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16 Jun 2020
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Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework

Stasis and the phenotypic gambit

Recommended by based on reviews by Jacob Johansson, Katja Räsänen and 1 anonymous reviewer

The preprint "Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework" by Coulson (2020) presents a general framework for evolutionary ecology, useful to interpret patterns of selection and evolutionary responses to environmental transitions. The paper is written in an accessible and intuitive manner. It reviews important concepts which are at the heart of evolutionary ecology. Together, they serve as a worldview which you can carry with you to interpret patterns in data or observations in nature. I very much appreciate it that Coulson (2020) presents his personal intuition laid bare, the framework he uses for his research and how several strong concepts from theoretical ecology fit in there. Overviews as presented in this paper are important to understand how we as researchers put the pieces together.
A main message of the paper is that resource detection and acquisition traits, broadly called "resource accrual traits" are at the core of evolutionary dynamics. These traits and the processes they are involved in often urge some degree of individual specialization. Not all traits are resource accrual traits all the time. Guppies are cited as an example, which have traits in high predation environments that make foraging easier for them, such as being less conspicuous to predators. In the absence of predators, these same traits might be neutral. Their colour pattern might then contribute much less to the odds of obtaining resources.
"Resource accrual" reminds me of discussions of resource holding potential (Parker 1974), which can be for example the capacity to remain on a bird feeder without being dislodged. However, the idea is much broader and aggression does not need to be important for the acquisition of resources. Evolutionary success is reserved for those steadily obtaining resources. This recalls the pessimization principle of Metz et al. (2008), which applies in a restricted set of situations and where the strategy which persists at the lowest resource levels systematically wins evolutionary contests. If this principle would apply universally, the world then inherently become the worst possible. Resources determine energy budgets and different life history strategies allocate these differently to maximize fitness. The fine grain of environments and the filtration by individual histories generate a lot of variation in outcomes. However, constraint-centered approaches (Kempes et al. 2019, Kooijman 2010) are mentioned but are not at the core of this preprint. Evolution is rather seen as dynamic programming optimization with interactions within and between species. Coulson thus extends life history studies such as for example Tonnabel et al. (2012) with eco-evolutionary feedbacks. Examples used are guppies, algae-rotifer interactions and others. Altogether, this makes for an optimistic paper pushing back the pessimization principle.
Populations are expected to spend most of the time in quasi-equilibrium states where the long run stochastic growth rate is close to zero for all genotypes, alleles or other chosen classes. In the preprint, attention is given to reproductive value calculus, another strong tool in evolutionary dynamics (Grafen 2006, Engen et al. 2009), which tells us how classes within a population contribute to population composition in the distant future. The expected asymptotic fitness of an individual is equated to its expected reproductive value, but this might require particular ways of calculating reproductive values (Coulson 2020). Life history strategies can also be described by per generation measures such as R0 (currently on everyone's radar due to the coronavirus pandemic), generation time etc. Here I might disagree because I believe that this focus in per generation measures can lead to an incomplete characterization of plastic and other strategies involved in strategies such as bet-hedging. A property at quasi-equilibrium states is precise enough to serve as a null hypothesis which can be falsified: all types must in the long run leave equal numbers of descendants. If there is any property in evolutionary ecology which is useful it is this one and it rightfully merits attention.
However, at quasi-equilibrium states, directional selection has been observed, often without the expected evolutionary response. The preprint aims to explain this and puts forward the presence of non-additive gene action as a mechanism. I don't believe that it is the absence of clonal inheritance which matters very much in itself (Van Dooren 2006) unless genes with major effect are present in protected polymorphisms. The preprint remains a bit unclear on how additive gene action is broken, and here I add from the sphere in which I operate. Non-additive gene action can be linked to non-linear genotype-phenotype maps (Van Dooren 2000, Gilchrist and Nijhout 2001) and if these maps are non-linear enough to create constraints on phenotype determination, by means of maximum or minimum phenotypes which cannot be surpassed for any combination of the underlying traits, then they create additional evolutionary quasi-equilibrium states, with directional selection on a phenotype such as body size. I believe Coulson hints at this option (Coulson et al. 2006), but also at a different one: if body size is mostly determined by variation in resource accrual traits, then the resource accrual traits can be under stabilizing selection while body size is not. This requires that all resource accrual traits affect other phenotypic or demographic properties next to body size. In both cases, microevolutionary outcomes cannot be inferred from inspecting body sizes alone, either resource accrual traits need to be included explicitly, or non-linearities, or both when the map between resource accrual and body size is non-linear (Van Dooren 2000).
The discussion of the phenotypic gambit (Grafen 1984) leads to another long-standing issue in evolutionary biology. Can predictions of adaptation be made by inspecting and modelling individual phenotypes alone? I agree that with strongly non-linear genotype-phenotype maps they cannot and for multivariate sets of traits, genetic and phenotypic correlations can be very different (Hadfield et al. 2007). However, has the phenotypic gambit ever claimed to be valid globally or should it rather be used locally for relatively small amounts of variation? Grafen (1984) already contained caveats which are repeated here. As a first approximation, additivity might produce quite correct predictions and thus make the gambit operational in many instances. When important individual traits are omitted, it may just be misspecified. I am interested to see cases where the framework Coulson (2020) proposes is used for very large numbers of phenotypic and genotypic attributes. In the end, these highly dimensional trait distributions might basically collapse to a few major axes of variation due to constraints on resource accrual.
I highly recommend reading this preprint and I am looking forward to the discussion it will generate.

References

[1] Coulson, T. (2020) Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework. bioRxiv, 509067, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/509067
[2] Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X., and Kendall, B. E. (2006). Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evolutionary Ecology Research, 8(7), 1155-1171.
[3] Engen, S., Lande, R., Sæther, B. E. and Dobson, F. S. (2009) Reproductive value and the stochastic demography of age-structured populations. The American Naturalist 174: 795-804. doi: 10.1086/647930
[4] Gilchrist, M. A. and Nijhout, H. F. (2001). Nonlinear developmental processes as sources of dominance. Genetics, 159(1), 423-432.
[5] Grafen, A. (1984) Natural selection, kin selection and group selection. In: Behavioural Ecology: An Evolutionary Approach,2nd edn (JR Krebs & NB Davies eds), pp. 62–84. Blackwell Scientific, Oxford.
[6] Grafen, A. (2006). A theory of Fisher's reproductive value. Journal of mathematical biology, 53(1), 15-60. doi: 10.1007/s00285-006-0376-4
[7] Hadfield, J. D., Nutall, A., Osorio, D. and Owens, I. P. F. (2007). Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of evolutionary biology, 20(2), 549-557. doi: 10.1111/j.1420-9101.2006.01262.x
[8] Kempes, C. P., West, G. B., and Koehl, M. (2019). The scales that limit: the physical boundaries of evolution. Frontiers in Ecology and Evolution, 7, 242. doi: 10.3389/fevo.2019.00242
[9] Kooijman, S. A. L. M. (2010) Dynamic Energy Budget theory for metabolic organisation. University Press, third edition.
[10] Metz, J. A. J., Mylius, S.D. and Diekman, O. (2008) When does evolution optimize?. Evolutionary Ecology Research 10: 629-654.
[11] Parker, G. A. (1974). Assessment strategy and the evolution of fighting behaviour. Journal of theoretical Biology, 47(1), 223-243. doi: 10.1016/0022-5193(74)90111-8
[12] Tonnabel, J., Van Dooren, T. J. M., Midgley, J., Haccou, P., Mignot, A., Ronce, O., and Olivieri, I. (2012). Optimal resource allocation in a serotinous non‐resprouting plant species under different fire regimes. Journal of Ecology, 100(6), 1464-1474. doi: 10.1111/j.1365-2745.2012.02023.x
[13] Van Dooren, T. J. M. (2000). The evolutionary dynamics of direct phenotypic overdominance: emergence possible, loss probable. Evolution, 54(6), 1899-1914. doi: 10.1111/j.0014-3820.2000.tb01236.x
[14] Van Dooren, T. J. M. (2006). Protected polymorphism and evolutionary stability in pleiotropic models with trait‐specific dominance. Evolution, 60(10), 1991-2003. doi: 10.1111/j.0014-3820.2006.tb01837.x

Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback frameworkTim Coulson<p>I provide a general framework for linking ecology and evolution. I start from the fact that individuals require energy, trace molecules, water, and mates to survive and reproduce, and that phenotypic resource accrual traits determine an individ...Eco-evolutionary dynamics, Evolutionary ecologyTom Van Dooren2019-01-03 10:05:16 View
15 Jun 2020
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Investigating the rare behavior of male parental care in great-tailed grackles

Studying a rare behavior in a polygamous bird: male parental care in great-tailed grackles

Recommended by based on reviews by Matthieu Paquet and André C Ferreira

The Great-tailed grackle (Quiscalus mexicanus) is a polygamous bird species that is originating from Central America and rapidly expanding its geographic range toward the North, and in which females were long thought to be the sole nest builders and caretakers of the young. In their pre-registration [1], Folsom and collaborators report repeated occurrences of male parental care and develop hypotheses aiming at better understanding the occurrence and the fitness consequences of this very rarely observed male behavior. They propose to assess if male parental care correlates with the circulating levels of several relevant hormones, increases offspring survival, is a local adaptation, and is a mating strategy, in surveying three populations located in Arizona (middle of the geographic range expansion), California (northern edge of the geographic range), and in Central America (core of the range). This study is part of a 5-year bigger project.
Both reviewers and I strongly value Folsom and collaborators’ commitment to program a study, in natural field conditions, of a rare, yet likely evolutionary-important behavior, namely parental care by males of the great-tailed grackle. Yet, we all also recognized that it is a risky endeavor, and as a consequence, we wondered about the authors’ ability to reach a sufficient sample size to statistically test (all) hypotheses and predictions with enough confidence (e.g. risk of type I errors, also known as false positives).
Folsom and collaborators acknowledged these limitations in their pre-registration. (i) They made the exploratory nature of their research work clear to readers. (ii) They adapted their analysis plan in running prior power analyses and in focusing on effect sizes (estimates and confidence intervals). (iii) Last and not least, Folsom and collaborators clearly exposed a priori hypotheses, their associated predictions and alternatives, and ranked the latter based on their plausibility according to knowledge in the current and other study systems. Developing theory about male parental care behavior more generally with regard to a polygamous species that is rapidly expanding its geographic range and that is considered not to provide male parental care is without any doubt an added value to this study.
In summary, while this study will likely be insufficient to fully understand male parental care behavior of great-tailed grackles, it is much needed because it will definitely allow rejecting some predictions (e.g., if this behavior is present in all the studied populations, it would be common across range against expectation; finding only one male providing care to an unrelated offspring would lead to reject the prediction that males only care for their own offspring) and thus it will help laying the foundation of future research directions.
I strongly support the pre-registration system and thank all the contributors for producing a fruitful discussion throughout the review process, which in fine improved the clarity and logic of this pre-registration. Given the positive and encouraging reviews, the detailed and thorough answers to all comments by Folsom and collaborators, and their satisfactory and interesting revisions, I am happy to recommend this pre-registration and I look forward to seeing its outcomes.

References

[1] Folsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJ. 2020. Investigating the rare behavior of male parental care in great-tailed grackles. corinalogan.com/Preregistrations/gmalecare.html In principle acceptance by PCI Ecology of the version on 15 June 2020 corinalogan/grackles/blob/master/Files/Preregistrations/gmalecare.Rmd.

Investigating the rare behavior of male parental care in great-tailed gracklesFolsom MA, MacPherson M, Lukas D, McCune KB, Bergeron L, Bond A, Blackwell A, Rowney C, Logan CJThis is a PREREGISTRATION submitted for pre-study peer review. Our planned data collection START DATE is May 2020, therefore it would be ideal if the peer review process could be completed before then. Abstract: Great-tailed grackles (Quiscalus...Behaviour & Ethology, Biological invasions, Preregistrations, ZoologyMarie-Jeanne Holveck2019-12-05 17:38:47 View
12 May 2020
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On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations

A stronger statistical test of stream restoration experiments

Recommended by based on reviews by Eric Harvey and Mariana Perez Rocha

The metacommunity framework acknowledges that local sites are connected to other sites through dispersal, and that these connectivity patterns can influence local dynamics [1]. This framework is slowly moving from a framework that guides fundamental research to being actively applied in for instance a conservation context (e.g. [2]). Swan and Brown [3,4] analyzed the results of a suite of experimental manipulations in headwater and mainstem streams on invertebrate community structure in the context of the metacommunity concept. This was an important contribution to conservation ecology.
However, David Murray-Stoker [5] was not satisfied with their statistical analyses, and recreated, and more importantly, improved their original analyses in the peer-reviewed article. The new analyses are based on a combination of a more consistent site selection, checking the model assumptions, using different estimation procedures, and focusing more on effect size calculations versus statistical significance. This peer-reviewed article is thus the perfect example of the advantages of open research: the original authors making available both the data and their R script files, initially first updating the analyses and results themselves, followed by more in-depth analyses of the original data and question.
This peer reviewed went through a very in-depth process itself, with several rounds of questions and feedback that addressed both the statistical analyses, the interpretation of the results, and the conclusions. It also, however, addressed something that is often harder to provide feedback on, for instance the tone of the argument. I hope that scientists interested in these issues will not only read the final manuscript, but also the different steps of the peer review processes. These are very informative, I think, and provide a more complete picture of mainly the raison for certain decisions.
Not only does this provide the reader interested in stream conservation with the opportunity to make up their own mind on the appropriateness of these decisions, but it could potentially lead to more analyses of this important data set. For instance, maybe a formal meta-analysis that starts with the effect sizes of all the original studies might bring some new insights into this question?

References

[1] Leibold, M. A., Holyoak, M., Mouquet, N. et al. (2004). The metacommunity concept: a framework for multi‐scale community ecology. Ecology letters, 7(7), 601-613. doi: 10.1111/j.1461-0248.2004.00608.x
[2] Heino, J. (2013). The importance of metacommunity ecology for environmental assessment research in the freshwater realm. Biological Reviews, 88(1), 166-178. doi: 10.1111/j.1469-185X.2012.00244.x
[3] Swan, C. M., and Brown, B. L. (2017). Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications, 27(7), 2209-2219. doi: 10.1002/eap.1602
[4] Swan, C. M., and Brown, B. L. (2018). Erratum for: Metacommunity theory meets restoration: isolation may mediate how ecological communities respond to stream restoration. Ecological Applications 28:1370–1371. doi: 10.1002/eap.1738
[5] Murray-Stoker, D. (2020). On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendations. bioRxiv, 611939, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/611939

On the efficacy of restoration in stream networks: comments, critiques, and prospective recommendationsDavid Murray-Stoker<p>Swan and Brown (2017) recently addressed the effects of restoration on stream communities under the meta-community framework. Using a combination of headwater and mainstem streams, Swan and Brown (2017) evaluated how position within a stream ne...Community ecology, Freshwater ecology, Spatial ecology, Metacommunities & MetapopulationsKarl Cottenie2019-09-21 22:12:57 View
11 May 2020
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Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa)

Urban past predicts contemporary genetic structure in city rats

Recommended by based on reviews by Torsti Schulz, ? and 1 anonymous reviewer

Urban areas are expanding worldwide, and have become a dominant part of the landscape for many species. Urbanization can fragment pre-existing populations of vulnerable species leading to population declines and the loss of connectivity. On the other hand, expansion of urban areas can also facilitate the spread of human commensals including pests. Knowledge of the features of cityscapes that facilitate gene flow and maintain diversity of pests is thus key to their management and eradication.
Cities are complex mosaics of natural and manmade surfaces, and habitat quality is not only influenced by physical aspects of the cityscape but also by socioeconomic factors and human behaviour. Constant development means that cities also change rapidly in time; contemporary urban life reflects only a snapshot of the environmental conditions faced by populations. It thus remains a challenge to identify the features that actually drive ecology and evolution of populations in cities [1]. While several studies have highlighted strong urban clines in genetic structure and adaption [2], few have considered the influence of factors beyond physical aspects of the cityscape or historical processes.
In this paper, Stragier et al. [3] sought to identify the current and past features of the cityscape and socioeconomic factors that shape genetic structure and diversity of the house mouse (Mus musculus domesticus) in Dakar, Senegal. The authors painstakingly digitized historical maps of Dakar from the time of European settlement in 1862 to present. The authors found that the main spatial genetic cline was best explained by historical cityscape features, with higher apparent gene flow and genetic diversity in areas that were connected earlier to initial European settlements. Beyond the main trend of spatial genetic structure, they found further evidence that current features of the cityscape were important. Specifically, areas with low vegetation and poor housing conditions were found to support large, genetically diverse populations. The authors demonstrate that their results are reproducible using several statistical approaches, including modeling that explicitly accounts for spatial autocorrelation.
The work of Stragier et al. [3] thus highlights that populations of city-dwelling species are the product of both past and present cityscapes. Going forward, urban evolutionary ecologists should consider that despite the potential for rapid evolution in urban landscapes, the signal of a species’ colonization can remain for generations.

References

[1] Rivkin, L. R., Santangelo, J. S., Alberti, M. et al. (2019). A roadmap for urban evolutionary ecology. Evolutionary Applications, 12(3), 384-398. doi: 10.1111/eva.12734
[2] Miles, L. S., Rivkin, L. R., Johnson, M. T., Munshi‐South, J. and Verrelli, B. C. (2019). Gene flow and genetic drift in urban environments. Molecular ecology, 28(18), 4138-4151. doi: 10.1111/mec.15221
[3] Stragier, C., Piry, S., Loiseau, A., Kane, M., Sow, A., Niang, Y., Diallo, M., Ndiaye, A., Gauthier, P., Borderon, M., Granjon, L., Brouat, C. and Berthier, K. (2020). Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa). bioRxiv, 557066, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/557066

Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa)Claire Stragier, Sylvain Piry, Anne Loiseau, Mamadou Kane, Aliou Sow, Youssoupha Niang, Mamoudou Diallo, Arame Ndiaye, Philippe Gauthier, Marion Borderon, Laurent Granjon, Carine Brouat, Karine Berthier<p>Population genetic approaches may be used to investigate dispersal patterns of species living in highly urbanized environment in order to improve management strategies for biodiversity conservation or pest control. However, in such environment,...Biological invasions, Landscape ecology, Molecular ecologyMichelle DiLeo2019-02-22 08:36:13 View
03 Apr 2020
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A macro-ecological approach to predators' functional response

A meta-analysis to infer generic predator functional response

Recommended by based on reviews by Ludek Berec and gyorgy barabas

Species interactions are classically derived from the law of mass action: the probability that, for example, a predation event occurs is proportional to the product of the density of the prey and predator species. In order to describe how predator and prey species populations grow, is then necessary to introduce functional response, describing the intake rate of a consumer as a function of food (e.g. prey) density.
Linear functional responses shapes are typically introduced in the ecological modeling of population dynamics for both predator-prey and mutualistic systems [1,2]. Recently some works have proposed alternatives to the classic approach for mutualistic systems [3,4], both because cooperative interactions also model effect not directly related to mass action [3] and for analytical tractability [4,5].
In this work [6] the authors challenge the classic modeling of functional response also for predator-prey systems. In particular, they use a meta-analysis of several observational studies of predator-prey ecosystems to infer a generic predator functional response, fitting a phenomenological generalization of the mass-action law. Using advanced statistical analysis, they show that the functional response obtained from data is clearly different from the mass-action assumption. In fact, they found that it scales sub-linearly as the square root of the ratio between predator and prey biomass. They further argue that, from a macro-ecological point of view, using such a phenomenological relationship might be more valuable than relying on various mechanistic functional response formulations.
The manuscript thus provides an interesting different perspective on how to approach predator-prey modelling and for this reason, I have recommended the work for PCI Ecology.

References

[1] Volterra, V. (1928). Variations and Fluctuations of the Number of Individuals in Animal Species living together. ICES Journal of Marine Science, 3(1), 3–51. doi: 10.1093/icesjms/3.1.3
[2] Bastolla, U., Fortuna, M. A., Pascual-García, A., Ferrera, A., Luque, B., and Bascompte, J. (2009). The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature, 458(7241), 1018–1020. doi: 10.1038/nature07950
[3] Tu, C., Suweis, S., Grilli, J., Formentin, M., and Maritan, A. (2019). Reconciling cooperation, biodiversity and stability in complex ecological communities. Scientific Reports, 9(1), 1–10. doi: 10.1038/s41598-019-41614-2
[4] García-Algarra, J., Galeano, J., Pastor, J. M., Iriondo, J. M., and Ramasco, J. J. (2014). Rethinking the logistic approach for population dynamics of mutualistic interactions. Journal of Theoretical Biology, 363, 332–343. doi: 10.1016/j.jtbi.2014.08.039
[5] Suweis, S., Simini, F., Banavar, J. R., and Maritan, A. (2013). Emergence of structural and dynamical properties of ecological mutualistic networks. Nature, 500(7463), 449–452. doi: 10.1038/nature12438
[6] Barbier, M., Wojcik, L., and Loreau, M. (2020). A macro-ecological approach to predators’ functional response. BioRxiv, 832220, ver. 4 recommended and peer-reviewed by Peer Community in Ecology. doi: 10.1101/832220

A macro-ecological approach to predators' functional responseMatthieu Barbier, Laurie Wojcik, Michel Loreau<p>Predation often deviates from the law of mass action: many micro- and meso-scale experiments have shown that consumption saturates with resource abundance, and decreases due to interference between consumers. But does this observation hold at m...Community ecology, Food webs, Meta-analyses, Theoretical ecologySamir Simon Suweis2019-11-08 15:42:16 View
03 Apr 2020
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Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)

Is vertebral count in mammals influenced by developmental temperature? A study with Dasypus novemcinctus

Recommended by based on reviews by Darin Croft and ?

Mammals show a very low level of variation in vertebral count, both among and within species, in comparison to other vertebrates [1]. Jordan’s rule for fishes states that the vertebral number among species increases with latitude, due to ambient temperatures during development [2]. Temperature has also been shown to influence vertebral count within species in fish [3], amphibians [4], and birds [5]. However, in mammals the count appears to be constrained, on the one hand, by a possible relationship between the development of the skeleton and the proliferations of cell lines with associated costs (neural malformations, cancer etc., [6]), and on the other by the cervical origin of the diaphragm [7].
Knight et al. [8] investigate the effect of intrauterine temperature variation on skeletal morphology during development, and focus on a particular mammal, Dasypus novemcinctus, or nine-banded armadillo. Armadillos (Xenarthra) and are characterized by relatively low body temperatures and low basal rates of metabolism. Dasypus novemcinctus is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the U.S., and one of the few mammals that invaded North America from South America. It is one of few placentals that withstand considerable decrease of body temperature without torpor. It presents a resting body temperature that is low and variable for a placental mammal of its size [9] and is the only vertebrate that gives birth to monozygotic quadruplets. Among 42 monotreme, marsupial and placental genera, Dasypus novemcinctus shows the highest variation of thoracolumbar vertebral count [10].
The particularities of Dasypus novemcinctus regarding vertebral count variation and ability to withstand variable temperature qualify it as a target organism for study of the relationship between skeleton morphology and temperature in mammals.
Knight et al. [8] explored variability in vertebral count within Dasypus novemcinctus to understand whether temperature during development determines skeleton morphology. To this end they experimented with 22 armadillos (19 with data) and litters from 12 pregnant females, in two environments, for three years — an impressive effort and experimental setup. Moreover, they used a wide variety of advanced experimental and analytical techniques. For example, they implanted intra-abdominal, long-term temperature recorders, which recorded data every 6 to 120 minutes for up to several months. They analysed body temperature periodicity by approximation of the recordings with Fourier series, and they CT-scanned fetuses.
All 19 individuals (from which data could be gathered) exhibited substantial daily variation in body temperature. Several intriguing results emerged such as the counter-intuitive finding that the mammals’ body temperature fluctuates more indoors than outdoors. Furthermore, three females (out of 12) were found to have offspring with atypical skeletons, and two of these mothers presented an extremely low internal temperature early in pregnancy. Additionally, genetically identical quadruplets differed skeletally among themselves within two litters.
Results are not yet definitive about the relationship of temperature during development and vertebral count in Dasypus novemcinctus. However, Knight et al. [8] demonstrated that nine-banded armadillos survive with high daily internal temperature fluctuations and successfully bring to term offspring which vary in skeletal morphology among and within genetically identical litters despite major temperature extremes.

References

[1] Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences, 107, 18903–18908. doi: 10.1073/pnas.1010335107
[2] Jordan, D.S. (1892) Relations of temperature to vertebrae among fishes. Proceedings of the United States National Museum, 1891, 107-120. doi: 10.5479/si.00963801.14-845.107
[3] Tibblin P, Berggren H, Nordahl O, Larsson P, Forsman A (2016) Causes and consequences of intra-specific variation in vertebral number. Scientific Reports, 6, 1–12. doi: 10.1038/srep26372
[4] Peabody RB, Brodie ED (1975) Effect of temperature, salinity and photoperiod on the number of trunk vertebrae in Ambystoma maculatum. Copeia, 1975, 741–746. doi: 10.2307/1443326
[5] Lindsey CC, Moodie GEE (1967) The effect of incubation temperature on vertebral count in the chicken. Canadian Journal of Zoology, 45, 891–892. doi: 10.1139/z67-099
[6] Galis F, Dooren TJMV, Feuth JD, Metz JAJ, Witkam A, Ruinard S, Steigenga MJ, Wunaendts LCD (2006) Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60, 2643–2654. doi: 10.1111/j.0014-3820.2006.tb01896.x
[7] Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evolution and Development, 11, 69–79. doi: 10.1111/j.1525-142X.2008.00303.x
[8] Knight F, Connor C, Venkataramanan R, Asher RJ. (2020). Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus). PCI-Ecology. doi: 10.17863/CAM.50971
[9] McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. Journal of Mammalogy, 61, 606–627. doi: 10.2307/1380307
[10] Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology, 24, 1080–1090. doi: 10.1111/j.1420-9101.2011.02240.x

Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus)Frank Knight, Cristin Connor, Ramji Venkataramanan, Robert J. Asher<p>The nine banded armadillo (*Dasypus novemcinctus*) is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the USA. It is not known to hibernate, but has been associated with unusually labile core body te...Behaviour & Ethology, Evolutionary ecology, Life history, Physiology, ZoologyMar Sobral2019-11-22 22:57:31 View
30 Mar 2020
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Environmental variables determining the distribution of an avian parasite: the case of the Philornis torquans complex (Diptera: Muscidae) in South America

Catching the fly in dystopian times

Recommended by based on reviews by 4 anonymous reviewers

Host-parasite interactions are ubiquitous on Earth. They are present in almost every conceivable ecosystem and often result from a long history of antagonist coevolution [1,2]. Recent studies on climate change have revealed, however, that modification of abiotic variables are often accompanied by shifts in the distributional range of parasites to habitats far beyond their original geographical distribution, creating new interactions in novel habitats with unpredictable consequences for host community structure and organization [3,4]. This situation may be especially critical for endangered host species having small population abundance and restricted distribution range. The infestation of bird species with larvae of the muscid fly genus Philornis is a case in point. At least 250 bird species inhabiting mostly Central and South America are infected by Philornis flies [5,6]. Fly larval development occurs in bird faeces, nesting material, or inside nestlings, affecting the development and nestling survival.
Recent reports indicate significant reduction of bird numbers associated with recent Philornis infection, the most conspicuous being Galapagos finches [7,8]. One way to prevent this potential effect consists in to examine the expected geographical shift of Philornis fly species under future climate change scenarios so that anticipatory conservation practices become implemented for endangered bird species. In this regard, Ecological Niche Modeling (ENM) techniques have been increasingly used as a useful tool to predict disease transmission as well as the species becoming infected under different climate change scenarios [9-11]. The paper of Cuervo et al. [12] is an important advance in this regard. By identifying for the first time the macro-environmental variables influencing the abiotic niche of species of the Philornis torquans complex in southern South America, the authors perform a geographical projection model that permits identification of the areas susceptible to be colonized by Philornis species in Argentina, Brazil, and Chile, including habitats where the parasitic fly is still largely absent at present. Their results are promissory for conservation studies and contribute to the still underdeveloped issue of the way climate change impacts on antagonistic ecological relationships.

References

[1] Thompson JN (1994) The Coevolutionary Process. University of Chicago Press.
[2] Poulin R (2007) Evolutionary Ecology of Parasites: (Second Edition). Princeton University Press. doi: 10.2307/j.ctt7sn0x
[3] Pickles RSA, Thornton D, Feldman R, Marques A, Murray DL (2013) Predicting shifts in parasite distribution with climate change: a multitrophic level approach. Global Change Biology, 19, 2645–2654. doi: 10.1111/gcb.12255
[4] Marcogliese DJ (2016) The distribution and abundance of parasites in aquatic ecosystems in a changing climate: More than just temperature. Integrative and Comparative Biology, 56, 611–619. doi: 10.1093/icb/icw036
[5] Dudaniec RY, Kleindorfer S (2006) Effects of the parasitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu - Austral Ornithology, 106, 13–20. doi: 10.1071/MU04040
[6] Antoniazzi LR, Manzoli DE, Rohrmann D, Saravia MJ, Silvestri L, Beldomenico PM (2011) Climate variability affects the impact of parasitic flies on Argentinean forest birds. Journal of Zoology, 283, 126–134. doi: 10.1111/j.1469-7998.2010.00753.x
[7] Fessl B, Sinclair BJ, Kleindorfer S (2006) The life-cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin’s finches and its impacts on nestling survival. Parasitology, 133, 739–747. doi: 10.1017/S0031182006001089
[8] Kleindorfer S, Peters KJ, Custance G, Dudaniec RY, O’Connor JA (2014) Changes in Philornis infestation behavior threaten Darwin’s finch survival. Current Zoology, 60, 542–550. doi: 10.1093/czoolo/60.4.542
[9] Johnson EE, Escobar LE, Zambrana-Torrelio C (2019) An ecological framework for modeling the geography of disease transmission. Trends in Ecology and Evolution, 34, 655–668. doi: 10.1016/j.tree.2019.03.004
[10] Carvalho BM, Rangel EF, Ready PD, Vale MM (2015) Ecological niche modelling predicts southward expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), vector of Leishmania (Leishmania) amazonensis in South America, under climate change. PLOS ONE, 10, e0143282. doi: 10.1371/journal.pone.0143282
[11] Garrido R, Bacigalupo A, Peña-Gómez F, Bustamante RO, Cattan PE, Gorla DE, Botto-Mahan C (2019) Potential impact of climate change on the geographical distribution of two wild vectors of Chagas disease in Chile: Mepraia spinolai and Mepraia gajardoi. Parasites and Vectors, 12, 478. doi: 10.1186/s13071-019-3744-9
[12] Cuervo PF, Percara A, Monje L, Beldomenico PM, Quiroga MA (2020) Environmental variables determining the distribution of an avian parasite: the case of the Philornis torquans complex (Diptera: Muscidae) in South America. bioRxiv, 839589, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/839589

Environmental variables determining the distribution of an avian parasite: the case of the Philornis torquans complex (Diptera: Muscidae) in South AmericaPablo F. Cuervo, Alejandro Percara, Lucas Monje, Pablo M. Beldomenico, Martín A. Quiroga<p>*Philornis* flies are the major cause of myasis in altricial nestlings of neotropical birds. Its impact ranges from subtle to lethal, being of major concern in endangered bird species with geographically-restricted, fragmented and small-sized p...Biogeography, Macroecology, Parasitology, Species distributionsRodrigo Medel2019-11-26 21:31:33 View
23 Mar 2020
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Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades

Tell me what you’ve eaten, I’ll tell you how much you’ll eat (and be eaten)

Recommended by and based on reviews by Bastien Castagneyrol and 1 anonymous reviewer

Tritrophic interactions have a central role in ecological theory and applications [1-3]. Particularly, systems comprised of plants, herbivores and predators have historically received wide attention given their ubiquity and economic importance [4]. Although ecologists have long aimed to understand the forces that govern alternating ecological effects at successive trophic levels [5], several key open questions remain (at least partially) unanswered [6]. In particular, the analysis of complex food webs has questioned whether ecosystems can be viewed as a series of trophic chains [7,8]. Moreover, whether systems are mostly controlled by top-down (trophic cascades) or bottom-up processes remains an open question [6].
Traditionally, studies have addressed how species diversity at different food chain compartments affect the strength and direction of trophic cascades [9]. For example, many studies have tested whether biological control was more efficient with more than one species of natural enemies [10-12]. Much less attention has been given to the role of within-species variation in shaping trophic cascades [13]. In particular, whereas the impact of trait variation within species of plants or predators on successive trophic levels has been recently addressed [14,15], the impact of intraspecific herbivore variation is in its infancy (but see [16]). This is at odds with the resurgent acknowledgment of the importance of individual variation for several ecological processes operating at higher levels of biological organization [17].
Sources of variation within species can come in many flavours. In herbivores, striking ecological variation can be found among populations occurring on different host plants, which become genetically differentiated, thus forming host races [18,19]. Curiously, the impact of variation across host races on the strength of trophic cascades has, to date, not been explored. This is the gap that the manuscript by Sentis and colleagues [20] fills. They experimentally studied a curious tri-trophic system where the primary consumer, pea aphids, specializes in different plant hosts, creating intraspecific variation across biotypes. Interestingly, there is also ecological variation across lineages from the same biotype. The authors set up experimental food chains, where pea aphids from different lineages and biotypes were placed in their universal legume host (broad bean plants) and then exposed to a voracious but charming predator, ladybugs. The full factorial design of this experiment allowed the authors to measure vertical effects of intraspecific variation in herbivores on both plant productivity (top-down) and predator individual growth (bottom-up).
The results nicely uncover the mechanisms by which intraspecific differences in herbivores precipitates vertical modulation in food chains. Herbivore lineage and host-plant specialization shaped the strength of trophic cascades, but curiously these effects were not modulated by density-dependence. Further, ladybugs consuming pea aphids from different lineages and biotypes grew at distinct rates, revealing bottom-up effects of intraspecific variation in herbivores.
These findings are novel and exciting for several reasons. First, they show how intraspecific variation in intermediate food chain compartments can simultaneously reverberate both top-down and bottom-up effects. Second, they bring an evolutionary facet to the understanding of trophic cascades, providing valuable insights on how genetically differentiated populations play particular ecological roles in food webs. Finally, Sentis and colleagues’ findings [20] have critical implications well beyond their study systems. From an applied perspective, they provide an evident instance on how consumers’ evolutionary specialization matters for their role in ecosystems processes (e.g. plant biomass production, predator conversion rate), which has key consequences for biological control initiatives and invasive species management. From a conceptual standpoint, their results ignite the still neglected value of intraspecific variation (driven by evolution) in modulating the functioning of food webs, which is a promising avenue for future theoretical and empirical studies.

References

[1] Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., & Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual review of Ecology and Systematics, 11(1), 41-65. doi: 10.1146/annurev.es.11.110180.000353
[2] Olff, H., Brown, V.K. & Drent, R.H. (1999). Herbivores: between plants and predators. Blackwell Science, Oxford.
[3] Tscharntke, T. & Hawkins, B.A. (2002). Multitrophic level interactions. Cambridge University Press. doi: 10.1017/CBO9780511542190
[4] Agrawal, A. A. (2000). Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current opinion in plant biology, 3(4), 329-335. doi: 10.1016/S1369-5266(00)00089-3
[5] Pace, M. L., Cole, J. J., Carpenter, S. R., & Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution, 14(12), 483-488. doi: 10.1016/S0169-5347(99)01723-1
[6] Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., ... & Mooney, K. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology letters, 22(12), 2151-2167. doi: 10.1111/ele.13392
[7] Polis, G.A. & Winemiller, K.O. (1996). Food webs. Integration of patterns and dynamics. Chapmann & Hall, New York. doi: 10.1007/978-1-4615-7007-3
[8] Torres‐Campos, I., Magalhães, S., Moya‐Laraño, J., & Montserrat, M. (2020). The return of the trophic chain: Fundamental vs. realized interactions in a simple arthropod food web. Functional Ecology, 34(2), 521-533. doi: 10.1111/1365-2435.13470
[9] Polis, G. A., Sears, A. L., Huxel, G. R., Strong, D. R., & Maron, J. (2000). When is a trophic cascade a trophic cascade?. Trends in Ecology & Evolution, 15(11), 473-475. doi: 10.1016/S0169-5347(00)01971-6
[10] Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in ecology & evolution, 13(9), 350-355. doi: 10.1016/S0169-5347(98)01437-2
[11] Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. Journal of Applied Ecology, 50(1), 262-270. doi: 10.1111/1365-2664.12032
[12] Snyder, W. E. (2019). Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biological control, 135, 73-82. doi: 10.1016/j.biocontrol.2019.04.017
[13] Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T., ... & Palkovacs, E. P. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2(1), 57-64. doi: 10.1038/s41559-017-0402-5
[14] Bustos‐Segura, C., Poelman, E. H., Reichelt, M., Gershenzon, J., & Gols, R. (2017). Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage. Ecology Letters, 20(1), 87-97. doi: 10.1111/ele.12713
[15] Start, D., & Gilbert, B. (2017). Predator personality structures prey communities and trophic cascades. Ecology letters, 20(3), 366-374. doi: 10.1111/ele.12735
[16] Turcotte, M. M., Reznick, D. N., & Daniel Hare, J. (2013). Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid. The American Naturalist, 181(S1), S46-S57. doi: 10.1086/668078
[17] Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., ... & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in ecology & evolution, 26(4), 183-192. doi: 10.1016/j.tree.2011.01.009
[18] Drès, M., & Mallet, J. (2002). Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1420), 471-492. doi: 10.1098/rstb.2002.1059
[19] Magalhães, S., Forbes, M. R., Skoracka, A., Osakabe, M., Chevillon, C., & McCoy, K. D. (2007). Host race formation in the Acari. Experimental and Applied Acarology, 42(4), 225-238. doi: 10.1007/s10493-007-9091-0
[20] Sentis, A., Bertram, R., Dardenne, N., Simon, J.-C., Magro, A., Pujol, B., Danchin, E. and J.-L. Hemptinne (2020) Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades. bioRxiv, 722140, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/722140

Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascadesArnaud Sentis, Raphaël Bertram, Nathalie Dardenne, Jean-Christophe Simon, Alexandra Magro, Benoit Pujol, Etienne Danchin and Jean-Louis Hemptinne<p>Trophic cascades, the indirect effect of predators on non-adjacent lower trophic levels, are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of t...Community ecology, Eco-evolutionary dynamics, Food webs, Population ecologySara Magalhães2019-08-02 09:11:03 View
06 Mar 2020
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Interplay between the paradox of enrichment and nutrient cycling in food webs

New insights into the role of nutrient cycling in food web dynamics

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

Understanding the factors that govern the relationship between structure, stability and functioning of food webs has been a central problem in ecology for many decades. Historically, apart from microbial and soil food webs, the role of nutrient cycling has largely been ignored in theoretical and empirical food web studies. A prime example of this is the widespread use of Lotka-Volterra type models in theoretical studies; these models per se are not designed to capture the effect of nutrients being released back into the system by interacting populations. Thus overall, we still lack a general understanding of how nutrient cycling affects food web dynamics.
A new study by Quévreux, Barot and Thébault [1] tackles this problem by building a new food web model. This model features some important biological details: trophic interactions and vital rates constrained by species' body masses (using Ecological Metabolic Theory), adaptive foraging, and stoichiometric rules to ensure meaningful conversion between carbon and nutrient flows. The authors analyze the model through detailed simulations combined with thorough sensitivity analyses of model assumptions and parametrizations (including of allometric scaling relationships). I am happy to recommend this preprint because of the novelty of the work and it's technical quality.
The study yields interesting and novel findings. Overall, nutrient cycling does have a strong effect on community dynamics. Nutrient recycling is driven mostly by consumers at low mineral nutrient inputs, and by primary producers at high inputs. The extra nutrients made available through recycling increases species' persistence at low nutrient input levels, but decreases persistence at higher input levels by increasing population oscillations (a new, nuanced perspective on the classical "paradox of enrichment"). Also, for the same level of nutrient input, food webs with nutrient recycling show more fluctuations in primary producer biomass (and less at higher trophic levels) than those without recycling, with this effect weakening in more complex food webs.
Overall, these results provide new insights, suggesting that nutrient cycling may enhance the positive effects of species richness on ecosystem stability, and point at interesting new directions for future theoretical and empirical studies.

References

[1] Quévreux, P., Barot, S. and E. Thébault (2020) Interplay between the paradox of enrichment and nutrient cycling in food webs. bioRxiv, 276592, ver. 7 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/276592

Interplay between the paradox of enrichment and nutrient cycling in food websPierre Quévreux, Sébastien Barot and Élisa Thébault<p>Nutrient cycling is fundamental to ecosystem functioning. Despite recent major advances in the understanding of complex food web dynamics, food web models have so far generally ignored nutrient cycling. However, nutrient cycling is expected to ...Biodiversity, Community ecology, Ecosystem functioning, Food webs, Interaction networks, Theoretical ecologySamraat Pawar2018-11-03 21:47:37 View
06 Mar 2020
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A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Marine holobiont in the high throughput sequencing era

Recommended by and based on reviews by Sophie Arnaud-Haond and Aurélie Tasiemski

The concept of holobiont dates back to more than thirty years, it was primarily coined to hypothesize the importance of symbiotic associations to generate significant evolutionary novelties. Quickly adopted to describe the now well-studied system formed by zooxanthella associated corals, this concept expanded much further after the emergence of High-Throughput Sequencing and associated progresses in metabarcoding and metagenomics.
Holobionts – defined as the association between an individual host and its microbiota - are now increasingly described at sea and on land. The opinion article by Dittami et al. [1] provides a synthetic overview of marine holobionts. It retraces the history of the holobiont concept, recalls the main mechanisms underlying the association between hosts and microbial communities, highlights the influence of these symbioses on marine ecosystem functioning, and outlines current tools and future lines of research.
In particular, the article discusses some particularities of marine systems, such as the strong connectivity allowing an exchange of microorganisms and chemical signals between and within holobionts.
The authors advocate the need to bridge the gap between large scale exploration studies and smaller scale mechanistic studies, by conducting interdisciplinary research (combining physiology, biochemistry, ecology, experimentation and computational modeling) on some keystone holobionts.
Finally, one strength of the paper by Dittami et al. [1] is that it places the concept of the holobiont in an applied research framework. Several possible applications of knowledge on host-microbiota interactions are suggested, both in the field of aquaculture and that of monitoring the health of marine ecosystems. This article contains all the necessary elements for someone who would like to jump into the study of the holobionths in the marine world.

References
[1] Dittami SM, Arboleda E, Auguet J, Bigalke A, Briand E, Cardenas P, Cardini U, Decelle J, Engelen AH, Eveillard D, Gachon CMM, Griffiths SM, Harder T, Kayal E, Kazamia E, Lallier FH, Medina M, Marzinelli E, Morganti T, Núñez Pons L, Prado S, Pintado J, Saha M, Selosse M, Skillings D, Stock W, Sunagawa S, Toulza E, Vorobev A, Leblanc C, Not F. (2020). A community perspective on the concept of marine holobionts: current status, challenges, and future directions. Zenodo, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.5281/zenodo.3696771

A community perspective on the concept of marine holobionts: current status, challenges, and future directionsSimon M. Dittami, Enrique Arboleda, Jean-Christophe Auguet, Arite Bigalke, Enora Briand, Paco Cárdenas, Ulisse Cardini, Johan Decelle, Aschwin Engelen, Damien Eveillard, Claire M.M. Gachon, Sarah Griffiths, Tilmann Harder, Ehsan Kayal, Elena Kazam...Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. T...Marine ecology, Microbial ecology & microbiology, SymbiosisSophie Arnaud-Haond2019-02-05 17:57:11 View