Science Advances 5: eaaw4099. doi: 10.1126/sciadv.aaw4099
[4] Crook, R. J., Hanlon, R. T. and Walters, E. T. 2013. Squid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury. Journal of Neuroscience, 33(24), 10021-10026. doi: 10.1523/JNEUROSCI.0646-13.2013
[5] Walters E. T. 2018. Nociceptive biology of molluscs and arthropods: evolutionary clues about functions and mechanisms potentially related to pain. Frontiers in Physiololgy 9: doi: 10.3389/fphys.2018.01049
[6] Garshelis, D. L. 2006. On the allure of noninvasive genetic sampling-putting a face to the name. Ursus 17: 109-123. doi: 10.2192/1537-6176(2006)17[109:OTAONG]2.0.CO;2

Blood, sweat and tears: a review of non-invasive DNA samplingMarie-Caroline Lefort, Robert H Cruickshank, Kris Descovich, Nigel J Adams, Arijana Barun, Arsalan Emami-Khoyi, Johnaton Ridden, Victoria R Smith, Rowan Sprague, Benjamin Waterhouse, Stephane Boyer<p>The use of DNA data is ubiquitous across animal sciences. DNA may be obtained from an organism for a myriad of reasons including identification and distinction between cryptic species, sex identification, comparisons of different morphocryptic ...Behaviour & Ethology, Conservation biology, Molecular ecology, ZoologyThomas Wilson Sappington2018-11-30 13:33:31 View
24 May 2022
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Controversy over the decline of arthropods: a matter of temporal baseline?

Don't jump to conclusions on arthropod abundance dynamics without appropriate data

Recommended by ORCID_LOGO based on reviews by Gabor L Lovei and 1 anonymous reviewer

Humans are dramatically modifying many aspects of our planet via increasing concentrations of carbon dioxide in the atmosphere, patterns of land-use change, and unsustainable exploitation of the planet’s resources. These changes impact the abundance of species of wild organisms, with winners and losers. Identifying how different species and groups of species are influenced by anthropogenic activity in different biomes, continents, and habitats, has become a pressing scientific question with many publications reporting analyses of disparate data on species population sizes. Many conclusions are based on the linear analysis of rather short time series of organismal abundances.
 
There has been particular interest in how arthropods are impacted by environmental change, with several recent papers reporting contradictory results. To investigate why these contradictions might arise, Duchenne et al. (2022) conducted an analysis of four published data sets along with a series of experimental analyses of simulated time series to examine the power of widely used statistical analyses to gain inference on temporal trends. Their important paper reveals that accurate inference on dynamics, particularly of species that exhibit large temporal fluctuations in abundance, requires time series that are substantially longer than are typically collected, as well as careful thought as to whether linear models are appropriate. Linear analyses of short time series are susceptible to providing unreliable inference as trends can be strongly influenced by points at either end of the time series. 
 
Duchenne et al.’s paper provides important insight on the conditions when strong inference on temporal trends of arthropod (and other species) abundances can be made, and when they should be treated with caution. They do not doubt that many insect and arachnid species are changing their abundances, and that patterns in these changes may vary spatially. What their results do say is that we should treat grand claims of population recovery or rapid declines apparently to extinction with caution when they are based on short time series, particularly of species that show significant boom and bust dynamics. In many ways, these results are not unexpected, but it is nice to see such careful and thoughtful analyses and interpretation. More data are required for most arthropod species before clear assessments of abundance trends can be made. Given our reliance on many arthropods for food, pollination, and numerous ecosystem services, and the ability of other species to spread devastating human diseases such as dengue and malaria, it is advisable that we slow our modification of their habitats while additional data are collected to allow us to better characterise the trajectory of arthropod populations to understand what the consequences of our actions on the natural world are likely to be.  
 
References

Duchenne F, Porcher E, Mihoub J-B, Loïs G, Fontaine C (2022) Controversy over the decline of arthropods: a matter of temporal baseline? bioRxiv, 2022.02.09.479422, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.09.479422

Controversy over the decline of arthropods: a matter of temporal baseline?François Duchenne, Emmanuelle Porcher, Jean-Baptiste Mihoub, Grégoire Loïs, Colin Fontaine<p style="text-align: justify;">Recently, a number of studies have reported somewhat contradictory patterns of temporal trends in arthropod abundance, from decline to increase. Arthropods often exhibit non-monotonous variation in abundance over ti...Conservation biologyTim Coulson2022-02-11 15:44:44 View
03 Jun 2022
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Evolutionary emergence of alternative stable states in shallow lakes

How to evolve an alternative stable state

Recommended by ORCID_LOGO based on reviews by Jean-François Arnoldi and 1 anonymous reviewer

Alternative stable states describe ecosystems that can persist in more than one configuration. An ecosystem can shift between stable states following some form of perturbation. There has been much work on predicting when ecosystems will shift between stable states, but less work on why some ecosystems are able to exist in alternative stable states in the first place. The paper by Ardichvili, Loeuille, and Dakos (2022) addresses this question using a simple model of a shallow lake. Their model is based on a trade-off between access to light and nutrient availability in the water column, two essential resources for the macrophytes they model. They then identify conditions when the ancestral macrophyte will diversify resulting in macrophyte species living at new depths within the lake. The authors find a range of conditions where alternative stable states can evolve, but the range is narrow. Nonetheless, their model suggests that for alternative stable states to exist, one requirement is for there to be asymmetric competition between competing species, with one species being a better competitor on one limiting resource, with the other being a better competitor on a second limiting resource. 

These results are interesting and add to growing literature on how asymmetric competition can aid species coexistence. Asymmetric competition may be widespread in nature, with closely related species often being superior competitors on different resources. Incorporating asymmetric competition, and its evolution, into models does complicate theoretical investigations, but Ardichvili, Loeuille, and Dakos’ paper elegantly shows how substantial progress can be made with a model that is still (relatively) simple.

References 

Ardichvili A, Loeuille N, Dakos V (2022) Evolutionary emergence of alternative stable states in shallow lakes. bioRxiv, 2022.02.23.481597, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.02.23.481597

Evolutionary emergence of alternative stable states in shallow lakesAlice Ardichvili, Nicolas Loeuille, Vasilis Dakos<p style="text-align: justify;">Ecosystems under stress may respond abruptly and irreversibly through tipping points. Although much is explored on the mechanisms that affect tipping points and alternative stable states, little is known on how ecos...Community ecology, Competition, Eco-evolutionary dynamics, Theoretical ecologyTim Coulson2022-03-01 10:54:05 View
24 May 2023
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Evolutionary determinants of reproductive seasonality: a theoretical approach

When does seasonal reproduction evolve?

Recommended by ORCID_LOGO based on reviews by Francois-Xavier Dechaume-Moncharmont, Nigel Yoccoz and 1 anonymous reviewer

Have you ever wondered why some species breed seasonally while others do not? You might think it is all down to lattitude and the harshness of winters but it turns out it is quite a bit more complicated than that. A consequence of this is that climate change may result in the evolution of the degree of seasonal reproduction, with some species perhaps becoming less seasonal and others more so even in the same habitat. 

Burtschell et al. (2023) investigated how various factors influence seasonal breeding by building an individual-based model of a baboon population from which they calculated the degree of seasonality for the fittest reproductive strategy. They then altered key aspects of their model to examine how these changes impacted the degree of seasonality in the reproductive strategy. What they found is fascinating. 

The degree of seasonality in reproductive strategy is expected to increase with increased seasonality in the environment, decreased food availability, increased energy expenditure, and how predictable resource availability is. Interestingly, neither female cycle length nor extrinsic infant mortality influenced the degree of seasonality in reproduction.

What this means in reality for seasonal species is more challenging to understand. Some environments appear to be becoming more seasonal yet less predictable, and some species appear to be altering their daily energy budgets in response to changing climate in quite complex ways. As with pretty much everything in biology, Burtschell et al.'s work reveals much nuance and complexity, and that predicting how species might alter their reproductive timing is fraught with challenges.

The paper is very well written. With a simpler model it may have proven possible to achieve analytical solutions, but this is a very minor gripe. The reviewers were positive about the paper, and I have little doubt it will be well-cited. 

REFERENCES

Burtschell L, Dezeure J, Huchard E, Godelle B (2023) Evolutionary determinants of reproductive seasonality: a theoretical approach. bioRxiv, 2022.08.22.504761, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.08.22.504761

Evolutionary determinants of reproductive seasonality: a theoretical approachLugdiwine Burtschell, Jules Dezeure, Elise Huchard, Bernard Godelle<p style="text-align: justify;">Reproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood ...Evolutionary ecology, Life history, Theoretical ecologyTim Coulson Nigel Yoccoz2022-08-23 21:37:28 View