scholarly journals Selection against expression noise explains the origin of the hourglass pattern of Evo-Devo

2019 ◽  
Author(s):  
Jialin Liu ◽  
Michael Frochaux ◽  
Vincent Gardeux ◽  
Bart Deplancke ◽  
Marc Robinson-Rechavi
Keyword(s):  
Regulatory Elements ◽  
Mutational Robustness ◽  
Expression Variability ◽  
Expression Noise ◽  
Environmental Perturbations ◽  
Phylotypic Stage ◽  
Robustness To Noise ◽  
Selection For ◽  
Hourglass Model ◽  
Evo Devo

The evolution of embryological development has long been characterized by deep conservation. Both morphological and transcriptomic surveys have proposed a “hourglass” model of Evo-Devo1,2. A stage in mid-embryonic development, the phylotypic stage, is highly conserved among species within the same phylum3–7. However, the reason for this phylotypic stage is still elusive. Here we hypothesize that the phylotypic stage might be characterized by selection for robustness to noise and environmental perturbations. This could lead to mutational robustness, thus evolutionary conservation of expression and the hourglass pattern. To test this, we quantified expression variability of single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that indeed expression variability is lower at extended germband, the phylotypic stage. We explain this pattern by stronger histone modification mediated transcriptional noise control at this stage. In addition, we find evidence that histone modifications can also contribute to mutational robustness in regulatory elements. Thus, the robustness to noise does indeed contributes to robustness of gene expression to genetic variations, and to the conserved phylotypic stage.

scholarly journals Inter-embryo gene expression variability recapitulates the hourglass pattern of evo-devo

BMC Biology ◽  
2020 ◽  
Vol 18 (1) ◽  
Author(s):  
Jialin Liu ◽  
Michael Frochaux ◽  
Vincent Gardeux ◽  
Bart Deplancke ◽  
Marc Robinson-Rechavi
Keyword(s):  
Gene Expression ◽  
Stochastic Variation ◽  
Expression Variability ◽  
Animal Development ◽  
Regulatory Architecture ◽  
Phylotypic Stage ◽  
Gene Regulatory ◽  
Evo Devo ◽  
Late Stages ◽  
Selection Of

Abstract Background The evolution of embryological development has long been characterized by deep conservation. In animal development, the phylotypic stage in mid-embryogenesis is more conserved than either early or late stages among species within the same phylum. Hypotheses to explain this hourglass pattern have focused on purifying the selection of gene regulation. Here, we propose an alternative—genes are regulated in different ways at different stages and have different intrinsic capacities to respond to perturbations on gene expression. Results To eliminate the influence of natural selection, we quantified the expression variability of isogenetic single embryo transcriptomes throughout fly Drosophila melanogaster embryogenesis. We found that the expression variability is lower at the phylotypic stage, supporting that the underlying regulatory architecture in this stage is more robust to stochastic variation on gene expression. We present evidence that the phylotypic stage is also robust to genetic variations on gene expression. Moreover, chromatin regulation appears to play a key role in the variation and evolution of gene expression. Conclusions We suggest that a phylum-level pattern of embryonic conservation can be explained by the intrinsic difference of gene regulatory mechanisms in different stages.

scholarly journals Higher-fitness yeast genotypes are less robust to deleterious mutations

Science ◽  
2019 ◽  
Vol 366 (6464) ◽  
pp. 490-493 ◽  
Author(s):  
Milo S. Johnson ◽  
Alena Martsul ◽  
Sergey Kryazhimskiy ◽  
Michael M. Desai
Keyword(s):  
Second Order ◽  
Order Selection ◽  
Deleterious Mutations ◽  
Mutational Robustness ◽  
First Order ◽  
Fitness Effects ◽  
Yeast Strains ◽  
Selection For ◽  
Microbial Systems ◽  
Insertion Mutations

Natural selection drives populations toward higher fitness, but second-order selection for adaptability and mutational robustness can also influence evolution. In many microbial systems, diminishing-returns epistasis contributes to a tendency for more-fit genotypes to be less adaptable, but no analogous patterns for robustness are known. To understand how robustness varies across genotypes, we measure the fitness effects of hundreds of individual insertion mutations in a panel of yeast strains. We find that more-fit strains are less robust: They have distributions of fitness effects with lower mean and higher variance. These differences arise because many mutations have more strongly deleterious effects in faster-growing strains. This negative correlation between fitness and robustness implies that second-order selection for robustness will tend to conflict with first-order selection for fitness.

scholarly journals Gene Expression Does Not Support the Developmental Hourglass Model in Three Animals with Spiralian Development

2019 ◽  
Vol 36 (7) ◽  
pp. 1373-1383 ◽  
Author(s):  
Longjun Wu ◽  
Kailey E Ferger ◽  
J David Lambert
Keyword(s):  
Gene Expression ◽  
Large Fraction ◽  
Molecular Data ◽  
Development Stage ◽  
Data Sets ◽  
Rna Seq ◽  
Developmental Evolution ◽  
Phylotypic Stage ◽  
Hourglass Model ◽  
Almost All

Abstract It has been proposed that animals have a pattern of developmental evolution resembling an hourglass because the most conserved development stage—often called the phylotypic stage—is always in midembryonic development. Although the topic has been debated for decades, recent studies using molecular data such as RNA-seq gene expression data sets have largely supported the existence of periods of relative evolutionary conservation in middevelopment, consistent with the phylotypic stage and the hourglass concepts. However, so far this approach has only been applied to a limited number of taxa across the tree of life. Here, using established phylotranscriptomic approaches, we found a surprising reverse hourglass pattern in two molluscs and a polychaete annelid, representatives of the Spiralia, an understudied group that contains a large fraction of metazoan body plan diversity. These results suggest that spiralians have a divergent midembryonic stage, with more conserved early and late development, which is the inverse of the pattern seen in almost all other organisms where these phylotranscriptomic approaches have been reported. We discuss our findings in light of proposed reasons for the phylotypic stage and hourglass model in other systems.

scholarly journals Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion

2017 ◽  
Vol 372 (1713) ◽  
pp. 20150476 ◽  
Author(s):  
Thomas Cavalier-Smith
Keyword(s):  
Connective Tissue ◽  
Photosynthetic Bacteria ◽  
Cell Structure ◽  
Morphological Diversity ◽  
Cambrian Explosion ◽  
Feeding Modes ◽  
Selection For ◽  
Evo Devo ◽  
Gastraea Theory ◽  
Bacterial Food

Evolving multicellularity is easy, especially in phototrophs and osmotrophs whose multicells feed like unicells. Evolving animals was much harder and unique; probably only one pathway via benthic ‘zoophytes’ with pelagic ciliated larvae allowed trophic continuity from phagocytic protozoa to gut-endowed animals. Choanoflagellate protozoa produced sponges. Converting sponge flask cells mediating larval settling to synaptically controlled nematocysts arguably made Cnidaria. I replace Haeckel's gastraea theory by a sponge/coelenterate/bilaterian pathway: Placozoa, hydrozoan diploblasty and ctenophores were secondary; stem anthozoan developmental mutations arguably independently generated coelomate bilateria and ctenophores. I emphasize animal origin's conceptual aspects (selective, developmental) related to feeding modes, cell structure, phylogeny of related protozoa, sequence evidence, ecology and palaeontology. Epithelia and connective tissue could evolve only by compensating for dramatically lower feeding efficiency that differentiation into non-choanocytes entails. Consequentially, larger bodies enabled filtering more water for bacterial food and harbouring photosynthetic bacteria, together adding more food than cell differentiation sacrificed. A hypothetical presponge of sessile triploblastic sheets (connective tissue sandwiched between two choanocyte epithelia) evolved oogamy through selection for larger dispersive ciliated larvae to accelerate benthic trophic competence and overgrowing protozoan competitors. Extinct Vendozoa might be elaborations of this organismal grade with choanocyte-bearing epithelia, before poriferan water channels and cnidarian gut/nematocysts/synapses evolved. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

scholarly journals Selection for thermostability can lead to the emergence of mutational robustness in an RNA virus

2010 ◽  
Vol 23 (11) ◽  
pp. 2453-2460 ◽  
Author(s):  
P. DOMINGO-CALAP ◽  
M. PEREIRA-GÓMEZ ◽  
R. SANJUÁN
Keyword(s):  
Rna Virus ◽  
Mutational Robustness ◽  
Selection For

Selection for mutational robustness in finite populations

2006 ◽  
Vol 243 (2) ◽  
pp. 181-190 ◽  
Author(s):  
Robert Forster ◽  
Christoph Adami ◽  
Claus O. Wilke
Keyword(s):  
Finite Populations ◽  
Mutational Robustness ◽  
Selection For

scholarly journals DNA methylation in cockroaches is essential in early embryo development and reduces gene expression noise

2020 ◽  
Author(s):  
Alba Ventos-Alfonso ◽  
Guillem Ylla ◽  
Jose-Carlos Montañes ◽  
Xavier Belles
Keyword(s):  
Dna Methylation ◽  
Dna Methyltransferase ◽  
Early Embryo ◽  
Expression Change ◽  
Reduced Representation ◽  
Gene Expression Noise ◽  
Expression Variability ◽  
Functional Studies ◽  
Expression Noise ◽  
Hypermethylated Genes

AbstractThe influence of DNA methylation on gene behavior, and its consequent phenotypic effects appear to be very important, but the details are not well understood. Insects offer a diversity of DNA methylation modes, making them an excellent lineage for comparative analyses. However, functional studies have tended to focus on quite specialized holometabolan species, such as wasps, bees, beetles, and flies. Here we have studied DNA methylation in a hemimetabolan insect, the cockroach Blattella germanica, a model of early-branching insects. In this cockroach, one of the main genes responsible for DNA methylation, DNA methyltransferase 1 (DNMT1), is expressed in early embryogenesis. In our experiments, DNMT1 interference by RNAi reduces DNA methylation and impairs blastoderm formation. Using Reduced Representation Bisulfite Sequencing (RRBS) and transcriptomic analyses, we observed that hypermethylated genes are associated with metabolism and are highly expressed, whereas hypomethylated genes are related to signaling and have low expression levels. Moreover, the expression change in hypermethylated genes is greter than that in hypomethylated genes, whereas hypermethylated genes have less expression variability than hypomethylated genes. The latter observation has also been reported for humans and in Arabidopsis plants. A reduction in expression noise may therefore be one of the few universal effects of DNA methylation.

scholarly journals Higher fitness yeast genotypes are less robust to deleterious mutations

2019 ◽  
Author(s):  
Milo S. Johnson ◽  
Alena Martsul ◽  
Sergey Kryazhimskiy ◽  
Michael M. Desai
Keyword(s):  
Second Order ◽  
Order Selection ◽  
Deleterious Mutations ◽  
Mutational Robustness ◽  
First Order ◽  
Fitness Effects ◽  
Yeast Strains ◽  
Selection For ◽  
Microbial Systems ◽  
Insertion Mutations

AbstractNatural selection drives populations towards higher fitness, but second-order selection for adaptability and mutational robustness can also influence the dynamics of adaptation. In many microbial systems, diminishing returns epistasis contributes to a tendency for more-fit genotypes to be less adaptable, but no analogous patterns for robustness are known. To understand how robustness varies across genotypes, we measure the fitness effects of hundreds of individual insertion mutations in a panel of yeast strains. We find that more-fit strains are less robust: they have distributions of fitness effects (DFEs) with lower mean and higher variance. These shifts in the DFE arise because many mutations have more strongly deleterious effects in faster-growing strains. This negative correlation between fitness and robustness implies that second-order selection for robustness will tend to conflict with first-order selection for fitness.

scholarly journals Selection enhances protein evolvability by increasing mutational robustness and foldability

Science ◽  
2020 ◽  
Vol 370 (6521) ◽  
pp. eabb5962
Author(s):  
Jia Zheng ◽  
Ning Guo ◽  
Andreas Wagner
Keyword(s):  
Natural Selection ◽  
Fluorescent Protein ◽  
Yellow Fluorescent Protein ◽  
Deleterious Mutations ◽  
Green Fluorescence ◽  
Weak Selection ◽  
Mutational Robustness ◽  
Evolutionary Success ◽  
Selection For ◽  
Underlying Mechanisms

Natural selection can promote or hinder a population’s evolvability—the ability to evolve new and adaptive phenotypes—but the underlying mechanisms are poorly understood. To examine how the strength of selection affects evolvability, we subjected populations of yellow fluorescent protein to directed evolution under different selection regimes and then evolved them toward the new phenotype of green fluorescence. Populations under strong selection for the yellow phenotype evolved the green phenotype most rapidly. They did so by accumulating mutations that increase both robustness to mutations and foldability. Under weak selection, neofunctionalizing mutations rose to higher frequency at first, but more frequent deleterious mutations undermined their eventual success. Our experiments show how selection can enhance evolvability by enhancing robustness and create the conditions necessary for evolutionary success.

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