Highly regulated growth and development of the Ediacara macrofossil Dickinsonia costata

The Ediacara Biota represents the oldest fossil evidence for the appearance of animals but linking these taxa to specific clades has proved challenging. Dickinsonia is an abundant, apparently bilaterally symmetrical Ediacara fossil with uncertain affinities. We identified and measured key morphological features of over 900 specimens of Dickinsonia costata from the Ediacara Member, South Australia to characterize patterns in growth and morphology. Here we show that development in Dickinsonia costata was surprisingly highly regulated to maintain an ovoid shape via terminal addition and the predictable expansion of modules. This result, along with other characters found in Dickinsonia suggests that it does not belong within known animal groups, but that it utilized some of the developmental gene networks of bilaterians, a result predicted by gene sequencing of basal metazoans but previously unidentified in the fossil record. Dickinsonia thus represents an extinct clade located between sponges and the last common ancestor of Protostomes and Deuterostomes, and likely belongs within the Eumetazoa.

[1]  R. Kristensen,et al.  Spiralian Phylogeny Informs the Evolution of Microscopic Lineages , 2017, Current Biology.

[2]  S. Jensen,et al.  The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution , 2017, Biological reviews of the Cambridge Philosophical Society.

[3]  F. Ronquist,et al.  Xenacoelomorpha is the sister group to Nephrozoa , 2016, Nature.

[4]  M. Droser,et al.  EXCEPTIONAL PRESERVATION OF SOFT-BODIED EDIACARA BIOTA PROMOTED BY SILICA-RICH OCEANS , 2016 .

[5]  H. Philippe,et al.  Genomic data do not support comb jellies as the sister group to all other animals , 2015, Proceedings of the National Academy of Sciences.

[6]  D. Jacobs,et al.  Ancestral state reconstruction of ontogeny supports a bilaterian affinity for Dickinsonia , 2015, Evolution & development.

[7]  J. Dzik,et al.  Taphonomy of the Ediacaran Podolimirus and associated dipleurozoans from the Vendian of Ukraine , 2015 .

[8]  M. Droser,et al.  Dickinsonia liftoff: Evidence of current derived morphologies , 2015 .

[9]  M. Droser,et al.  The advent of animals: The view from the Ediacaran , 2015, Proceedings of the National Academy of Sciences.

[10]  K. Halanych.  The ctenophore lineage is older than sponges? That cannot be right! Or can it? , 2015, Journal of Experimental Biology.

[11]  Andrew Meade,et al.  Detecting Regular Sound Changes in Linguistics as Events of Concerted Evolution , 2015, Current Biology.

[12]  D. Erwin,et al.  Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record , 2015 .

[13]  S. Morris,et al.  Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan , 2014 .

[14]  Jennifer F. Hoyal Cuthill,et al.  Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan , 2014, Proceedings of the National Academy of Sciences.

[15]  Anne Weigert,et al.  Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. , 2014, Molecular biology and evolution.

[16]  M. Droser,et al.  A New Enigmatic, Tubular Organism from the Ediacara Member, Rawnsley Quartzite, South Australia , 2014 .

[17]  N. Patel,et al.  What is a segment? , 2013, EvoDevo.

[18]  M. Droser,et al.  How well do fossil assemblages of the Ediacara Biota tell time , 2013 .

[19]  D. Erwin,et al.  The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat? , 2013 .

[20]  K. Peterson,et al.  The identification of microRNAs in calcisponges: independent evolution of microRNAs in basal metazoans. , 2013, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[21]  Victor A Albert,et al.  The unique pseudanthium of Actinodium (Myrtaceae) - morphological reinvestigation and possible regulation by CYCLOIDEA-like genes , 2013, EvoDevo.

[22]  G. Hunt,et al.  DEVELOPMENTAL TRAIT EVOLUTION IN TRILOBITES , 2012, Evolution; international journal of organic evolution.

[23]  D. Erwin,et al.  The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals , 2011, Science.

[24]  J. Vinther,et al.  A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes , 2010, Evolution & development.

[25]  A. Ivantsov.  New reconstruction of Kimberella, problematic Vendian metazoan , 2009 .

[26]  D. Erwin.  Early origin of the bilaterian developmental toolkit , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  S. Xiao,et al.  On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. , 2009, Trends in ecology & evolution.

[28]  J. Antcliffe,et al.  Dickinsonia from Ediacara: A new look at morphology and body construction , 2008 .

[29]  O. Voigt,et al.  Field biology of placozoans (Trichoplax): distribution, diversity, biotic interactions. , 2007, Integrative and comparative biology.

[30]  G. Retallack.  Growth, decay and burial compaction of Dickinsonia, an iconic Ediacaran fossil , 2007 .

[31]  A. Ivantsov.  Small Vendian transversely Articulated fossils , 2007 .

[32]  J. Antcliffe,et al.  Charnia and sea pens are poles apart , 2007, Journal of the Geological Society.

[33]  J. Reitner,et al.  A Fresh Look at Dickinsonia: Removing It from Vendobionta , 2006 .

[34]  R. Jenner,et al.  When molecules and morphology clash: reconciling conflicting phylogenies of the Metazoa by considering secondary character loss , 2004, Evolution & development.

[35]  A. Dorresteijn,et al.  The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[36]  Y. Maruyama.  Occurrence in the Field of a Long-Term, Year-Round, Stable Population of Placozoans , 2004, The Biological Bulletin.

[37]  A. Minelli,et al.  Exploring Developmental Modes in a Fossil Arthropod: Growth and Trunk Segmentation of the Trilobite Aulacopleura konincki , 2003, The American Naturalist.

[38]  A. Seilacher,et al.  Ediacaran biota: The dawn of animal life in the shadow of giant protists , 2003 .

[39]  M. Fedonkin.  The origin of the Metazoa in the light of the Proterozoic fossil record , 2003 .

[40]  J. Dzik.  Anatomical Information Content in the Ediacaran Fossils and Their Possible Zoological Affinities1 , 2003, Integrative and comparative biology.

[41]  J. Dzik,et al.  Internal anatomy of a new Precambrian dickinsoniid dipleurozoan from northern Russia , 2002 .

[42]  Eric H Davidson,et al.  The last common bilaterian ancestor. , 2002, Development.

[43]  B. Schierwater,et al.  The evolution of the placozoa: A new morphological model , 2002 .

[44]  O. Giere,et al.  Taxonomy and new bacterial symbioses of gutless marine Tubificidae (Annelida, Oligochaeta) from the Island of Elba (Italy) , 2002 .

[45]  J. Gehling.  Microbial mats in terminal Proterozoic siliciclastics; Ediacaran death masks , 1999 .

[46]  A. Seilacher.  Vendobionta and Psammocorallia: lost constructions of Precambrian evolution , 1992, Journal of the Geological Society.

[47]  C. Klingenberg,et al.  Dyar's rule and multivariate allometric growth in nine species of waterstriders (Heteroptera: Gerridae) , 1992 .

[48]  V. B. Pearse.  Growth and Behavior of Trichoplax adhaerens: First Record of the Phylum Placozoa in Hawaii , 1989 .

[49]  B. Runnegar.  Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit , 1982 .

[50]  M. Wade.  Dickinsonia: polychaete worms from the late Precambrian Ediacara fauna, South Australia , 1972 .

[51]  M. Glaessner,et al.  The Late Precambrian fossils from Ediacara, South Australia , 1966 .

[52]  C. Reg.  Early Cambrian jellyfishes of Ediacara, South Australia and Mount John, Kimberley District, Western Australia , 1949 .