24 Oct 2022
Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscuraAndres Mesas, Luis E. Castaneda https://doi.org/10.1101/2022.02.03.479001
The other side of the evolution of heat tolerance: correlated responses in metabolism and life-history traitsRecommended by Inês Fragata and Pedro Simões based on reviews by Marija Savić Veselinović and 1 anonymous reviewer
Understanding how species respond to environmental changes is becoming increasingly important in order to predict the future of biodiversity and species distributions under current global warming conditions (Rezende 2020; Bennett et al 2021). Two key factors to take into account in these predictions are the tolerance of organisms to heat stress and subsequently how they adapt to increasingly warmer temperatures. Coupled with this, one important factor that is often overlooked when addressing the evolution of thermal tolerance, is the correlated responses in traits that are important to fitness, such as life histories, behavior and the underlying metabolic processes.
The rate and intensity of the thermal stress are expected to be major factors in shaping the evolution of heat tolerance and correlated responses in other traits. For instance, lower rates of thermal stress are predicted to select for individuals with a slower metabolism (Santos et al 2012), whereas low metabolism is expected to lead to a lower reproductive rate (Dammhahn et al 2018). To quantify the importance of the rate and intensity of thermal stress on the evolutionary response of heat tolerance and correlated response in behavior, Mesas et al (2021) performed experimental evolution in Drosophila subobscura using selective regimes with slow or fast ramping protocols. Whereas both regimes showed increased heat tolerance with similar evolutionary rates, the correlated responses in thermal performance curves for locomotor behavior differed between selection regimes. These findings suggest that thermal rate and intensity may shape the evolution of correlated responses in other traits, urging the need to understand possible correlated responses at relevant levels such as life history and metabolism.
In the present contribution, Mesas and Castañeda (2022) investigate whether the disparity in thermal performance curves observed in the previous experiment (Mesas et al 2021) could be explained by differences in metabolic energy production and consumption, and how this correlated with the reproductive output (fecundity and viability). Overall, the authors show some evidence for lowered enzyme activity and increased performance in life-history traits, particularly for the slow-ramping selected flies. Specifically, the authors observe a reduction in glucose metabolism and increased viability when evolving under slow ramping stress. Interestingly, both regimes show a general increase in fecundity, suggesting that adaptation to these higher temperatures is not costly (for reproduction) in the ancestral environment. The evidence for a somewhat lower metabolism in the slow-ramping lines suggests the evolution of a slow “pace of life”. The “pace of life” concept tries to bridge variation across several levels namely metabolism, physiology, behavior and life history, with low “pace of life” organisms presenting lower metabolic rates, later reproduction and higher longevity than fast “pace of life” organisms (Dammhahn et al 2018, Tuzun & Stocks 2022). As the authors state there is not a clear-cut association with the expectations of the pace of life hypothesis since there was evidence for increased reproductive output under both selection intensity regimes. This suggests that, given sufficient trait genetic variance, positively correlated responses may emerge during some stages of thermal evolution. As fecundity estimates in this study were focussed on early life, the possibility of a decrease in the cumulative reproductive output of the selected flies, even under benign conditions, cannot be excluded. This would help explain the apparent paradox of increased fecundity in selected lines. In this context, it would also be interesting to explore the variation in reproductive output at different temperatures, i.e to obtain thermal performance curves for life histories.
Mesas and Castañeda (2022) raise important questions to pursue in the future and contribute to the growing evidence that, in order to predict the distribution of ectothermic species under current global warming conditions, we need to expand beyond determining the physiological thermal limits of each organism (Parratt et al 2021). Ultimately, integrating metabolic, life-history and behavioral changes during evolution under different thermal stresses within a coherent framework is key to developing better predictions of temperature effects on natural populations.
Bennett, J.M., Sunday, J., Calosi, P. et al. The evolution of critical thermal limits of life on Earth. Nat Commun 12, 1198 (2021). https://doi.org/10.1038/s41467-021-21263-8
Dammhahn, M., Dingemanse, N.J., Niemelä, P.T. et al. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72, 62 (2018). https://doi.org/10.1007/s00265-018-2473-y
Mesas, A, Jaramillo, A, Castañeda, LE. Experimental evolution on heat tolerance and thermal performance curves under contrasting thermal selection in Drosophila subobscura. J Evol Biol 34, 767– 778 (2021). https://doi.org/10.1111/jeb.13777
Parratt, S.R., Walsh, B.S., Metelmann, S. et al. Temperatures that sterilize males better match global species distributions than lethal temperatures. Nat. Clim. Chang. 11, 481–484 (2021). https://doi.org/10.1038/s41558-021-01047-0
Santos, M, Castañeda, LE, Rezende, EL Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits? Ecology and evolution, 2(11), 2866-2880 (2012). https://doi.org/10.1002/ece3.385
Tüzün, N, Stoks, R. A fast pace-of-life is traded off against a high thermal performance. Proceedings of the Royal Society B, 289(1972), 20212414 (2022). https://doi.org/10.1098/rspb.2021.2414
Rezende, EL, Bozinovic, F, Szilágyi, A, Santos, M. Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242-1245 (2020). https://doi.org/10.1126/science.aba9287
|Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura
|Andres Mesas, Luis E. Castaneda
|<p>Adaptations to warming conditions exhibited by ectotherms include increasing heat tolerance but also metabolic changes to reduce maintenance costs (metabolic depression), which can allow them to redistribute the energy surplus to biological fun...
|Adaptation, Evolutionary Ecology, Experimental Evolution, Life History
11 Mar 2020
Phylogenomic approaches reveal how a climatic inversion and glacial refugia shape patterns of diversity in an African rain forest tree speciesAndrew J. Helmstetter, Biowa E. N. Amoussou, Kevin Bethune, Narcisse G. Kandem, Romain Glèlè Kakaï, Bonaventure Sonké, Thomas L. P. Couvreur https://doi.org/10.1101/807727
Remarkable insights into processes shaping African tropical tree diversityRecommended by Michael Pirie based on reviews by Miguel de Navascués, Lars Chatrou and Oscar Vargas
Tropical biodiversity is immense, under enormous threat, and yet still poorly understood. Global climatic breakdown and habitat destruction are impacting on and removing this diversity before we can understand how the biota responds to such changes, or even fully appreciate what we are losing . This is particularly the case for woody shrubs and trees  and for the flora of tropical Africa .
Helmstetter et al.  have taken a significant step to improve our understanding of African tropical tree diversity in the context of past climatic change. They have done so by means of a remarkably in-depth analysis of one species of the tropical plant family Annonaceae: Annickia affinis . A. affinis shows a distribution pattern in Africa found in various plant (but interestingly not animal) groups: a discontinuity between north and south of the equator . There is no obvious physical barrier to cause this discontinuity, but it does correspond with present day distinct northern and southern rainy seasons. Various explanations have been proposed for this discontinuity, set out as hypotheses to be tested in this paper: climatic fluctuations resulting in changes in plant distributions in the Pleistocene, or differences in flowering times or in ecological niche between northerly and southerly populations. These explanations are not mutually exclusive, but they can be tested using phylogenetic inference – if you can sample variable enough sequence data from enough individuals – complemented with analysis of ecological niches and traits.
Using targeted sequence capture, the authors amassed a dataset representing 351 nuclear markers for 112 individuals of A. affinis. This dataset is impressive for a number of reasons: First, sampling such a species across such a wide range in tropical Africa presents numerous challenges of itself. Second, the technical achievement of using this still relatively new sequencing technique with a custom set of baits designed specifically for this plant family  is also considerable. The result is a volume of data that just a few years ago would not have been feasible to collect, and which now offers the possibility to meaningfully analyse DNA sequence variation within a species across numerous independent loci of the nuclear genome. This is the future of our research field, and the authors have ably demonstrated some of its possibilities.
Using this data, they performed on the one hand different population genetic clustering approaches, and on the other, different phylogenetic inference methods. I would draw attention to their use and comparison of coalescence and network-based approaches, which can account for the differences between gene trees that might be expected between populations of a single species. The results revealed four clades and a consistent sequence of divergences between them. The authors inferred past shifts in geographic range (using a continuous state phylogeographic model), depicting a biogeographic scenario involving a dispersal north over the north/south discontinuity; and demographic history, inferring in some (but not all) lineages increases in effective population size around the time of the last glacial maximum, suggestive of expansion from refugia. Using georeferenced specimen data, they compared ecological niches between populations, discovering that overlap was indeed smallest comparing north to south. Just the phenology results were effectively inconclusive: far better data on flowering times is needed than can currently be harvested from digitised herbarium specimens.
Overall, the results add to the body of evidence for the impact of Pleistocene climatic changes on population structure, and for niche differences contributing to the present day north/south discontinuity. However, they also paint a complex picture of idiosyncratic lineage-specific responses, even within a single species. With the increasing accessibility of the techniques used here we can look forward to more such detailed analyses of independent clades necessary to test and to expand on these conclusions, better to understand the nature of our tropical plant diversity while there is still opportunity to preserve it for future generations.
 Mace, G. M., Gittleman, J. L., and Purvis, A. (2003). Preserving the Tree of Life. Science, 300(5626), 1707–1709. doi: 10.1126/science.1085510
|Phylogenomic approaches reveal how a climatic inversion and glacial refugia shape patterns of diversity in an African rain forest tree species
|Andrew J. Helmstetter, Biowa E. N. Amoussou, Kevin Bethune, Narcisse G. Kandem, Romain Glèlè Kakaï, Bonaventure Sonké, Thomas L. P. Couvreur
|<p>The world’s second largest expanse of tropical rain forest is in Central Africa and it harbours enormous species diversity. Population genetic studies have consistently revealed significant structure across central African rain forest plants, i...
|Evolutionary Dynamics, Phylogeography & Biogeography
03 Oct 2018
Range size dynamics can explain why evolutionarily age and diversification rate correlate with contemporary extinction risk in plantsAndrew J. Tanentzap, Javier Igea, Matthew G. Johnston, Matthew J. Larcombe https://doi.org/10.1101/152215
Are both very young and the very old plant lineages at heightened risk of extinction?Recommended by Arne Mooers based on reviews by Dan Greenberg and 1 anonymous reviewer
Human economic activity is responsible for the vast majority of ongoing extinction, but that does not mean lineages are being affected willy-nilly. For amphibians  and South African flowering plants , young species have a somewhat higher than expected chance of being threatened with extinction. In contrast, older Australian marsupial lineages seem to be more at risk . Both of the former studies suggested that situations leading to peripheral isolation might simultaneously increase ongoing speciation and current threat via small geographic range, while the authors of the latter study suggested that older species might have evolved increasingly narrow niches. Here, Andrew Tanentzap and colleagues  dig deeper into the putative links between species age, niche breadth and threat status. Across 500-some plant genera worldwide, they find that, indeed, ""younger"" species (i.e. from younger and faster-diversifying genera) were more likely to be listed as imperiled by the IUCN, consistent with patterns for amphibians and African plants. Given this, results from their finer-level analyses of conifers are initially bemusing: here, ""older"" (i.e., on longer terminal branches) species were at higher risk. This would make conifers more like Australian marsupials, with the rest of the plants being more like amphibians. However, here where the data were more finely grained, the authors detected a second interesting pattern: using an intriguing matched-pair design, they detect a signal of conifer species niches seemingly shrinking as a function of age. The authors interpret this as consistent with increasing specialization, or loss of ancestral warm wet habitat, over paleontological time. It is true that conifers in general are older than plants more generally, with some species on branches that extend back many 10s of millions of years, and so a general loss of suitable habitat makes some sense. If so, both the pattern for all plants (small initial ranges heightening extinction) and the pattern for conifers (eventual increasing specialization or habitat contraction heightening extinction) could occur, each on a different time scale. As a coda, the authors detected no effect of age on threat status in palms; however, this may be both because palms have already lost species to climate-change induced extinction, and because they are thought to speciate more via long-distance dispersal and adaptive divergence then via peripheral isolation.
 Greenberg, D. A., & Mooers, A. Ø. (2017). Linking speciation to extinction: Diversification raises contemporary extinction risk in amphibians. Evolution Letters, 1, 40–48. doi: 10.1002/evl3.4
|Range size dynamics can explain why evolutionarily age and diversification rate correlate with contemporary extinction risk in plants
|Andrew J. Tanentzap, Javier Igea, Matthew G. Johnston, Matthew J. Larcombe
|<p>Extinction threatens many species, yet few factors predict this risk across the plant Tree of Life (ToL). Taxon age is one factor that may associate with extinction if occupancy of geographic and adaptive zones varies with time, but evidence fo...
|Macroevolution, Phylogenetics / Phylogenomics, Phylogeography & Biogeography
08 Feb 2019
Genome plasticity in Papillomaviruses and de novo emergence of E5 oncogenesAnouk Willemsen, Marta Félez-Sánchez, and Ignacio G. Bravo https://doi.org/10.1101/337477
E5, the third oncogene of PapillomavirusRecommended by Hirohisa Kishino based on reviews by Leonardo de Oliveira Martins and 1 anonymous reviewer
Papillomaviruses (PVs) infect almost all mammals and possibly amniotes and bony fishes. While most of them have no significant effects on the hosts, some induce physical lesions. Phylogeny of PVs consists of a few crown groups , among which AlphaPVs that infect primates including human have been well studied. They are associated to largely different clinical manifestations: non-oncogenic PVs causing anogenital warts, oncogenic and non-oncogenic PVs causing mucosal lesions, and non-oncogenic PVs causing cutaneous warts.
 Bravo, I. G., & Alonso, Á. (2004). Mucosal human papillomaviruses encode four different E5 proteins whose chemistry and phylogeny correlate with malignant or benign growth. Journal of virology, 78, 13613-13626. doi: 10.1128/JVI.78.24.13613-13626.2004
|Genome plasticity in Papillomaviruses and de novo emergence of E5 oncogenes
|Anouk Willemsen, Marta Félez-Sánchez, and Ignacio G. Bravo
|<p>The clinical presentations of papillomavirus (PV) infections come in many different flavors. While most PVs are part of a healthy skin microbiota and are not associated to physical lesions, other PVs cause benign lesions, and only a handful of ...
|Genome Evolution, Molecular Evolution, Phylogenetics / Phylogenomics
06 Jun 2019
Multi-model inference of non-random mating from an information theoretic approachAntonio Carvajal-Rodríguez https://doi.org/10.1101/305730
Tell me who you mate with, I’ll tell you what’s going onRecommended by Sara Magalhaes and Alexandre Courtiol based on reviews by Alexandre Courtiol and 2 anonymous reviewers
The study of sexual selection goes as far as Darwin himself. Since then, elaborate theories concerning both intra- and inter-sexual sexual have been developed, and elegant experiments have been designed to test this body of theory. It may thus come as a surprise that the community is still debating on the correct way to measure simple components of sexual selection, such as the Bateman gradient (i.e., the covariance between the number of matings and the number of offspring)[1,2], or to quantify complex behaviours such as mate choice (the non-random choice of individuals with particular characters as mates)[3,4] and their consequences.
 Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2(3), 349-368. doi: 10.1038/hdy.1948.21
|Multi-model inference of non-random mating from an information theoretic approach
|<p>Non-random mating has a significant impact on the evolution of organisms. Here, I developed a modelling framework for discrete traits (with any number of phenotypes) to explore different models connecting the non-random mating causes (mate comp...
|Evolutionary Ecology, Evolutionary Theory, Sexual Selection
07 Nov 2019
New insights into the population genetics of partially clonal organisms: when seagrass data meet theoretical expectationsArnaud-Haond, Sophie, Stoeckel, Solenn, and Bailleul, Diane https://arxiv.org/abs/1902.10240v6
Inferring rates of clonal versus sexual reproduction from population genetics dataRecommended by Olivier J Hardy based on reviews by Ludwig TRIEST, Stacy Krueger-Hadfield and 1 anonymous reviewer
In partially clonal organisms, genetic markers are often used to characterize the genotypic diversity of populations and infer thereof the relative importance of clonal versus sexual reproduction. Most studies report a measure of genotypic diversity based on a ratio, R, of the number of distinct multilocus genotypes over the sample size, and qualitatively interpret high / low R as indicating the prevalence of sexual / clonal reproduction. However, a theoretical framework allowing to quantify the relative rates of clonal versus sexual reproduction from genotypic diversity is still lacking, except using temporal sampling. Moreover, R is intrinsically highly dependent on sample size and sample design, while alternative measures of genotypic diversity are more robust to sample size, like D*, which is equivalent to the Gini-Simpson diversity index applied to multilocus genotypes. Another potential indicator of reproductive strategies is the inbreeding coefficient, Fis, because population genetics theory predicts that clonal reproduction should lead to negative Fis, at least when the sexual reproduction component occurs through random mating. Taking advantage of this prediction, Arnaud-Haond et al.  reanalysed genetic data from 165 populations of four partially clonal seagrass species sampled in a standardized way. They found positive correlations between Fis and both R and D* within each species, reflecting variation in the relative rates of sexual versus clonal reproduction among populations. Moreover, the differences of mean genotypic diversity and Fis values among species were also consistent with their known differences in reproductive strategies. Arnaud-Haond et al.  also conclude that previous works based on the interpretation of R generally lead to underestimate the prevalence of clonality in seagrasses. Arnaud-Haond et al.  confirm experimentally that Fis merits to be interpreted more properly than usually done when inferring rates of clonal reproduction from population genetics data of species reproducing both sexually and clonally. An advantage of Fis is that it is much less affected by sample size than R, and thus should be more reliable when comparing studies differing in sample design. Hence, when the rate of clonal reproduction becomes significant, we expect Fis < 0 and D* < 1. I expect these two indicators of clonality to be complementary because they rely on different consequences of clonality on pattern of genetic variation. Nevertheless, both measures can be affected by other factors. For example, null alleles, selfing or biparental inbreeding can pull Fis upwards, potentially eliminating the signature of clonal reproduction. Similarly, D* (and other measures of genotypic diversity) can be low because the polymorphism of the genetic markers used is too limited or because sexual reproduction often occurs through selfing, eventually resulting in highly similar homozygous genotypes.
 Arnaud-Haond, S., Stoeckel, S., and Bailleul, D. (2019). New insights into the population genetics of partially clonal organisms: when seagrass data meet theoretical expectations. ArXiv:1902.10240 [q-Bio], v6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. Retrieved from http://arxiv.org/abs/1902.10240
|New insights into the population genetics of partially clonal organisms: when seagrass data meet theoretical expectations
|Arnaud-Haond, Sophie, Stoeckel, Solenn, and Bailleul, Diane
|<p>Seagrass meadows are among the most important coastal ecosystems, in terms of both spatial extent and ecosystem services, but they are also declining worldwide. Understanding the drivers of seagrass meadow dynamics is essential for designing so...
|Evolutionary Ecology, Population Genetics / Genomics, Reproduction and Sex
|Olivier J Hardy
31 Mar 2022
Gene network robustness as a multivariate characterArnaud Le Rouzic https://arxiv.org/abs/2101.01564
Genetic and environmental robustness are distinct yet correlated evolvable traits in a gene networkRecommended by Frédéric Guillaume based on reviews by Diogo Melo, Charles Mullon and Charles Rocabert
Organisms often show robustness to genetic or environmental perturbations. Whether these two components of robustness can evolve separately is the focus of the paper by Le Rouzic . Using theoretical analysis and individual-based computer simulations of a gene regulatory network model, he shows that multiple aspects of robustness can be investigated as a set of pleiotropically linked quantitative traits. While genetically correlated, various robustness components (e.g., mutational, developmental, homeostasis) of gene expression in the regulatory network evolved more or less independently from each other under directional selection. The quantitative approach of Le Rouzic could explain both how unselected robustness components can respond to selection on other components and why various robustness-related features seem to have their own evolutionary history. Moreover, he shows that all components were evolvable, but not all to the same extent. Robustness to environmental disturbances and gene expression stability showed the largest responses while increased robustness to genetic disturbances was slower. Interestingly, all components were positively correlated and remained so after selection for increased or decreased robustness.
This study is an important contribution to the discussion of the evolution of robustness in biological systems. While it has long been recognized that organisms possess the ability to buffer genetic and environmental perturbations to maintain homeostasis (e.g., canalization ), the genetic basis and evolutionary routes to robustness and canalization are still not well understood. Models of regulatory gene networks have often been used to address aspects of robustness evolution (e.g., ). Le Rouzic  used a gene regulatory network model derived from Wagner’s model . The model has as end product the expression level of a set of genes influenced by a set of regulatory elements (e.g., transcription factors). The level and stability of expression are a property of the regulatory interactions in the network.
Le Rouzic made an important contribution to the study of such gene regulation models by using a quantitative genetics approach to the evolution of robustness. He crafted a way to assess the mutational variability and selection response of the components of robustness he was interested in. Le Rouzic’s approach opens avenues to investigate further aspects of gene network evolutionary properties, for instance to understand the evolution of phenotypic plasticity.
Le Rouzic also discusses ways to measure his different robustness components in empirical studies. As the model is about gene expression levels at a set of protein-coding genes influenced by a set of regulatory elements, it naturally points to the possibility of using RNA sequencing to measure the variation of gene expression in know gene networks and assess their robustness. Robustness could then be studied as a multidimensional quantitative trait in an experimental setting.
 Le Rouzic, A (2022) Gene network robustness as a multivariate character. arXiv: 2101.01564, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://arxiv.org/abs/2101.01564
 Waddington CH (1942) Canalization of Development and the Inheritance of Acquired Characters. Nature, 150, 563–565. https://doi.org/10.1038/150563a0
 Draghi J, Whitlock M (2015) Robustness to noise in gene expression evolves despite epistatic constraints in a model of gene networks. Evolution, 69, 2345–2358. https://doi.org/10.1111/evo.12732
 Wagner A (1994) Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization. Proceedings of the National Academy of Sciences, 91, 4387–4391. https://doi.org/10.1073/pnas.91.10.4387
|Gene network robustness as a multivariate character
|Arnaud Le Rouzic
|<p style="text-align: justify;">Robustness to genetic or environmental disturbances is often considered as a key property of living systems. Yet, in spite of being discussed since the 1950s, how robustness emerges from the complexity of genetic ar...
|Bioinformatics & Computational Biology, Evolutionary Theory, Genotype-Phenotype, Quantitative Genetics
|Charles Mullon, Charles Rocabert, Diogo Melo
05 Feb 2021
Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and solitary pollinating beesArthur Weyna, Jonathan Romiguier https://doi.org/10.1101/2020.04.14.038893
Multi-gene and lineage comparative assessment of the strength of selection in HymenopteraRecommended by Bertanne Visser based on reviews by Michael Lattorff and 1 anonymous reviewer
Genetic variation is the raw material for selection to act upon and the amount of genetic variation present within a population is a pivotal determinant of a population’s evolutionary potential. A large effective population size, i.e., the ideal number of individuals experiencing the same amount of genetic drift and inbreeding as an actual population, Ne (Wright 1931, Crow 1954), thus increases the probability of long-term survival of a population. However, natural populations, as opposed to theoretical ones, rarely adhere to the requirements of an ideal panmictic population (Sjödin et al. 2005). A range of circumstances can reduce Ne, including the structuring of populations (through space and time, as well as age and developmental stages) and inbreeding (Charlesworth 2009). In mammals, species with a larger body mass (as a proxy for lower Ne) were found to have a higher rate of nonsynonymous nucleotide substitutions (that alter the amino acid sequence of a protein), as well as radical amino acid substitutions (altering the physicochemical properties of a protein) (Popadin et al. 2007). In general, low effective population sizes increase the chance of mutation accumulation and drift, while reducing the strength of selection (Sjödin et al. 2005).
Charlesworth, B. (2009). Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics, 10(3), 195-205. doi: https://doi.org/10.1038/nrg2526
|Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and solitary pollinating bees
|Arthur Weyna, Jonathan Romiguier
|<p>With one of the highest number of parasitic, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of lifestyles. At the population genetic level, such life-history strategies are expected to decrease e...
|Behavior & Social Evolution, Genome Evolution, Life History, Molecular Evolution, Population Genetics / Genomics
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
16 Dec 2016
Spatiotemporal microbial evolution on antibiotic landscapesBaym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R 10.1126/science.aag0822
A poster child for experimental evolutionRecommended by Daniel Rozen and Arjan de Visser
Evolution is usually studied via two distinct approaches: by inferring evolutionary processes from relatedness patterns among living species or by observing evolution in action in the laboratory or field. A recent study by Baym and colleagues in Science  has now combined these approaches by taking advantage of the pattern left behind by spatially evolving bacterial populations.
Evolution is often considered too slow to see, and can only be inferred by studying patterns of relatedness using phylogenetic trees. Increasingly, however, researchers are moving nature into the lab and watching as evolution unfolds under their noses. The field of experimental evolution follows evolutionary change in the laboratory over 10s to 1000s of generations, yielding insights into bacterial, viral, plant, or fly evolution (among many other species) that are simply not possible in the field. Yet, as powerful as experimental evolution is, it lacks a posterchild. There is no Galapagos finch radiation, nor a stunning series of cichlids to showcase to our students to pique their interests. Let’s face it, E. coli is no stickleback! And while practitioners of experimental evolution can explain the virtues of examining 60,000 generations of bacterial evolution in action, appreciating this nevertheless requires a level of insight and imagination that often eludes students, who need to see “it” to get it.
Enter MEGA, an idea and a film that could become the new face of experimental evolution. It replaces big numbers of generations or images of scientists, with an actual picture of the scientific result. MEGA, or Microbial Evolution and Growth Arena, is essentially an enormous petri dish and is the brainchild of Michael Baym, Tami Leiberman and their colleagues in Roy Kishony’s lab at Technion Israel Institute of Technology and Harvard Medical School. The idea of MEGA is to allow bacteria to swim over a spatially defined landscape while adapting to the local conditions, in this case antibiotics. When bacteria are inoculated onto one end of the plate they consume resources while swarming forward from the plate edge. In a few days, the bacteria grow into an area with antibiotics to which they are susceptible. This stops growth until a mutation arises that permits the bacteria to jump this hurdle, after which growth proceeds until the next hurdle of a 10-fold higher antibiotic concentration, and so on. By this simple approach, Baym et al.  evolved E. coli that were nearly 105-fold more resistant to two different antibiotics in just over 10 days. In addition, they identified the mutations that were required for these changes, showed that mutations conferring smaller benefits were required before bacteria could evolve maximal resistance, observed changes to the mutation rate, and demonstrated the importance of spatial structure in constraining adaptation.
For one thing, the rate of resistance evolution is impressive, and also quite scary given the mounting threat of antibiotic-resistant pathogens. However, MEGA also offers a uniquely visual insight into evolutionary change. By taking successive images of the MEGA plate, the group was able to watch the bacteria move, get trapped because of their susceptibility to the antibiotic, and then get past these traps as new mutations emerged that increased resistance. Each transition showcases evolution in real time. In addition, by leaving a spatial pattern of evolutionary steps behind, the MEGA plate offers unique opportunities to thoroughly investigate these steps when the experiment is finished. For instance, subsequent steps in mutational pathways can be characterized, but also their effects on fitness can be quantified in situ by measuring changes in survival and reproduction. This new method is undoubtedly a boon to the field of experimental evolution and offers endless opportunities for experimental elaboration. Perhaps of equal importance, MEGA is a tool that is portable to the classroom and to the public at large. Don’t believe in evolution? Watch this. You only have time for a short internship or lab practical? No problem. Don’t worry much about antibiotic resistance? Check this out. Like the best experimental tools, MEGA is simple but allows for complicated insights. And even if it is less charismatic than a finch, it still allows for the kinds of “gee-whiz” insights that will get students hooked on evolutionary biology.
 Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R. 2016. Spatiotemporal microbial evolution on antibiotic landscapes. Science 353:1147-1151. doi: 10.1126/science.aag0822
|Spatiotemporal microbial evolution on antibiotic landscapes
|Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R
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|Adaptation, Evolutionary Applications, Experimental Evolution
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