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Old Questions and Young Approaches to Animal Evolution pp 57–72Cite as

Comparative Embryology as a Way to Understand Evolution

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Abstract

In the nineteenth century and the first half of the twentieth century, comparative embryology has been indispensable for reconstructing the evolutionary history of Metazoa. The rise of molecular phylogeny and developmental genetics in the last decade of the twentieth century, however, has radically changed the role of comparative embryology in the study of animal evolution. Now, comparative embryology is no longer directly used in building phylogenetic trees, and the role of development in evolution has been recast as the mediator of morphological changes. The new technological developments have enabled investigators to study gene expression patterns and gene functions in embryonic development of many different animal species. By comparing developmental data from different species and reconstructing how developmental mechanisms evolved along the phylogenetic tree, it is now possible to imagine how animal body plans originated and evolved. Therefore, although the role of comparative embryology in evolution research has changed a lot in the past 50 years, it continues to be the forefront of Metazoan evolution research in the twenty-first century.

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References

  • Abzhanov A, Extavour CG, Groover A, Hodges SA, Hoekstra HE, Kramer EM, Monteiro A (2008) Are we there yet? Tracking the development of new model systems. Trends Genet 24:353–360

    Article  CAS  PubMed  Google Scholar 

  • Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud’homme B, de Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Nat Acad Sci U S A 97:4453–4456

    Article  CAS  Google Scholar 

  • Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garet JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  CAS  PubMed  Google Scholar 

  • Alwes F, Scholtz G (2014) The early development of the onychopod cladoceran Bythotrephes longimanus (Crustacea, Branchiopoda). Front Zool 11:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson DT (1969) On the embryology of the cirripede crustaceans Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of crustacean phylogenetic relationships. Philos Trans R Soc Lond B Biol Sci 256:183–235

    Article  Google Scholar 

  • Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon, Oxford

    Google Scholar 

  • Ankeny RA (2001) The natural history of Caenorhabditis elegans research. Nat Rev Genet 2:474–479

    Article  CAS  PubMed  Google Scholar 

  • Backfisch B, Kozin VV, Kirchmaier S, Tessmar-Raible K, Raible F (2014) Tools for gene-regulatory analyses in the marine annelid Platynereis dumerilii. PLoS One 9:e93076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baker MW, Macagno ER (2000) RNAi of the receptor tyrosine phosphatase HmLAR2 in a single cell of an intact leech embryo leads to growth-cone collapse. Curr Biol 7:1071–1074

    Article  Google Scholar 

  • Bigelow MA (1902) The early development of Lepas: a study of cell-lineage and germ-layers. Bull Mus Comp Zool 40:61–144

    Google Scholar 

  • Bolker JA (1995) Model systems in developmental biology. BioEssays 17:451–455

    Article  CAS  PubMed  Google Scholar 

  • Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangement. Nature 376:163–165

    Article  CAS  PubMed  Google Scholar 

  • Cannon JT, Vellutini BC, Smith J, Ronquist F, Jondelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93

    Article  CAS  PubMed  Google Scholar 

  • Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376:479–485

    Article  CAS  PubMed  Google Scholar 

  • Chen J-N, Fishman MC (1996) Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 122:3809–3816

    CAS  PubMed  Google Scholar 

  • Conklin EG (1897) The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gasteropods. J Morphol 13:1–226

    Article  Google Scholar 

  • Cornwell W, Nakagawa S (2017) Phylogenetic comparative methods. Curr Biol 27:R333–R336

    Article  CAS  PubMed  Google Scholar 

  • Costello DP, Henley C (1976) Spiralian development: a perspective. Am Zool 16:277–291

    Article  Google Scholar 

  • Cuvier G (1817) Le Règne Animal Distribué d’après son Organisation, pour Servir de Base à l’Histoire Naturelle des Animaux et d’Introduction à l’Anatomie Comparée. chez Deterville, libraire, Paris

    Google Scholar 

  • Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London

    Google Scholar 

  • Delsman HC (1917) Die Embryonalentwicklung von Balanus balanoides Linn. Tijdschr Ned Dierk Ver 15:419–520

    Google Scholar 

  • De Robertis EM (2008) Evo-Devo: variations on ancestral themes. Cell 132:185–195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dunn CW et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  CAS  PubMed  Google Scholar 

  • Ekker SC, Larson JD (2001) Morphant technology in model developmental systems. Genesis 30:89–93

    Article  CAS  PubMed  Google Scholar 

  • Ferguson EL (1996) Conservation of dorsal-ventral patterning in arthropods and chordates. Curr Opin Genet Dev 6:424–431

    Article  CAS  PubMed  Google Scholar 

  • Freeman G, Lundelius JW (1992) Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J Evol Biol 5:205–247

    Article  Google Scholar 

  • Friedrich M, Tautz D (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165–167

    Article  CAS  PubMed  Google Scholar 

  • Gardiner EG (1895) Early development of Polychoerus caudatus, mark. J Morphol 11:155–176

    Article  Google Scholar 

  • Geoffroy Saint-Hilaire E, Hilaire É (1822) Philosophie anatomique: des monstruosités humaines. chez l’auteur, Paris

    Google Scholar 

  • Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801

    Article  CAS  PubMed  Google Scholar 

  • Gilles AF, Averof M (2014) Functional genetics for all: engineered nucleases, CRISPR and the gene editing revolution. EvoDevo 5:43

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • González-Estévez C, Momose T, Gehring WJ, Saló E (2003) Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proc Nat Acad Sci U S A 100:14046–14051

    Article  CAS  Google Scholar 

  • Grunwald DJ, Eisen JS (2002) Headwaters of the zebrafish - emergence of a new model vertebrate. Nat Rev Genet 3:717–724

    Article  CAS  PubMed  Google Scholar 

  • Gurdon JB (1992) The generation of diversity and pattern in animal development. Cell 68:185–199

    Article  CAS  PubMed  Google Scholar 

  • Gurdon JB, Elsdale TR, Fischberg M (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182:64–65

    Article  CAS  PubMed  Google Scholar 

  • Halanych KM, Bacheller JD, Aguinaldo AMA, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643

    Article  CAS  PubMed  Google Scholar 

  • Halder G, Callaerts P, Gehring WJ (1995) New perspectives on eye evolution. Curr Opin Genet Dev 5:602–609

    Article  CAS  PubMed  Google Scholar 

  • Hall BK (1999) Evolutionary developmental biology, 2nd edn. Kluwer Academic, Dordrecht

    Book  Google Scholar 

  • Harland RM, Grainger RM (2011) Xenopus research: metamorphosed by genetics and genomics. Trends Genet 27:507–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hejnol A, Schnabel R (2005) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361

    Article  CAS  PubMed  Google Scholar 

  • Hejnol A, Schnabel R, Scholtz G (2006) A 4D-microscopic analysis of the germ band in the isopod crustacean Porcellio scaber (Malacostraca, Peracarida) - developmental and phylogenetic implications. Dev Genes Evol 216:755–767

    Article  PubMed  Google Scholar 

  • Henry JQ (2014) Spiralian model systems. Int J Dev Biol 58:389–401

    Article  PubMed  Google Scholar 

  • Henry JJ, Raff RA (1990) Evolutionary change in the process of dorsoventral axis determination in the direct developing sea urchin, Heliocidaris erythrogramma. Dev Biol 141:55–69

    Article  CAS  PubMed  Google Scholar 

  • Henry JJ, Wray GA, Raff RA (1990) The dorsoventral axis is specified prior to first cleavage in the direct developing sea urchin Heliocidaris erythrogramma. Development 110:875–884

    CAS  PubMed  Google Scholar 

  • Henry JQ, Martindale MQ, Boyer BC (2000) The unique developmental program of the acoel flatworm, Neochildia fusca. Dev Biol 220:285–295

    Article  CAS  PubMed  Google Scholar 

  • Jenner RA, Wills MA (2007) The choice of model organisms in evo-devo. Nat Rev Genet 8:311–314

    Article  CAS  PubMed  Google Scholar 

  • Jennings HS (1896) The early development of Asplanchna herrickii de Guerne. A contribution to developmental mechanics. Bull Mus Comp Zool 30:1–117

    Google Scholar 

  • Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK (2008) Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:1065–1069

    Article  CAS  PubMed  Google Scholar 

  • Kishi K, Onuma TA, Nishida H (2014) Long-distance cell migration during larval development in the appendicularian, Oikopleura dioica. Dev Biol 395:299–306

    Article  CAS  PubMed  Google Scholar 

  • Klann M, Scholtz G (2014) Early embryonic development of the freshwater shrimp Caridina multidentata (Crustacea, Decapoda, Atyidae). Zoomorphology 133:295–306

    Article  Google Scholar 

  • Kohler RE (1993) Drosophila: a life in the laboratory. J Hist Biol 26:281–310

    Article  CAS  PubMed  Google Scholar 

  • Kong J, Lasko P (2012) Translational control in cellular and developmental processes. Nat Rev Genet 13:383–394

    Article  CAS  PubMed  Google Scholar 

  • Koopman P (2001) In situ hybridization to mRNA: from black art to guiding light. Int J Dev Biol 45:619–622

    CAS  PubMed  Google Scholar 

  • Korzh V, Grunwald D (2001) Nadine Dobrovolsakia-Zavadskaia and the dawn of developmental genetics. BioEssays 23:365–371

    Article  CAS  PubMed  Google Scholar 

  • Lambert JD (2010) Developmental patterns in spiralian embryos. Curr Biol 20:R72–R77

    Article  CAS  PubMed  Google Scholar 

  • Laumer CE et al (2015) Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol 25:2000–2006

    Article  CAS  PubMed  Google Scholar 

  • Lawrence PA (1992) The making of a Fly. Blackwell Science, Oxford

    Google Scholar 

  • Lillie FR (1895) The embryology of the Unionidae. A study in cell-lineage. J Morphol 10:1–100

    Article  Google Scholar 

  • Lillie FR (1898) Adaptation in cleavage. Biol Lect 1898:43–66

    Google Scholar 

  • Lohmann JU, Endl I, Bosch TCG (1999) Silencing of developmental genes in Hydra. Dev Biol 214:211–214

    Article  CAS  PubMed  Google Scholar 

  • Lyons DC, Perry KJ, Lesoway MP, Henry JQ (2012) Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development. EvoDevo 3:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Mead AD (1897) The early development of marine annelids. J Morphol 13:227–327

    Article  Google Scholar 

  • Newmark PA, Reddien PW, Cebrià F, Sánchez Alvarado A (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Nat Acad Sci U S A 100:11861–11865

    Article  CAS  Google Scholar 

  • Nielsen C (2004) Trochophora larvae: cell lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. J Exp Zool (Mol Dev Evol) 302B:35–68

    Article  Google Scholar 

  • Nielsen C (2005) Trochophora larvae: cell lineages, ciliary bands, and body regions. 2. Other groups and general discussion. J Exp Zool (Mol Dev Evol) 304B:401–447

    Article  Google Scholar 

  • Nishiyama A, Fujiwara S (2008) RNA interference by expressing short hairpin RNA in the Ciona intestinalis embryo. Dev Growth Diff 50:521–529

    Article  CAS  Google Scholar 

  • O’Meara BC (2012) Evolutionary inferences from phylogenies: a review of methods. Annu Rev Ecol Evol Syst 43:267–285

    Article  Google Scholar 

  • Panganiban G et al (1997) The origin and evolution of animal appendages. Proc Nat Acad Sci U S A 94:5162–5166

    Article  CAS  Google Scholar 

  • Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS (1989) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968

    Article  CAS  PubMed  Google Scholar 

  • Pavlopoulos A, Averof M (2005) Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. Proc Nat Acad Sci U S A 102:7888–7893

    Article  CAS  Google Scholar 

  • Pavlopoulos A, Berghammer AJ, Averof M, Klingler M (2004) Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 167:737–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raff RA, Love AC (2004) Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of Evo-devo. J Exp Zool (Mol Dev Evol) 302B:19–34

    Article  Google Scholar 

  • Ronquist F (2004) Bayesian inference of character evolution. Trends Ecol Evol 19:475–481

    Article  PubMed  Google Scholar 

  • Rouhana L et al (2013) RNA interference by feeding in vitro-synthesized double-stranded RNA to planarians: methodology and dynamics. Dev Dyn 242:718–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Trillo I, Riutort M, Littlewood DTJ, Herniou EA, Baguñà J (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283:1919–1923

    Article  CAS  PubMed  Google Scholar 

  • Sasakura Y, Oogai Y, Matsuoka T, Satoh N, Awazu S (2007) Transposon mediated transgenesis in a marine invertebrate chordate: Ciona intestinalis. Genome Biol 8:S3

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawyer RT (1984) Arthropodization in the Hirudinea: evidence for a phylogenetic link with insects and other Uniramia? Zool J Linnean Soc 80:303–322

    Article  Google Scholar 

  • Schnabel R, Hutter H, Moerman D, Schnabel H (1997) Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev Biol 184:234–265

    Article  CAS  PubMed  Google Scholar 

  • Stach T, Anselmi C (2015) High-precision morphology: bifocal 4D-microscopy enables the comparison of detailed cell lineages of two chordate species separated for more than 525 million years. BMC Biol 13:113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stach T, Winter J, Bouquet JM, Chourrout D, Schnabel R (2008) Embryology of a planktonic tunicate reveals traces of sessility. Proc Nat Acad Sci U S A 105:7229–7234

    Article  CAS  Google Scholar 

  • Tieg OW, Manton SM (1958) The evolution of the Arthropoda. Biol Rev 33:255–333

    Article  Google Scholar 

  • Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395:854

    Article  CAS  PubMed  Google Scholar 

  • Treadwell AL (1901) Cytogeny of Podarke obscura Verrill. J Morphol 17:399–487

    Article  Google Scholar 

  • Vellutini BC, Martín-Durán JM, Hejnol A (2017) Cleavage modification did not alter blastomere fates during bryozoan evolution. BMC Biol 15:33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wacker SA, Oswald F, Wiedenmann J, Knöchel W (2007) A green to red photoconvertible protein as an analyzing tool for early vertebrate development. Dev Dyn 236:473–480

    Article  CAS  PubMed  Google Scholar 

  • Wedeen CJ, Weisblat DA (1991) Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. Development 113:805–814

    CAS  PubMed  Google Scholar 

  • Weisblat DA, Sawyer RT, Stent GS (1978) Cell lineage analysis by intracellular injection of a tracer enzyme. Science 202:1295–1298

    Article  CAS  PubMed  Google Scholar 

  • Weisblat DA, Zackson SL, Blair SS, Young JD (1980) Cell lineage analysis by intracellular injection of fluorescent tracers. Science 209:1538–1541

    Article  CAS  PubMed  Google Scholar 

  • Willems M et al (2009) Embryonic origins of hull cells in the flatworm Macrostomum lignano through cell lineage analysis: developmental and phylogenetic implications. Dev Genes Evol 219:409–417

    Article  PubMed  Google Scholar 

  • Wilson EB (1892) A cell-lineage of Nereis. A contribution to the cytogeny of the annelid body. J Morphol 6:361–481

    Article  Google Scholar 

  • Wilson EB (1898a) Cell-lineage and ancestral reminiscence. Biol Lect 1898:21–42

    Google Scholar 

  • Wilson EB (1898b) Considerations on cell-lineage and ancestral reminiscence. Ann N Y Acad Sci 11:1–27

    Article  Google Scholar 

  • Winsor MP (1969) Barnacle larvae in the nineteenth century: a case study in taxonomic theory. J Hist Med Allied Sci 24:294–309

    Article  CAS  PubMed  Google Scholar 

  • Winsor MP (1976) Starfish, jellyfish, and the order of life. Yale University Press, New Haven, CT

    Google Scholar 

  • Wolff C, Scholtz G (2006) Cell lineage analysis of the mandibular segment of the amphipod Orchestia cavimana reveals that the crustacean paragnaths are sternal outgrowths and not limbs. Front Zool 3:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Wray GA, Raff RA (1989) Evolutionary modification of cell lineage in the direct-developing sea urchin Helioidaris erythrogramma. Dev Biol 132:458–470

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Life Science, National Taiwan University, Taipei, Taiwan

    Dian-Han Kuo

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  1. Dian-Han Kuo
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Correspondence to Dian-Han Kuo .

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  1. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    José M. Martín-Durán

  2. Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany

    Bruno C. Vellutini

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Kuo, DH. (2019). Comparative Embryology as a Way to Understand Evolution. In: Martín-Durán, J., Vellutini, B. (eds) Old Questions and Young Approaches to Animal Evolution. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-18202-1_4

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