|Id||Title||Authors||Abstract||Picture||Thematic fields||Recommender||Reviewers||Submission date|
30 May 2023
slendr: a framework for spatio-temporal population genomic simulations on geographic landscapesMartin Petr, Benjamin C. Haller, Peter L. Ralph, Fernando Racimo https://doi.org/10.1101/2022.03.20.485041
A new powerful tool to easily encode the geo-spatial dimension in population genetics simulationsRecommended by Emiliano Trucchi based on reviews by Liisa Loog and 2 anonymous reviewers
Models explaining the evolutionary processes operating in living beings are often impossible to test in the real world. This is mainly because of the long time (i.e., the number of generations) which is necessary for evolution to unfold. In addition, any such experiment would require a large number of individuals and, more importantly, many replicates to account for the inherent variance of the evolutionary processes under investigation. Only organisms with fast generation times and favourable rearing conditions can be used to explicitly test for specific evolutionary hypotheses.
Computer simulations have filled this gap, revolutionising experimental testing in evolutionary biology by integrating genetic models into complex population dynamics, which can be run for (potentially) any length of time. Without going into an extensive description of the many available approaches for population genetics simulations (an exhaustive review can be found in Hoban et al 2012), three main aspects are, in my opinion, important for categorising and choosing one simulation approach over another. The first concerns the basic distinction between coalescent-based and individual-based simulators: the former being an efficient approach, which simulates back in time the coalescence events of a sample of homologous DNA fragments, while the latter is a more computationally intensive approach where all of the individuals (and their underlying genetic/genomic features) in the population are simulated forward-in-time, generation after generation. The second aspect concerns the simulation of natural selection. Although natural selection can be integrated into backward-in-time simulations, it is more realistically implemented as individual-based fitness in forward-in-time simulators. The third point, which has been often overlooked in evolutionary simulations, is about the possibility to design a simulation scenario where individuals and populations can exploit a physical (geographical) space.
Amongst the coalescent-based simulators, SPLATCHE (Currat et al 2004), and its derivatives, is one of the few simulation tools deploying the coalescence process in sub-demes which are all connected by migration, thus getting as close as possible to a spatially-explicit population. On the other hand, individual-based simulators, whose development followed the increasing power of computational machines, offer a great opportunity to include spatio-temporal dynamics within a genomic simulation model. One of the most realistic and efficient individual-based forward-in-time simulators available is SLiM (Haller and Messer 2017), which allows users to implement simulations in arbitrarily complex spaces. Here, the more challenging part is encoding the spatially-explicit scenarios using the SLiM-specific EIDOS language.
The new R package slendr (Petr et al 2022) offers a practical solution to this issue. By wrapping different tools into a well-known scripting language, slendr allows the design of spatiotemporal simulation scenarios which can be directly executed in the individual-based SLiM simulator, and the output stored with modern tree-sequence analysis tools (tskit; Kellerer et al 2018). Alternatively, simulations of non-spatial models can be run using a coalescent-based algorithm (msprime; Baumdicker et al 2022). The main advantage of slendr is that the whole simulative experiment can be performed entirely in the R environment, taking advantage of the many libraries available for geospatial and genomic data analysis, statistics, and visualisation. The open-source nature of this package, whose main aim is to make complex population genomics modelling more accessible, and the vibrant community of SLiM and tskit users will very likely make slendr widely used amongst the molecular ecology and evolutionary biology communities.
Slendr handles real Earth cartographic data where users can design realistic demographic processes which characterise natural populations (i.e., expansions, displacement of large populations, interactions among populations, migrations, population splits, etc.) by changing spatial population boundaries across time and space. All in all, slendr is a very flexible and scalable framework to test the accuracy of spatial models, hypotheses about demography and selection, and interactions between organisms across space and time.
Baumdicker, F., Bisschop, G., Goldstein, D., Gower, G., Ragsdale, A. P., Tsambos, G., ... & Kelleher, J. (2022). Efficient ancestry and mutation simulation with msprime 1.0. Genetics, 220(3), iyab229. https://doi.org/10.1093/genetics/iyab229
Currat, M., Ray, N., & Excoffier, L. (2004). SPLATCHE: a program to simulate genetic diversity taking into account environmental heterogeneity. Molecular Ecology Notes, 4(1), 139-142. https://doi.org/10.1046/j.1471-8286.2003.00582.x
Haller, B. C., & Messer, P. W. (2017). SLiM 2: flexible, interactive forward genetic simulations. Molecular biology and evolution, 34(1), 230-240. https://doi.org/10.1093/molbev/msw211
Hoban, S., Bertorelle, G., & Gaggiotti, O. E. (2012). Computer simulations: tools for population and evolutionary genetics. Nature Reviews Genetics, 13(2), 110-122. https://doi.org/10.1038/nrg3130
Kelleher, J., Thornton, K. R., Ashander, J., & Ralph, P. L. (2018). Efficient pedigree recording for fast population genetics simulation. PLoS computational biology, 14(11), e1006581. https://doi.org/10.1371/journal.pcbi.1006581
Petr, M., Haller, B. C., Ralph, P. L., & Racimo, F. (2023). slendr: a framework for spatio-temporal population genomic simulations on geographic landscapes. bioRxiv, 2022.03.20.485041, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.03.20.485041
|slendr: a framework for spatio-temporal population genomic simulations on geographic landscapes||Martin Petr, Benjamin C. Haller, Peter L. Ralph, Fernando Racimo||<p style="text-align: justify;">One of the goals of population genetics is to understand how evolutionary forces shape patterns of genetic variation over time. However, because populations evolve across both time and space, most evolutionary proce...||Bioinformatics & Computational Biology, Evolutionary Theory, Phylogeography & Biogeography, Population Genetics / Genomics||Emiliano Trucchi||2022-09-14 12:57:56||View|
22 May 2023
Weak seed banks influence the signature and detectability of selective sweepsKevin Korfmann, Diala Abu Awad, Aurélien Tellier https://doi.org/10.1101/2022.04.26.489499
New insights into the dynamics of selective sweeps in seed-banked speciesRecommended by Renaud Vitalis based on reviews by Guillaume Achaz, Jere Koskela, William Shoemaker and Simon Boitard
Many organisms across the Tree of life have the ability to produce seeds, eggs, cysts, or spores, that can remain dormant for several generations before hatching. This widespread adaptive trait in bacteria, fungi, plants and animals, has a significant impact on the ecology, population dynamics and population genetics of species that express it (Evans and Dennehy 2005).
In population genetics, and despite the recognition of its evolutionary importance in many empirical studies, few theoretical models have been developed to characterize the evolutionary consequences of this trait on the level and distribution of neutral genetic diversity (see, e.g., Kaj et al. 2001; Vitalis et al. 2004), and also on the dynamics of selected alleles (see, e.g., Živković and Tellier 2018). However, due to the complexity of the interactions between evolutionary forces in the presence of dormancy, the fate of selected mutations in their genomic environment is not yet fully understood, even from the most recently developed models.
In a comprehensive article, Korfmann et al. (2023) aim to fill this gap by investigating the effect of germ banking on the probability of (and time to) fixation of beneficial mutations, as well as on the shape of the selective sweep in their vicinity. To this end, Korfmann et al. (2023) developed and released their own forward-in-time simulator of genome-wide data, including neutral and selected polymorphisms, that makes use of Kelleher et al.’s (2018) tree sequence toolkit to keep track of gene genealogies.
The originality of Korfmann et al.’s (2023) study is to provide new quantitative results for the effect of dormancy on the time to fixation of positively selected mutations, the shape of the genomic landscape in the vicinity of these mutations, and the temporal dynamics of selective sweeps. Their major finding is the prediction that germ banking creates narrower signatures of sweeps around positively selected sites, which are detectable for increased periods of time (as compared to a standard Wright-Fisher population).
The availability of Korfmann et al.’s (2023) code will allow a wider range of parameter values to be explored, to extend their results to the particularities of the biology of many species. However, as they chose to extend the haploid coalescent model of Kaj et al. (2001), further development is needed to confirm the robustness of their results with a more realistic diploid model of seed dormancy.
Evans, M. E. K., and J. J. Dennehy (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. The Quarterly Review of Biology, 80(4): 431-451. https://doi.org/10.1086/498282
Kaj, I., S. Krone, and M. Lascoux (2001) Coalescent theory for seed bank models. Journal of Applied Probability, 38(2): 285-300. https://doi.org/10.1239/jap/996986745
Kelleher, J., K. R. Thornton, J. Ashander, and P. L. Ralph (2018) Efficient pedigree recording for fast population genetics simulation. PLoS Computational Biology, 14(11): e1006581. https://doi.org/10.1371/journal.pcbi.1006581
Korfmann, K., D. Abu Awad, and A. Tellier (2023) Weak seed banks influence the signature and detectability of selective sweeps. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.04.26.489499
Vitalis, R., S. Glémin, and I. Olivieri (2004) When genes go to sleep: the population genetic consequences of seed dormancy and monocarpic perenniality. American Naturalist, 163(2): 295-311. https://doi.org/10.1086/381041
Živković, D., and A. Tellier (2018). All but sleeping? Consequences of soil seed banks on neutral and selective diversity in plant species. Mathematical Modelling in Plant Biology, 195-212. https://doi.org/10.1007/978-3-319-99070-5_10
|Weak seed banks influence the signature and detectability of selective sweeps||Kevin Korfmann, Diala Abu Awad, Aurélien Tellier||<p style="text-align: justify;">Seed banking (or dormancy) is a widespread bet-hedging strategy, generating a form of population overlap, which decreases the magnitude of genetic drift. The methodological complexity of integrating this trait impli...||Adaptation, Bioinformatics & Computational Biology, Evolutionary Applications, Evolutionary Ecology, Genome Evolution, Life History, Population Genetics / Genomics||Renaud Vitalis||2022-05-23 13:01:57||View|
16 May 2023
A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofsThierry de Meeûs and Camille Noûs https://doi.org/10.5281/zenodo.7927968
All you ever wanted to know about Ne in one handy placeRecommended by Charles Baer based on reviews by Jesse ("Jay") Taylor and 1 anonymous reviewer
Of the four evolutionary forces, three can be straightforwardly summarized both conceptually and mathematically in the context of an allele at a genomic locus. Mutation (the mutation rate, μ) is simply captured by the per-site, per-generation probability that an allele mutates into a different allele. Recombination (the recombination rate, r) is captured as the probability of recombination between two sites, wherein alleles that are in different genomes in one generation come together in the same genome in the next generation. Natural selection (the selection coefficient, s) is captured by the probability that an allele is present in the next generation, relative to some reference.
Random genetic drift – the random fluctuation in allele frequency due to sampling in a finite population - is not so straightforwardly summarized. The first, and most common way of characterizing evolutionary dynamics in a finite population is the Wright-Fisher model, in which the only deviation from the assumptions of Hardy-Weinberg conditions is finite population size. Importantly, in a W-F population, mating between diploid individuals is random, which implies self-fertile monoecy, and generations are non-overlapping. In an ideal W-F population, the probability that a gene copy leaves i descendants in the next generation is the result of binomial sampling of uniting gametes (if the locus is biallelic). The – and the next word is meaningful – magnitude/strength/rate/power/amount of genetic drift is proportional to 1/2N, where N is the size of the population. All of the following are affected by genetic drift: (1) the probability that a neutral allele ultimately reaches fixation, (2) the rate of loss of genetic variation within a population, (3) the rate of increase of genetic variance among populations, (4) the amount of genetic variation segregating in a population, (5) the probability of fixation/loss of a weakly selected variant.
Presumably no real population adheres to ideal W-F conditions, which leads to the notion of "effective population size", Ne (Wright 1931), loosely defined as "the size of an ideal W-F population that experiences an equivalent strength of genetic drift". Almost always, Ne<N, and any violation of W-F assumptions can affect Ne. Importantly, Ne can be defined in different ways, and the specific formulation of Ne can have different implications for evolution. Ne was initially defined in terms of the rate of decrease of heterozygosity (inbreeding effective size) and increase in variance among populations (variance effective size). Ewens (1979) defined the Eigenvalue effective size (equivalent to the "random extinction" effective size) and elaborated on the conditions under which the various formulations of Ne differ (Ewens 1982). Nordborg and Krone (2002) defined the effective size in terms of the coalescent, and they identified conditions in which genetic drift cannot be described in terms of a W-F model (Sjodin et al. 2005); also see Karasov et al. (2010); Neher and Shraiman (2011).
Distinct from the issue of defining Ne is the issue of calculating Ne from data, which is the focus of this paper by De Meeus and Noûs (2023). Pudovkin et al. (1996) showed that the Eigenvalue effective size in a dioecious population can be formulated in terms of excess heterozygosity, which the current authors note is equivalent to formulating Ne in terms of Wright's FIS statistic. As emphasized by the title, the marquee contribution of this paper is to provide a better approximation of the Eigenvalue effective size in a dioecious population. Science marches onward, although the empirical utility of this advance is obviously limited, given the tremendous inherent sources of uncertainty in real-world estimates of Ne. Perhaps more valuable, however, is the extensive set of appendixes, in which detailed derivations are provided for the various formulations of effective size. By way of analogy, the material presented here can be thought of as an extension of the material presented in section 7.6 of Crow and Kimura (1970), in which the Inbreeding and Variance effective population sizes are derived and compared. The appendixes should serve as a handy go-to source of detailed theoretical information with respect to the different formulations of effective population size.
Crow, J. F. and M. Kimura. 1970. An Introduction to Population Genetics Theory. The Blackburn Press, Caldwell, NJ.
De Meeûs, T. and Noûs, C. 2023. A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofs. Zenodo, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.5281/zenodo.7927968
Ewens, W. J. 1979. Mathematical Population Genetics. Springer-Verlag, Berlin.
Ewens, W. J. 1982. On the concept of the effective population size. Theoretical Population Biology 21:373-378. https://doi.org/10.1016/0040-5809(82)90024-7
Karasov, T., P. W. Messer, and D. A. Petrov. 2010. Evidence that adaptation in Drosophila Is not limited by mutation at single sites. Plos Genetics 6. https://doi.org/10.1371/journal.pgen.1000924
Neher, R. A. and B. I. Shraiman. 2011. Genetic Draft and Quasi-Neutrality in Large Facultatively Sexual Populations. Genetics 188:975-U370. https://doi.org/10.1534/genetics.111.128876
Nordborg, M. and S. M. Krone. 2002. Separation of time scales and convergence to the coalescent in structured populations. Pp. 194–232 in M. Slatkin, and M. Veuille, eds. Modern Developments in Theoretical Population Genetics: The Legacy of Gustave Malécot. Oxford University Press, Oxford. https://www.webpages.uidaho.edu/~krone/malecot.pdf
Pudovkin, A. I., D. V. Zaykin, and D. Hedgecock. 1996. On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383-387. https://doi.org/10.1093/genetics/144.1.383
Sjodin, P., I. Kaj, S. Krone, M. Lascoux, and M. Nordborg. 2005. On the meaning and existence of an effective population size. Genetics 169:1061-1070. https://doi.org/10.1534/genetics.104.026799
Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:0097-0159. https://doi.org/10.1093/genetics/16.2.97
|A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofs||Thierry de Meeûs and Camille Noûs||<p>The effective population size is an important concept in population genetics. It corresponds to a measure of the speed at which genetic drift affects a given population. Moreover, this is most of the time the only kind of population size that e...||Bioinformatics & Computational Biology, Evolutionary Ecology, Evolutionary Theory, Population Genetics / Genomics, Reproduction and Sex||Charles Baer||2023-02-22 16:53:49||View|
11 May 2023
Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineagesAlejandro Manzano-Marín, Armelle Coeur d'acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, Emmanuelle Jousselin https://doi.org/10.1101/2022.08.28.505559
Flexibility in Aphid Endosymbiosis: Dual Symbioses Have Evolved Anew at Least Six TimesRecommended by Olivier Tenaillon based on reviews by Alex C. C. Wilson and 1 anonymous reviewer
In this intriguing study (Manzano-Marín et al. 2022) by Alejandro Manzano-Marin and his colleagues, the association between aphids and their symbionts is investigated through meta-genomic analysis of new samples. These associations have been previously described as leading to fascinating genomic evolution in the symbiont (McCutcheon and Moran 2012). The bacterial genomes exhibit a significant reduction in size and the range of functions performed. They typically lose the ability to produce many metabolites or biobricks created by the host, and instead, streamline their metabolism by focusing on the amino acids that the host cannot produce. This level of co-evolution suggests a stable association between the two partners.
However, the new data suggests a much more complex pattern as multiple independent acquisitions of co-symbionts are observed. Co-symbiont acquisition leads to a partition of the functions carried out on the bacterial side, with the new co-symbiont taking over some of the functions previously performed by Buchnera. In most cases, the new co-symbiont also brings the ability to produce B1 vitamin. Various facultative symbiotic taxa are recruited to be co-symbionts, with the frequency of acquisition related to the bacterial niche and lifestyle.
Manzano-Marín, Alejandro, Armelle Coeur D’acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, and Emmanuelle Jousselin. 2023. “Co-Obligate Symbioses Have Repeatedly Evolved across Aphids, but Partner Identity and Nutritional Contributions Vary across Lineages.” bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.28.505559.
McCutcheon, John P., and Nancy A. Moran. 2012. “Extreme Genome Reduction in Symbiotic Bacteria.” Nature Reviews Microbiology 10 (1): 13–26. https://doi.org/10.1038/nrmicro2670.
|Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages||Alejandro Manzano-Marín, Armelle Coeur d'acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, Emmanuelle Jousselin||<p style="text-align: justify;">Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, <em>Buchnera aphidicola</em>, to supply them with essential nutrients lacking in their diet. This association ...||Genome Evolution, Other, Species interactions||Olivier Tenaillon||2022-11-16 10:13:37||View|
02 May 2023
Host-symbiont-gene phylogenetic reconciliationHugo Menet, Alexia Nguyen Trung, Vincent Daubin, Eric Tannier https://doi.org/10.1101/2022.07.01.498457
Reconciling molecular evolution and evolutionary ecology studies: a phylogenetic reconciliation method for gene-symbiont-host systemsRecommended by Emmanuelle Jousselin based on reviews by Vincent Berry and Catherine Matias
Interactions between species are a driving force in evolution. Many organisms host symbiotic partners that live all or part of their life in or on their host. Whether they are mutualistic or parasitic, these symbiotic associations impose strong selective pressures on both partners and affect their evolutionary trajectories. In fine, they can have a significant impact on the diversification patterns of both host and symbiont lineages, with symbiotic lineages sometimes speciating simultaneously with their hosts and/or switching from one host species to another. Long-term associations between species can also result in gene transfers between the involved organisms. Those lateral gene transfers are a source of ecological innovation but can obscure the phylogenetic signals and render the process of phylogenetic reconstructions complex (Lerat et al. 2003).
Methods known as reconciliations explore similarities and differences between phylogenetic trees. They have been widely used to both compare the diversification patterns of hosts and symbionts and identify lateral gene transfers between species. Though the reconciliation approaches used in host/ symbiont and species/ gene phylogenetic studies are identical, they are always applied separately to solve either molecular evolution questions or investigate the evolution of ecological interactions. However, the two questions are often intimately linked and the current interest in multi-level systems (e.g. the holobiont concept) calls for a unique model that will take into account three-level nested organization (gene/symbiont/ host) where both symbiont and genes can transfer among hosts.
Here Menet and collaborators (2023) provide such a model to produce three-level reconciliations. In order to do so, they extend the two-level reconciliation model implemented in “ALE” software (Szöllősi et al. 2013), one of the most used and proven reconciliation methods. Briefly, given a symbiont gene tree, a symbiont tree and a host tree, as in previous reconciliation models, the symbiont tree is mapped onto the host tree by mixing three types of events: Duplication, Transfer or Loss (DTL), with a possibility of the symbiont evolving temporarily outside the host phylogeny (in a “ghost” host lineage). The gene tree evolves similarly inside the symbiont tree, but horizontal transfers are constrained to symbionts co-occurring within the same host. Joint reconciliation scenarios are reconstructed and DTL event rates and likelihoods are estimated according to the model. As a nice addition, the authors propose a method to infer the symbiont phylogeny through amalgamation from gene trees and a host tree.
The authors then explore the diverse possibilities offered by this method by testing it on both simulated datasets and biological datasets in order to check whether considering three nested levels is worthwhile. They convincingly show that three-level reconciliation has a better capacity to retrieve the symbiont donors and receivers of horizontal gene transfers, probably because transfers are constrained by additional elements relevant to the biological systems. Using, aphids, their obligate endosymbionts, and the symbiont genes involved in their nutritional functions, they identify horizontal gene transfers between aphid symbionts that are missed by two-level reconciliations but detected by expertise (Manzano-Marín et al. 2020). The other dataset presented here is on the human pathogen Helicobacter pylori, which history is supposed to reflect human migration. They use more than 1000 H. pylori gene families, and four populations, and use likelihood computations to compare different hypotheses on the diversification of the host.
In summary, this study is a proof-of-concept of a 3-level reconciliation, where the authors manage to convey the applicability of their framework to many biological systems. Reported complexities, confirmed by reported running times, show that the method is computationally efficient. Without a doubt, the tool presented here will be very useful to evolutionary biologists who want to investigate multi-scale cophylogenies and it will move forward the study of associations between host and symbionts when symbiont genomic data are available.
Lerat, E., Daubin, V., & Moran, N. A. (2003). From gene trees to organismal phylogeny in prokaryotes: the case of the γ-Proteobacteria. PLoS biology, 1(1), e19.
Menet H, Trung AN, Daubin V, Tannier E (2023) Host-symbiont-gene phylogenetic reconciliation. bioRxiv, 2022.07.01.498457, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.07.01.498457
Szöllősi, G. J., Rosikiewicz, W., Boussau, B., Tannier, E., & Daubin, V. (2013). Efficient exploration of the space of reconciled gene trees. Systematic biology, 62(6), 901-912.
|Host-symbiont-gene phylogenetic reconciliation||Hugo Menet, Alexia Nguyen Trung, Vincent Daubin, Eric Tannier||<p style="text-align: justify;"><strong>Motivation:</strong> Biological systems are made of entities organized at different scales e.g. macro-organisms, symbionts, genes...) which evolve in interaction.<br>These interactions range from indepe...||Bioinformatics & Computational Biology, Phylogenetics / Phylogenomics||Emmanuelle Jousselin||2022-08-21 18:34:27||View|
02 May 2023
Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemmaLoup Rimbaud, Julien Papaïx, Jean-François Rey, Benoît Moury, Luke G. Barrett, Peter H. Thrall https://doi.org/10.1101/2022.08.30.505787
Plant resistance to pathogens: just you wait?Recommended by Timothée Poisot based on reviews by Jean-Paul Soularue and 1 anonymous reviewer
In this preprint, Rimbaud et al. (2023) examine whether Adult Plant Resistance (APR), where plants delay their response to pathogens, is a viable alternative when the solution to evolve complete resistance from the seedling stage exists. At first glance, delaying resistance seems like a counter-intuitive strategy, unless it can result in a weaker selection of the pathogen, and therefore slow down its adaption to plant resistance.
The approach of Rimbaud et al. is to incorporate as much of the mechanisms as possible into a model. By accounting for explicit spatio-temporal dynamics, stochasticity, and the coupling between demography and population genetics, to simulate an agricultural landscape, they reach a nuanced conclusion.
Weaker and delayed activation of genes that confer APR does indeed reduce the selection pressure acting on the pathogen, at the cost of overall less effective protection. The alternative strategy of rapid or complete activation of these genes, although it results in better results in defending against the pathogen, is at risk of being overcome because it introduces a stronger selection pressure.
One important feature of this work is that it accounts for agricultural practices. The landscape that is simulated can account for monoculture, mosaic cultures, mixed cultures, and rotations of crops (with different strategies for resistance). This introduces an interesting element to the conclusion: that human practices will have an impact on the selection pressures acting within the system.
Perhaps the most striking result is that, for the plants, it might be more beneficial to bear the cost of a wild-type pathogen that can benefit from delayed activation of resistance, and therefore exclude the more virulent strains by simply being there first, and essentially buying the plant some time before it activates its resistance more completely. When the landscape is aggregated, even wild-type pathogens can cause severe epidemics; increasing fragmentation, because it enables connectivity between patches of plants with different strategies, allows pathogens to move across cultivars, and reduces the epidemic risk on susceptible plants.
These results should encourage scaling up the perspective on APR, and indeed Rimbaud et al. adopt a landscape-scale perspective, to show that APR genes and genes conferring more complete resistance early on can have synergistic effects. This is, again, both an interesting result for evolutionary biologists, but also a useful way to prioritize different crop management strategies over large spatial scales.
Rimbaud, Loup, et al. Durable Resistance or Efficient Disease Control? Adult Plant Resistance (APR) at the Heart of the Dilemma. 2023. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.30.505787
|Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma||Loup Rimbaud, Julien Papaïx, Jean-François Rey, Benoît Moury, Luke G. Barrett, Peter H. Thrall||<p style="text-align: justify;">Adult plant resistance (APR) is an incomplete and delayed protection of plants against pathogens. At first glance, such resistance should be less efficient than classical major-effect resistance genes, which confer ...||Adaptation, Evolutionary Applications, Evolutionary Epidemiology||Timothée Poisot||2022-09-02 16:36:32||View|
13 Apr 2023
The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variationGustavo V Barroso, Julien Y Dutheil https://doi.org/10.1101/2021.09.16.460667
An unusual suspect: the mutation landscape as a determinant of local variation in nucleotide diversityRecommended by Fernando Racimo based on reviews by David Castellano and 1 anonymous reviewer
Sometimes, important factors for explaining biological processes fall through the cracks, and it is only through careful modeling that their importance eventually comes out to light. In this study, Barroso and Dutheil introduce a new method based on the sequentially Markovian coalescent (SMC, Marjoran and Wall 2006) for jointly estimating local recombination and coalescent rates along a genome. Unlike previous SMC-based methods, however, their method can also co-estimate local patterns of variation in mutation rates.
This is a powerful improvement which allows them to tackle questions about the reasons for the extensive variation in nucleotide diversity across the chromosomes of a species - a problem that has plagued the minds of population geneticists for decades (Begun and Aquadro 1992, Andolfatto 2007, McVicker et al., 2009, Pouyet and Gilbert 2021). The authors find that variation in de novo mutation rates appears to be the most important factor in determining nucleotide diversity in Drosophila melanogaster. Though seemingly contradicting previous attempts at addressing this problem (Comeron 2014), they take care to investigate and explain why that might be the case.
Barroso and Dutheil have also taken care to carefully explain the details of their new approach and have carried a very thorough set of analyses comparing competing explanations for patterns of nucleotide variation via causal modeling. The reviewers raised several issues involving choices made by the authors in their analysis of variance partitioning, the proper evaluation of the role of linked selection and the recombination rate estimates emerging from their model. These issues have all been extensively addressed by the authors, and their conclusions seem to remain robust. The study illustrates why the mutation landscape should not be ignored as an important determinant of local variation in genetic diversity, and opens up questions about the generalizability of these results to other organisms.
Andolfatto, P. (2007). Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome research, 17(12), 1755-1762. https://doi.org/10.1101/gr.6691007
Barroso, G. V., & Dutheil, J. Y. (2021). The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation. bioRxiv, 2021.09.16.460667, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.09.16.460667
Begun, D. J., & Aquadro, C. F. (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature, 356(6369), 519-520. https://doi.org/10.1038/356519a0
Comeron, J. M. (2014). Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genetics, 10(6), e1004434. https://doi.org/10.1371/journal.pgen.1004434
Marjoram, P., & Wall, J. D. (2006). Fast" coalescent" simulation. BMC genetics, 7, 1-9. https://doi.org/10.1186/1471-2156-7-16
McVicker, G., Gordon, D., Davis, C., & Green, P. (2009). Widespread genomic signatures of natural selection in hominid evolution. PLoS genetics, 5(5), e1000471. https://doi.org/10.1371/journal.pgen.1000471
Pouyet, F., & Gilbert, K. J. (2021). Towards an improved understanding of molecular evolution: the relative roles of selection, drift, and everything in between. Peer Community Journal, 1, e27. https://doi.org/10.24072/pcjournal.16
|The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation||Gustavo V Barroso, Julien Y Dutheil||<p style="text-align: justify;">What shapes the distribution of nucleotide diversity along the genome? Attempts to answer this question have sparked debate about the roles of neutral stochastic processes and natural selection in molecular evolutio...||Bioinformatics & Computational Biology, Population Genetics / Genomics||Fernando Racimo||2022-10-30 07:52:07||View|
11 Apr 2023
Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?Chloé Larose, Guillaume Lavanchy, Susana Freitas, Darren J. Parker, Tanja Schwander https://doi.org/10.1101/2022.03.25.485836
Facultative parthenogenesis and transitions from sexual to asexual reproductionRecommended by Trine Bilde based on reviews by 3 anonymous reviewers
Despite a vast array of ways in which organisms can reproduce (Bell, 1982), most animals engage in sexual reproduction (Otto & Lenormand, 2002). A fascinating alternative to sex is parthenogenesis, where offspring are produced asexually from a gamete, typically the egg, without receiving genetic material from another gamete (Simon, Delmotte, Rispe, & Crease, 2003). One of the long-standing questions in the field is why parthenogenesis is not more widespread, given the costs associated with sex (Otto & Lenormand, 2002). Natural populations of most species appear to be reproducing either sexually or parthenogenetically, even if a species can employ both reproductive modes (Larose et al 2023). Larose et al (2023) highlight the conundrum in this pattern, as organisms that are capable of employing parthenogenesis facultatively would be able to gain the benefits of both modes of reproduction. Why then, is facultative parthenogenesis not more common?
Larose et al (2023) propose that constraints on being efficient in both sexual and asexual reproduction could cause a trade-off between reproductive modes that favours an obligate strategy of either sex or no sex. This would provide an explanation for why facultative parthenogenesis is rare. Timema stick insects provide an excellent system to investigate reproductive strategies, as some species have parthenogenetic females, while other species are sexual, and they show repeated transitions from sexual reproduction to obligate parthenogenesis (Schwander & Crespi, 2009). The authors performed comprehensive and complementary studies in a recently discovered species T. douglasi, in which populations show both modes of reproduction, with some populations consisting only of females and others showing equal proportions of males and females. The sex ratio varied significantly, with the proportion of females ranging between 43-100% across 29 populations. These populations form a monophyletic clade with clustering into three genetic lineages and only a few cases of admixture. Females from all populations were capable of producing unfertilized eggs, but the hatching success varied hugely among populations and lineages (3-100%). Parthenogenetically produced offspring were homozygous, showing that parthenogenesis causes a complete loss of heterozygosity in a single generation. After producing eggs as virgins, females were mated to assess the capacity to also reproduce sexually, and fertilization increased the hatching success of eggs in two lineages. In one lineage, in which the hatching success of unfertilized eggs is similar to that of other sexually reproducing Timema species, fertilization reduced egg-hatching success, indicating a trade-off between reproductive modes with parthenogenetic reproduction performing best. Approximately 58% of the offspring produced after mating were fertilized, demonstrating the capacity of females to reproduce parthenogenetically also after mating has occurred, however with huge variation among individuals.
This wonderful and meticulously performed study produces strong and complementary evidence for facultative parthenogenesis in T. douglasi populations. The study shows large variation in how reproductive mode is employed, supporting the existence of a trade-off between sexual and parthenogenetic reproduction. This might be an example of an ongoing transition from sexual to asexual reproduction, which indicates that obligate parthenogenesis may derive via transient facultative parthenogenesis.
Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press. 635 p.
Otto, S. P., & Lenormand, T. (2002). Resolving the paradox of sex and recombination. Nature Reviews Genetics, 3(4), 252-261. https://doi.org/10.1038/nrg761
Schwander, T., & Crespi, B. J. (2009). Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution, 63(1), 84-103.
Simon, J.-C., Delmotte, F., Rispe, C., & Crease, T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society, 79(1), 151-163. https://doi.org/10.1046/j.1095-8312.2003.00175.x
Larose, C., Lavanchy, G., Freitas, S., Parker, D.J., Schwander, T. (2023) Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects? bioRxiv, 2022.03.25.485836, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.03.25.485836
|Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?||Chloé Larose, Guillaume Lavanchy, Susana Freitas, Darren J. Parker, Tanja Schwander||<p>Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and char...||Reproduction and Sex||Trine Bilde||2022-05-20 10:41:13||View|
30 Mar 2023
Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow in a butterflyMaría Ángeles Rodríguez de Cara, Paul Jay, Quentin Rougemont, Mathieu Chouteau, Annabel Whibley, Barbara Huber, Florence Piron-Prunier, Renato Rogner Ramos, André V. L. Freitas, Camilo Salazar, Karina Lucas Silva-Brandão, Tatiana Texeira Torres, Mathieu Joron https://doi.org/10.1101/2021.09.29.462348
Is genetic diversity enhanced by a supergene?Recommended by Chris Jiggins based on reviews by Christelle Fraïsse and 2 anonymous reviewers
The butterfly species Heliconius numata has a remarkable wing pattern polymorphism, with multiple pattern morphs all controlled by a single genetic locus, which harbours multiple inversions. Each morph is a near-perfect mimic of a species in the fairly distantly related genus of butterflies, Melinaea.
The article by Rodríguez de Cara et al (2023) argues that the balanced polymorphism at this single wing patterning locus actually has a major effect on genetic diversity across the whole genome. First, polymorphic populations within H. numata are more dioverse than those without polymorphism. Second, H. numata is more genetically diverse than other related species and finally reconstruction of historical demography suggests that there has been a recent increase in effective population size, putatively associated with the acquisition of the supergene polymorphism. The supergene itself generates disassortative mating, such that morphs prefer to mate with others dissimilar to themselves - in this way it is similar to mechanisms for preventing inbreeding such as self-incompatibility loci in plants. This provides a potential mechanism whereby non-random mating patterns could increase effective population size. The authors also explore this mechanism using forward simulations, and show that mating patterns at a single locus can influence linked genetic diversity over a large scale.
Overall, this is an intriguing study, which suggests a far more widespread genetic impact of a single locus than might be expected. There are interesting parallels with mechanisms of inbreeding prevention in plants, such as the Pin/Thrum polymorphism in Primula, which also rely on mating patterns determined by a single locus but presumably also influence genetic diversity genome-wide by promoting outbreeding.
Rodríguez de Cara MÁ, Jay P, Rougemont Q, Chouteau M, Whibley A, Huber B, Piron-Prunier F, Ramos RR, Freitas AVL, Salazar C, Silva-Brandão KL, Torres TT, Joron M (2023) Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow. bioRxiv, 2021.09.29.462348, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.09.29.462348
|Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow in a butterfly||María Ángeles Rodríguez de Cara, Paul Jay, Quentin Rougemont, Mathieu Chouteau, Annabel Whibley, Barbara Huber, Florence Piron-Prunier, Renato Rogner Ramos, André V. L. Freitas, Camilo Salazar, Karina Lucas Silva-Brandão, Tatiana Texeira Torres, M...||<p style="text-align: justify;">Selection shapes genetic diversity around target mutations, yet little is known about how selection on specific loci affects the genetic trajectories of populations, including their genomewide patterns of diversity ...||Evolutionary Ecology, Genome Evolution, Hybridization / Introgression, Population Genetics / Genomics||Chris Jiggins||2021-10-13 17:54:33||View|
24 Mar 2023
Domestication of different varieties in the cheese-making fungus Geotrichum candidumBastien Bennetot, Jean-Philippe Vernadet, Vincent Perkins, Sophie Hautefeuille, Ricardo C. Rodríguez de la Vega, Samuel O’Donnell, Alodie Snirc, Cécile Grondin, Marie-Hélène Lessard, Anne-Claire Peron, Steve Labrie, Sophie Landaud, Tatiana Giraud, Jeanne Ropars https://doi.org/10.1101/2022.05.17.492043
Diverse outcomes in cheese fungi domesticationRecommended by Christelle Fraïsse based on reviews by Delphine Sicard and 1 anonymous reviewer
Domestication is a complex process that imprints the demography and the genomes of domesticated populations, enforcing strong selective pressures on traits favourable to humans, e.g. for food production . Domestication has been quite intensely studied in plants and animals, but less so in micro-organisms such as fungi, despite their assets (e.g. their small genomes and tractability in the lab). This elegant study by Bennetot and collaborators  on the cheese-making fungus Geotrichum candidum adds to the mounting body of studies in the genomics of fungi, proving they are excellent models in evolutionary biology for studying adaptation and drift in eukaryotes .
Bennetot et al. newly showed with whole genome sequences that all G. candidum strains isolated from cheese form a monophyletic clade subdivided into three genetically differentiated populations with several admixed strains, while the wild strains sampled from diverse geographic locations form a sister clade. This suggests the wild progenitor was not sampled in the present study and calls for future exciting work on the domestication history of the G. candidum fungus. The authors scanned the genomes for footprints of adaptation to the cheese environment and identified promising candidates, such as a gene involved in iron uptake (this element is limiting in cheese). Their functional genome analysis also provides evidence for higher contents of transposable elements in cheese-making strains, likely due to relaxed selection during the domestication process.
This paper is particularly impressive in that the authors complemented the population genomic approach with the phenotypic characterization of the strains and tested their ability to outcompete common fungal food spoilers. The authors convincingly showed that cheese-making strains display phenotypic differences relative to wild relatives for multiple traits such as slower growth, lower proteolysis activity and a greater amount of volatiles attractive to consumers, these phenotypes being beneficial for cheese making.
Finally, this work is particularly inspiring because it thoroughly discusses convergent evolution during domestication in different cheese-associated fungi. Indeed, studying populations experiencing similar environmental pressures is fundamental to understanding whether evolution is repeatable . For instance, all three cheese populations of G. candidum exhibit a lower genetic diversity than wild populations. However, only one population displays a stronger domestication syndrome, resembling the Penicillium camemberti situation . Furthermore, different cheese-making practices may have led to varying situations with clonal lineages in non-Roquefort P. roqueforti and P. camemberti [5, 6], while the cheese-making G. candidum populations still harbour some diversity. In a nutshell, Bennetot's study makes an important contribution to evolutionary biology and highlights the value of diversifying our model organisms toward under-represented clades.
 Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418: 700–707. https://doi.org/10.1038/nature01019
 Bennetot B, Vernadet J-P, Perkins V, Hautefeuille S, Rodríguez de la Vega RC, O’Donnell S, Snirc A, Grondin C, Lessard M-H, Peron A-C, Labrie S, Landaud S, Giraud T, Ropars J (2023) Domestication of different varieties in the cheese-making fungus Geotrichum candidum. bioRxiv, 2022.05.17.492043, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.05.17.492043
 Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, Rodríguez de la Vega RC, Branco S, Giraud T (2014) Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol. Ecol. 23: 753–773. https://doi.org/10.1111/mec.12631
 Bolnick DI, Barrett RD, Oke KB, Rennison DJ, Stuart YE (2018) (Non)Parallel evolution. Ann. Rev. Ecol. Evol. Syst. 49: 303–330. https://doi.org/10.1146/annurev-ecolsys-110617-062240
 Ropars J, Didiot E, Rodríguez de la Vega RC, Bennetot B, Coton M, Poirier E, Coton E, Snirc A, Le Prieur S, Giraud T (2020) Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties. Current Biol. 30: 4441–4453.e4. https://doi.org/10.1016/j.cub.2020.08.082
 Dumas, E, Feurtey, A, Rodríguez de la Vega, RC, Le Prieur S, Snirc A, Coton M, Thierry A, Coton E, Le Piver M, Roueyre D, Ropars J, Branca A, Giraud T (2020) Independent domestication events in the blue-cheese fungus Penicillium roqueforti. Mol Ecol. 29: 2639–2660. https://doi.org/10.1111/mec.15359
|Domestication of different varieties in the cheese-making fungus *Geotrichum candidum*||Bastien Bennetot, Jean-Philippe Vernadet, Vincent Perkins, Sophie Hautefeuille, Ricardo C. Rodríguez de la Vega, Samuel O’Donnell, Alodie Snirc, Cécile Grondin, Marie-Hélène Lessard, Anne-Claire Peron, Steve Labrie, Sophie Landaud, Tatiana Giraud,...||<p>Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. <em>Geotrichum candidum...||Adaptation, Genome Evolution, Population Genetics / Genomics||Christelle Fraïsse||2022-08-12 20:50:42||View|
Michael David Pirie
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