High expression of new genes in trochophore enlightening the ontogeny and evolution of trochozoans

Animals with trochophore larvae belong to Trochozoa, one of the main branches of Bilateria. In addition to exhibiting spiral cleavage and early cell fate determination, trochozoans typically undergo indirect development, which contributes to the most unique characteristics of their ontogeny. The indirect development of trochozoans has provoked discussion regarding the origin and evolution of marine larvae and is interesting from the perspective of phylogeny-ontogeny correspondence. While these phylo-onto correlations have an hourglass shape in Deuterostomia, Ecdysozoa, plants and even fungi, they have seldom been studied in Trochozoa, and even Lophotrochozoa. Here, we compared the ontogenetic transcriptomes of the Pacific oyster, Crassostrea gigas (Bivalvia, Mollusca), the Pacific abalone, Haliotis discus hannai (Gastropoda, Mollusca), and the sand worm Perinereis aibuhitensis (Polychaeta, Annelida) using several complementary phylotranscriptomic methods to examine their evolutionary trajectories. The results revealed the late trochophore stage as the phylotypic phase. However, this basic pattern is accompanied with increased use of new genes in the trochophore stages which marks specific adaptations of the larval body plans.

[1]  M. Hadfield,et al.  Why and how marine-invertebrate larvae metamorphose so fast. , 2000, Seminars in cell & developmental biology.

[2]  M. Robinson,et al.  A scaling normalization method for differential expression analysis of RNA-seq data , 2010, Genome Biology.

[3]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[4]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[5]  D. Tautz,et al.  A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns , 2010, Nature.

[6]  C. Nielsen Trochophora larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[7]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[8]  Jack D. Cohen Development of the zootype , 1993, Nature.

[9]  R. R. Strathmann,et al.  Plasticity of hatching and the duration of planktonic development in marine invertebrates. , 2011, Integrative and comparative biology.

[10]  Brian K. Hall,et al.  Keywords and Concepts in Evolutionary Developmental Biology , 2006 .

[11]  D. Tautz,et al.  The evolutionary origin of orphan genes , 2011, Nature Reviews Genetics.

[12]  L. Duret,et al.  Comparative population genomics in animals uncovers the determinants of genetic diversity , 2014, Nature.

[13]  J. Hui,et al.  A "developmental hourglass" in fungi. , 2015, Molecular biology and evolution.

[14]  Ximing Guo,et al.  Inbreeding Depression and Maternal Effects on Early Performance of Pacific Abalone , 2005 .

[15]  M. Martindale,et al.  Homology of ciliary bands in Spiralian Trochophores. , 2007, Integrative and comparative biology.

[16]  M. Martindale,et al.  Cellular and molecular mechanisms of segmentation in annelids , 1996 .

[17]  Nicholas H. Putnam,et al.  Insights into bilaterian evolution from three spiralian genomes , 2012, Nature.

[18]  Kevin R. Thornton,et al.  The origin of new genes: glimpses from the young and old , 2003, Nature Reviews Genetics.

[19]  Diethard Tautz,et al.  Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa , 2010, BMC Biology.

[20]  Jianzhi Zhang,et al.  Phylostratigraphic Bias Creates Spurious Patterns of Genome Evolution. , 2016, Molecular biology and evolution.

[21]  R. Raff Origins of the other metazoan body plans: the evolution of larval forms , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  I. Grosse,et al.  A transcriptomic hourglass in plant embryogenesis , 2012, Nature.

[23]  P. Robinson,et al.  Whole-exome sequencing for finding de novo mutations in sporadic mental retardation , 2010, Genome Biology.

[24]  Li Li,et al.  Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative real-time PCR. , 2013, Fish & shellfish immunology.

[25]  Dave T. Gerrard,et al.  Gene expression divergence recapitulates the developmental hourglass model , 2010, Nature.

[26]  D. Duboule Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. , 1994, Development (Cambridge, England). Supplement.

[27]  Itai Yanai,et al.  Developmental milestones punctuate gene expression in the Caenorhabditis embryo. , 2012, Developmental cell.

[28]  Victoria Svinti,et al.  New approaches for unravelling reassortment pathways , 2013, BMC Evolutionary Biology.

[29]  Tomislav Domazet-Loso,et al.  A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. , 2007, Trends in genetics : TIG.

[30]  C. Dunn,et al.  Animal Evolution: Are Phyla Real? , 2016, Current Biology.

[31]  Julio A. Rozas Liras,et al.  DnaSP v 5 : a software for comprehensive analysis of DNA polymorphism data , 2009 .

[32]  Qiang Wang,et al.  The oyster genome reveals stress adaptation and complexity of shell formation , 2012, Nature.

[33]  C. Nielsen Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea? , 2013, BMC Evolutionary Biology.

[34]  I. Grosse,et al.  Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis , 2015, Molecular biology and evolution.

[35]  Innes C Cuthill,et al.  The influence of a hot environment on parental cooperation of a ground-nesting shorebird, the Kentish plover Charadrius alexandrinus , 2010, Frontiers in Zoology.

[36]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[37]  M. Long,et al.  New genes important for development , 2014, EMBO reports.

[38]  Leon Anavy,et al.  The mid-developmental transition and the evolution of animal body plans , 2016, Nature.

[39]  Trey Ideker,et al.  Cytoscape 2.8: new features for data integration and network visualization , 2010, Bioinform..

[40]  D. Zaykin,et al.  Optimally weighted Z‐test is a powerful method for combining probabilities in meta‐analysis , 2011, Journal of evolutionary biology.

[41]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[42]  Thorsten Henrich,et al.  The normal development of Platynereis dumerilii (Nereididae, Annelida) , 2010, Frontiers in Zoology.

[43]  C. Arenas-Mena Indirect development, transdifferentiation and the macroregulatory evolution of metazoans , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Naoki Irie,et al.  Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis , 2011, Nature communications.

[45]  G. Giribet,et al.  Animal Phylogeny and Its Evolutionary Implications , 2014 .

[46]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[47]  Pablo Librado,et al.  DnaSP v5: a software for comprehensive analysis of DNA polymorphism data , 2009, Bioinform..

[48]  I. Grosse,et al.  Capturing Evolutionary Signatures in Transcriptomes with myTAI , 2016, bioRxiv.

[49]  X. Fang,et al.  Identification of Conserved and Novel MicroRNAs in the Pacific Oyster Crassostrea gigas by Deep Sequencing , 2014, PloS one.

[50]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[51]  Jianzhi Zhang,et al.  Evaluating Phylostratigraphic Evidence for Widespread De Novo Gene Birth in Genome Evolution. , 2016, Molecular biology and evolution.

[52]  D. Tautz,et al.  No Evidence for Phylostratigraphic Bias Impacting Inferences on Patterns of Gene Emergence and Evolution , 2016, bioRxiv.

[53]  T. Seki Biological studies on the seed production of the northern Japanese abalone, Haliotis discus Hannai Ino , 1997 .

[54]  P. Holland,et al.  Reinforcing the Egg-Timer: Recruitment of Novel Lophotrochozoa Homeobox Genes to Early and Late Development in the Pacific Oyster , 2015, Genome biology and evolution.

[55]  L. Page Molluscan Larvae: Pelagic Juveniles or Slowly Metamorphosing Larvae? , 2009, The Biological Bulletin.