The Origin of Animal Body Plans: a View from Fossil Evidence and the Regulatory Genome Douglas H
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The Architecture of Cell Differentiation in Choanoflagellates And
bioRxiv preprint doi: https://doi.org/10.1101/452185; this version posted October 29, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The architecture of cell differentiation in choanoflagellates 2 and sponge choanocytes 3 Davis Laundon1,2,6, Ben Larson3, Kent McDonald3, Nicole King3,4 and Pawel 4 Burkhardt1,5* 5 1 Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, 6 Plymouth, PL1 2PB, United Kingdom 7 2 Plymouth University, Drake Circus, Plymouth, PL4 8AA, United Kingdom 8 3 Department of Molecular and Cell Biology, University of California, Berkeley, USA 9 4 Howard Hughes Medical Institute 10 5 Sars International Centre for Molecular Marine Biology, University of Bergen, 11 Thormohlensgate 55, 5020 Bergen, Norway 12 6 Current Affiliation: University of East Anglia, Norwich, NR4 7TJ, United Kingdom 13 14 *Correspondence [email protected] 15 16 17 18 19 20 21 22 23 24 25 bioRxiv preprint doi: https://doi.org/10.1101/452185; this version posted October 29, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 26 SUMMARY 27 Collar cells are ancient animal cell types which are conserved across the animal 28 kingdom [1] and their closest relatives, the choanoflagellates [2]. -
[3 TD$DIFF]Interdisciplinary Team Science in Cell Biology
TICB 1268 No. of Pages 3 Scientific Life Cell biology, beginning largely as micro- detailed physical–chemical mechanisms Interdisciplinary[3_TD$IF] scopic observations, followed[1_TD$IF]the molec- [7]. The data required for these models ular biology revolution, which viewed are now in sight. New gene editing meth- Team Science in genes, cells, and the machinery that ods are providing endogenous expression underlies their activities as molecular sys- of tagged and mutant cells [8], and new Cell Biology tems that could be fully characterized and live-cell imaging methods are promising Rick Horwitz1,* understood using methods of genetics biochemistry in living cells, measuring con- and biochemistry. Viewing the cell as a centrations, dynamics, equilibria, and complex, dynamic molecular composite organization [9]. Similarly, super-resolution The cell is complex. With its multi- brought insights from chemistry and phys- microscopy and cryoEM tomography, tude of components, spatial– ics to bear on biological problems. Just as which allow structure determination and [6_TD$IF] temporal character, and gene the molecular genetic era was codified by organization in situ [3,4], imaging mass expression diversity, it is challeng- the publication of Watson's book, Molec- spectrometry [10], and single-cell and ing to comprehend the cell as an ular Biology of the Gene [1], two decades spatially-resolved genomic approaches integrated system and to develop later[8_TD$IF]the Molecular Biology of the Cell by [11–13], among other image-based tech- models that predict its behaviors. I Alberts, et al. [2] served a similar purpose nologies, all point to a new golden era of suggest an approach to address for cell biology. -
Assembly of the Cnidarian Camera-Type Eye from Vertebrate-Like Components
Assembly of the cnidarian camera-type eye from vertebrate-like components Zbynek Kozmik*†, Jana Ruzickova*‡, Kristyna Jonasova*‡, Yoshifumi Matsumoto§, Pavel Vopalensky*, Iryna Kozmikova*, Hynek Strnad*, Shoji Kawamura§, Joram Piatigorsky†¶, Vaclav Paces*, and Cestmir Vlcek*† *Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Videnska 1083, 142 20 Prague 4, Czech Republic; §Graduate School of Frontier Sciences, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan; and ¶National Eye Institute, National Institutes of Health, Bethesda, MD 20892-3655 Edited by Eviatar Nevo, University of Haifa, Haifa, Israel, and approved April 11, 2008 (received for review January 14, 2008) Animal eyes are morphologically diverse. Their assembly, however, containing Tripedalia eyes have sophisticated visual optics as do always relies on the same basic principle, i.e., photoreceptors advanced bilaterian phyla (11). located in the vicinity of dark shielding pigment. Cnidaria as the In the present work, we characterize genes required for the likely sister group to the Bilateria are the earliest branching phylum assembly of camera-type eyes in Tripedalia. We show that the with a well developed visual system. Here, we show that camera- genetic building blocks typical of vertebrate eyes, namely ciliary type eyes of the cubozoan jellyfish, Tripedalia cystophora, use opsin and the melanogenic pathway, are used by the cubozoan genetic building blocks typical of vertebrate eyes, namely, a ciliary eyes. Although our findings of unsuspected parallelism are phototransduction cascade and melanogenic pathway. Our find- consistent with either an independent origin or common ances- ings indicative of parallelism provide an insight into eye evolution. try of cubozoan and vertebrate eyes, we believe the present data Combined, the available data favor the possibility that vertebrate favor the former alternative. -
1 Eric Davidson and Deep Time Douglas H. Erwin Department Of
Eric Davidson and Deep Time Douglas H. Erwin Department of Paleobiology, MRC-121 National Museum of Natural History Washington, DC 20013-7012 E-mail: [email protected] Abstract Eric Davidson had a deep and abiding interest in the role developmental mechanisms played in the generating evolutionary patterns documented in deep time, from the origin of the euechinoids to the processes responsible for the morphological architectures of major animal clades. Although not an evolutionary biologist, Davidson’s interests long preceded the current excitement over comparative evolutionary developmental biology. Here I discuss three aspects at the intersection between his research and evolutionary patterns in deep time: First, understanding the mechanisms of body plan formation, particularly those associated with the early diversification of major metazoan clades. Second, a critique of early claims about ancestral metazoans based on the discoveries of highly conserved genes across bilaterian animals. Third, Davidson’s own involvement in paleontology through a collaborative study of the fossil embryos from the Ediacaran Doushantuo Formation in south China. Keywords Eric Davidson – Evolution – Gene regulatory networks – Bodyplan – Cambrian Radiation – Echinoderms 1 Introduction Eric Davidson was a developmental biologist, not an evolutionary biologist or paleobiologist. He was driven to understand the mechanisms of gene regulatory control and how they controlled development, but this focus was deeply embedded within concerns about the relationship between development and evolution. Questions about the origin of major metazoan architectures or body plans were central to Eric’s concerns since at least the late 1960s. His 1971 paper with Roy Britten includes a section on “The Evolutionary Growth of the Genome” illustrated with a figure depicting variations in genome size in major animal groups and a metazoan phylogeny (Britten and Davidson 1971). -
The Cambrian Explosion: a Big Bang in the Evolution of Animals
The Cambrian Explosion A Big Bang in the Evolution of Animals Very suddenly, and at about the same horizon the world over, life showed up in the rocks with a bang. For most of Earth’s early history, there simply was no fossil record. Only recently have we come to discover otherwise: Life is virtually as old as the planet itself, and even the most ancient sedimentary rocks have yielded fossilized remains of primitive forms of life. NILES ELDREDGE, LIFE PULSE, EPISODES FROM THE STORY OF THE FOSSIL RECORD The Cambrian Explosion: A Big Bang in the Evolution of Animals Our home planet coalesced into a sphere about four-and-a-half-billion years ago, acquired water and carbon about four billion years ago, and less than a billion years later, according to microscopic fossils, organic cells began to show up in that inert matter. Single-celled life had begun. Single cells dominated life on the planet for billions of years before multicellular animals appeared. Fossils from 635,000 million years ago reveal fats that today are only produced by sponges. These biomarkers may be the earliest evidence of multi-cellular animals. Soon after we can see the shadowy impressions of more complex fans and jellies and things with no names that show that animal life was in an experimental phase (called the Ediacran period). Then suddenly, in the relatively short span of about twenty million years (given the usual pace of geologic time), life exploded in a radiation of abundance and diversity that contained the body plans of almost all the animals we know today. -
Genomic Divergence and Brain Evolution: How Regulatory DNA Influences Development of the Cerebral Cortex
Prospects & Overviews Review essays Genomic divergence and brain evolution: How regulatory DNA influences development of the cerebral cortex Debra L. Silver1)2)3)4) The cerebral cortex controls our most distinguishing higher Introduction cognitive functions. Human-specific gene expression dif- ferences are abundant in the cerebral cortex, yet we have A large six-layered neocortex is a unique feature of only begun to understand how these variations impact brain mammalian brains. This specialized outer covering of the brain controls our higher cognitive functions including function. This review discusses the current evidence linking abstract thought and language, which together help uniquely non-coding regulatory DNA changes, including enhancers, define us as humans. Our distinguishing cognitive capacities with neocortical evolution. Functional interrogation using are specified within discrete cortical areas and are driven by animal models reveals converging roles for our genome in dynamic communication between neurons of the neocortex key aspects of cortical development including progenitor and other brain regions, as well as glial cell populations (including oligodendrocytes, microglia, and astrocytes). cell cycle and neuronal signaling. New technologies, Neurons are initially generated during human embryonic includingiPS cells and organoids, offerpotential alternatives and early fetal development, where they migrate to appropri- to modeling evolutionary modifications in a relevant species ate regions and begin establishing functional connections context. Several diseases rooted in the cerebral cortex during fetal and postnatal stages (Fig. 1). Disruptions to uniquely manifest in humans compared to other primates, cerebral cortex function arising during either development or thus highlighting the importance of understanding human adulthood, can result in neurodevelopmental and neurode- generative disorders. -
A Phylum-Wide Survey Reveals Multiple Independent Gains of Head Regeneration Ability in Nemertea
bioRxiv preprint doi: https://doi.org/10.1101/439497; this version posted October 11, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. A phylum-wide survey reveals multiple independent gains of head regeneration ability in Nemertea Eduardo E. Zattara1,2,5, Fernando A. Fernández-Álvarez3, Terra C. Hiebert4, Alexandra E. Bely2 and Jon L. Norenburg1 1 Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA 2 Department of Biology, University of Maryland, College Park, MD, USA 3 Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas, Barcelona, Spain 4 Institute of Ecology and Evolution, University of Oregon, Eugene, OR, USA 5 INIBIOMA, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Bariloche, RN, Argentina Corresponding author: E.E. Zattara, [email protected] Abstract Animals vary widely in their ability to regenerate, suggesting that regenerative abilities have a rich evolutionary history. However, our understanding of this history remains limited because regeneration ability has only been evaluated in a tiny fraction of species. Available comparative regeneration studies have identified losses of regenerative ability, yet clear documentation of gains is lacking. We surveyed regenerative ability in 34 species spanning the phylum Nemertea, assessing the ability to regenerate heads and tails either through our own experiments or from literature reports. Our sampling included representatives of the 10 most diverse families and all three orders comprising this phylum. -
Xenacoelomorpha's Significance for Understanding Bilaterian Evolution
Available online at www.sciencedirect.com ScienceDirect Xenacoelomorpha’s significance for understanding bilaterian evolution Andreas Hejnol and Kevin Pang The Xenacoelomorpha, with its phylogenetic position as sister biology models are the fruitfly Drosophila melanogaster and group of the Nephrozoa (Protostomia + Deuterostomia), plays the nematode Caenorhabditis elegans, in which basic prin- a key-role in understanding the evolution of bilaterian cell types ciples of developmental processes have been studied in and organ systems. Current studies of the morphological and great detail. It might be because the field of evolutionary developmental diversity of this group allow us to trace the developmental biology — EvoDevo — has its origin in evolution of different organ systems within the group and to developmental biology and not evolutionary biology that reconstruct characters of the most recent common ancestor of species under investigation are often called ‘model spe- Xenacoelomorpha. The disparity of the clade shows that there cies’. Criteria for selected representative species are cannot be a single xenacoelomorph ‘model’ species and primarily the ease of access to collected material and strategic sampling is essential for understanding the evolution their ability to be cultivated in the lab [1]. In some cases, of major traits. With this strategy, fundamental insights into the a supposedly larger number of ancestral characters or a evolution of molecular mechanisms and their role in shaping dominant role in ecosystems have played an additional animal organ systems can be expected in the near future. role in selecting model species. These arguments were Address used to attract sufficient funding for genome sequencing Sars International Centre for Marine Molecular Biology, University of and developmental studies that are cost-intensive inves- Bergen, Thormøhlensgate 55, 5008 Bergen, Norway tigations. -
A Unicellular Relative of Animals Generates a Layer of Polarized Cells
RESEARCH ARTICLE A unicellular relative of animals generates a layer of polarized cells by actomyosin- dependent cellularization Omaya Dudin1†*, Andrej Ondracka1†, Xavier Grau-Bove´ 1,2, Arthur AB Haraldsen3, Atsushi Toyoda4, Hiroshi Suga5, Jon Bra˚ te3, In˜ aki Ruiz-Trillo1,6,7* 1Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain; 2Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom; 3Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Oslo, Norway; 4Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Japan; 5Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Hiroshima, Japan; 6Departament de Gene`tica, Microbiologia i Estadı´stica, Universitat de Barcelona, Barcelona, Spain; 7ICREA, Barcelona, Spain Abstract In animals, cellularization of a coenocyte is a specialized form of cytokinesis that results in the formation of a polarized epithelium during early embryonic development. It is characterized by coordinated assembly of an actomyosin network, which drives inward membrane invaginations. However, whether coordinated cellularization driven by membrane invagination exists outside animals is not known. To that end, we investigate cellularization in the ichthyosporean Sphaeroforma arctica, a close unicellular relative of animals. We show that the process of cellularization involves coordinated inward plasma membrane invaginations dependent on an *For correspondence: actomyosin network and reveal the temporal order of its assembly. This leads to the formation of a [email protected] (OD); polarized layer of cells resembling an epithelium. We show that this stage is associated with tightly [email protected] (IR-T) regulated transcriptional activation of genes involved in cell adhesion. -
MOLECULAR CLOCKS Definition Introduction
MOLECULAR CLOCKS 583 Kishino, H., Thorne, J. L., and Bruno, W. J., 2001. Performance of Thorne, J. L., Kishino, H., and Painter, I. S., 1998. Estimating the a divergence time estimation method under a probabilistic model rate of evolution of the rate of molecular evolution. Molecular of rate evolution. Molecular Biology and Evolution, 18,352–361. Biology and Evolution, 15, 1647–1657. Kodandaramaiah, U., 2011. Tectonic calibrations in molecular dat- Warnock, R. C. M., Yang, Z., Donoghue, P. C. J., 2012. Exploring ing. Current Zoology, 57,116–124. uncertainty in the calibration of the molecular clock. Biology Marshall, C. R., 1997. Confidence intervals on stratigraphic ranges Letters, 8, 156–159. with nonrandom distributions of fossil horizons. Paleobiology, Wilkinson, R. D., Steiper, M. E., Soligo, C., Martin, R. D., Yang, Z., 23, 165–173. and Tavaré, S., 2011. Dating primate divergences through an Müller, J., and Reisz, R. R., 2005. Four well-constrained calibration integrated analysis of palaeontological and molecular data. Sys- points from the vertebrate fossil record for molecular clock esti- tematic Biology, 60,16–31. mates. Bioessays, 27, 1069–1075. Yang, Z., and Rannala, B., 2006. Bayesian estimation of species Parham, J. F., Donoghue, P. C. J., Bell, C. J., et al., 2012. Best practices divergence times under a molecular clock using multiple fossil for justifying fossil calibrations. Systematic Biology, 61,346–359. calibrations with soft bounds. Molecular Biology and Evolution, Peters, S. E., 2005. Geologic constraints on the macroevolutionary 23, 212–226. history of marine animals. Proceedings of the National Academy Zuckerkandl, E., and Pauling, L., 1962. Molecular disease, evolution of Sciences, 102, 12326–12331. -
Neoproterozoic Origin and Multiple Transitions to Macroscopic Growth in Green Seaweeds
bioRxiv preprint doi: https://doi.org/10.1101/668475; this version posted June 12, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds Andrea Del Cortonaa,b,c,d,1, Christopher J. Jacksone, François Bucchinib,c, Michiel Van Belb,c, Sofie D’hondta, Pavel Škaloudf, Charles F. Delwicheg, Andrew H. Knollh, John A. Raveni,j,k, Heroen Verbruggene, Klaas Vandepoeleb,c,d,1,2, Olivier De Clercka,1,2 Frederik Leliaerta,l,1,2 aDepartment of Biology, Phycology Research Group, Ghent University, Krijgslaan 281, 9000 Ghent, Belgium bDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium cVIB Center for Plant Systems Biology, Technologiepark 71, 9052 Zwijnaarde, Belgium dBioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium eSchool of Biosciences, University of Melbourne, Melbourne, Victoria, Australia fDepartment of Botany, Faculty of Science, Charles University, Benátská 2, CZ-12800 Prague 2, Czech Republic gDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742, USA hDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, 02138, USA. iDivision of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, DD2 5DA, UK jSchool of Biological Sciences, University of Western Australia (M048), 35 Stirling Highway, WA 6009, Australia kClimate Change Cluster, University of Technology, Ultimo, NSW 2006, Australia lMeise Botanic Garden, Nieuwelaan 38, 1860 Meise, Belgium 1To whom correspondence may be addressed. Email [email protected], [email protected], [email protected] or [email protected]. -
Oxygen Requirements of the Earliest Animals
Oxygen requirements of the earliest animals Daniel B. Millsa,1,2, Lewis M. Warda,b,1, CarriAyne Jonesa,c, Brittany Sweetena, Michael Fortha, Alexander H. Treuscha, and Donald E. Canfielda,2 aDepartment of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense M, Denmark; bDepartment of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125; and cDepartment of Microbiology and Immunology, University of British Columbia, Vancouver, BC, Canada V6T 1Z3 Contributed by Donald E. Canfield, January 14, 2014 (sent for review August 26, 2013) A rise in the oxygen content of the atmosphere and oceans is one 0.36% PAL, depending primarily on the organism’s length, of the most popular explanations for the relatively late and abrupt width, and possession of a vascular system (19). For example, appearance of animal life on Earth. In this scenario, Earth’s surface although an animal limited by pure diffusion for its internal environment failed to meet the high oxygen requirements of ani- oxygen supply is estimated to require 10% PAL to reach milli- mals up until the middle to late Neoproterozoic Era (850–542 mil- meter width (15), a diffusion-limited, 600-μm-long by 25-μm- lion years ago), when oxygen concentrations sufficiently rose to wide worm is estimated to require ∼0.36% PAL, with a 3-mm- permit the existence of animal life for the first time. Although long by 67-μm-wide worm with a circulatory system requiring multiple lines of geochemical evidence support an oxygenation only ∼0.14% PAL (19). Therefore, these estimates suggest that of the Ediacaran oceans (635–542 million years ago), roughly cor- early animals, in general, may have had relatively low oxygen responding with the first appearance of metazoans in the fossil requirements.