Cell and Tissue Research

, Volume 377, Issue 3, pp 445–458 | Cite as

Development and evolution of gut structures: from molecules to function

  • Rossella Annunziata
  • Carmen Andrikou
  • Margherita Perillo
  • Claudia Cuomo
  • Maria I. ArnoneEmail author


The emergence of a specialized system for food digestion and nutrient absorption was a crucial innovation for multicellular organisms. Digestive systems with different levels of complexity evolved in different animals, with the endoderm-derived one-way gut of most bilaterians to be the prevailing and more specialized form. While the molecular events regulating the early phases of embryonic tissue specification have been deeply investigated in animals occupying different phylogenetic positions, the mechanisms underlying gut patterning and gut-associated structures differentiation are still mostly obscure. In this review, we describe the main discoveries in gut and gut-associated structures development in echinoderm larvae (mainly for sea urchin and, when available, for sea star) and compare them with existing information in vertebrates. An impressive degree of conservation emerges when comparing the transcription factor toolkits recruited for gut cells and tissue differentiation in animals as diverse as echinoderms and vertebrates, thus suggesting that their function emerged in the deuterostome ancestor.


Echinoderm Gastrointestinal system Pancreas Sphincter Gene regulatory network 



This work was partially supported by the Marie Curie ITN EVONET (project 215781) to MIA (and fellowship to CA), fellowship of the SZN PhD program (to CC, MP and RA) and fellowships POR Campania FSE 2007–2013 Project MODO, Model Organism (to CA, MP and RA).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Al-Mahrouki AA, Youson JH (1999) Ultrastructure and immunocytochemistry of the islet organ of osteoglossomorpha (Teleostei). Gen Comp Endocrinol 116:409–421CrossRefGoogle Scholar
  2. Aloe L, Levi-Montalcini R (1979) Nerve growth factor-induced transformation of immature chromaffin cells in vivo into sympathetic neurons: effect of antiserum to nerve growth factor. Proc Natl Acad Sci U S A 76:1246–1250CrossRefGoogle Scholar
  3. Alpert S, Hanahan D, Teitelman G (1988) Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons. Cell 53:295–308CrossRefGoogle Scholar
  4. Andrikou C, Arnone MI (2015) Too many ways to make a muscle: evolution of GRNs governing myogenesis. Zool Anz 256:2–13Google Scholar
  5. Andrikou C, Iovene E, Rizzo F, Oliveri P, Arnone MI (2013) Myogenesis in the sea urchin embryo: the molecular fingerprint of the myoblast precursors. EvoDevo 4:33CrossRefGoogle Scholar
  6. Andrikou C, Pai CY, Su YH, Arnone MI (2015) Logics and properties of a genetic regulatory program that drives embryonic muscle development in an echinoderm. eLife 4:e07343Google Scholar
  7. Annunziata R, Arnone MI (2014) A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin. Development 141:2462–2472CrossRefGoogle Scholar
  8. Annunziata R, Martinez P, Arnone MI (2013) Intact cluster and chordate-like expression of ParaHox genes in a sea star. BMC Biol 11:68CrossRefGoogle Scholar
  9. Annunziata R, Perillo M, Andrikou C, Cole AG, Martinez P, Arnone MI (2014) Pattern and process during sea urchin gut morphogenesis: the regulatory landscape. Genesis 52:251–268CrossRefGoogle Scholar
  10. Arenas-Mena C, Cameron RA, Davidson EH (2006) Hindgut specification and cell-adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo. Develop Growth Differ 48:463–472CrossRefGoogle Scholar
  11. Arnone MI, Rizzo F, Annunciata R, Cameron RA, Peterson KJ, Martinez P (2006) Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: insights into the relationship between clustering and colinearity. Dev Biol 300:63–73Google Scholar
  12. Arnone M, Byrne M, Martínez P (2015) Echinodermata. In: Wanninger A (Ed) Evolutionary developmental biology of invertebrates 6: Deuterostomia. Springer-Verlag, Wien, pp 1-58Google Scholar
  13. Arntfield ME, van der Kooy D (2011) β-Cell evolution: how the pancreas borrowed from the brain. Bioessays 33:582–587CrossRefGoogle Scholar
  14. Ayanbule F, Belaguli NS, Berger DH (2011) GATA factors in gastrointestinal malignancy. World J Surg 35:1757–1765CrossRefGoogle Scholar
  15. Besnard V, Wert SE, Hull WM, Whitsett JA (2004) Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 5:193–208CrossRefGoogle Scholar
  16. Boyle MJ, Seaver EC (2010) Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). EvoDevo 1:2Google Scholar
  17. Boyle MJ, Yamaguchi E, Seaver EC (2014) Molecular conservation of metazoan gut formation: evidence from expression of endomesoderm genes in Capitella teleta (Annelida). EvoDevo 5:39Google Scholar
  18. Burke R (1981) Structure of the digestive tract of the pluteus larva of Dendraster excentricus (Echinodermata: Echinoida). Zoomorphology 98:209–225CrossRefGoogle Scholar
  19. Burke RD, Alvarez CM (1988) Development of the esophageal muscles in embryos of the sea urchin Strongylocentrotus purpuratus. Cell Tissue Res 252:411–417Google Scholar
  20. Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T, Liang S, Mu X, Agca C, Klein WH, Brandhorst BP, Rowe M, Wilson K, Churcher AM, Taylor JS, Chen N, Murray G, Wang D, Mellott D, Olinski R, Hallböök F, Thorndyke MC (2006) A genomic view of the sea urchin nervous system. Dev Biol 300:434–460CrossRefGoogle Scholar
  21. Cameron RA, Davidson EH (1991) Cell type specification during sea urchin development. Trends Genet 7:212–218CrossRefGoogle Scholar
  22. Cary GA, Cameron RA, Hinman VF (2019) Genomic resources for the study of echinoderm development and evolution. Methods Cell Biol 151:65–88CrossRefGoogle Scholar
  23. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F (2004) Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci U S A 101:7641–7645CrossRefGoogle Scholar
  24. Chia F-S (1977) Scanning electron microscopic observations of the mesenchyme cells in the larvae of the starfish Pisaster ochraceus. Acta Zool 58:45–51Google Scholar
  25. Ciglar L, Furlong EE (2009) Conservation and divergence in developmental networks: a view from Drosophila myogenesis. Curr Opin Cell Biol 21:754–760CrossRefGoogle Scholar
  26. Cole AG, Rizzo F, Martinez P, Fernandez-Serra M, Arnone MI (2009) Two ParaHox genes, SpLox and SpCdx, interact to partition the posterior endoderm in the formation of a functional gut. Development 136:541–549CrossRefGoogle Scholar
  27. Crawford BJ, Chia FS (1978) Coelomic pouch formation in the starfish Pisaster ochraceus (Echinodermata: Asteroidea). J Morphol 157:99–119Google Scholar
  28. Crawford B, Martin C (1998) Ultrastructure and differentiation of the larval esophageal muscle cells of the starfish Pisaster ochraceus. J Morphol 237:1–18Google Scholar
  29. Croce JC, McClay DR (2010) Dynamics of Delta/notch signaling on endomesoderm segregation in the sea urchin embryo. Development 137:83–91CrossRefGoogle Scholar
  30. Croce J, Range R, Wu SY, Miranda E, Lhomond G, Peng JC, Lepage T, McClay DR (2011) Wnt6 activates endoderm in the sea urchin gene regulatory network. Development 138:3297–3306CrossRefGoogle Scholar
  31. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Rust AG, Pan Z, Schilstra MJ, Clarke PJ, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002) A genomic regulatory network for development. Science 295:1669–1678CrossRefGoogle Scholar
  32. Eberhard D (2013) Neuron and beta-cell evolution: learning about neurons is learning about beta-cells. Bioessays 35:584CrossRefGoogle Scholar
  33. Esni F, Ghosh B, Biankin AV, Lin JW, Albert MA, Yu X, MacDonald RJ, Civin CI, Real FX, Pack MA, Ball DW, Leach SD (2004) Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development 131:4213–4224CrossRefGoogle Scholar
  34. Falkmer S, Dafgård E, el-Salhy M, Engström W, Grimelius L, Zetterberg A (1985) Phylogenetical aspects on islet hormone families: a minireview with particular reference to insulin as a growth factor and to the phylogeny of PYY and NPY immunoreactive cells and nerves in the endocrine and exocrine pancreas. Peptides 6(Suppl 3):315–320CrossRefGoogle Scholar
  35. Forander P, Broberger C, Stromberg I (2001) Glial-cell-line-derived neurotrophic factor induces nerve fibre formation in primary cultures of adrenal chromaffin cells. Cell Tissue Res 305:43–51CrossRefGoogle Scholar
  36. Frobius AC, Seaver EC (2006) ParaHox gene expression in the polychaete annelid Capitella sp. I. Dev Genes Evol 216:81–88Google Scholar
  37. Gao N, White P, Kaestner KH (2009) Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev Cell 16:588–599CrossRefGoogle Scholar
  38. Garner S, Zysk I, Byrne G, Kramer M, Moller D, Taylor V, Burke RD (2016) Neurogenesis in sea urchin embryos and the diversity of deuterostome neurogenic mechanisms. Development 143:286–297CrossRefGoogle Scholar
  39. Gliznutsa LA, Dautov SS (2011) Cell differentiation during the larval development of the ophiuroid Amphipholis kochii Lütken, 1872 (Echinodermata: Ophiuroidea). Russ J Mar Biol 37:384–400Google Scholar
  40. Goldberg WM (2002) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34:246–261Google Scholar
  41. Gross JM, McClay DR (2001) The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev Biol 239:132–147Google Scholar
  42. Gustafson T, Wolpert L (1967) Cellular movement and contact in sea urchin morphogenesis. Biol Rev Camb Philos Soc 42:442–498CrossRefGoogle Scholar
  43. Hald J, Hjorth JP, German MS, Madsen OD, Serup P, Jensen J (2003) Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development. Dev Biol 260:426–437CrossRefGoogle Scholar
  44. Haumaitre C, Barbacci E, Jenny M, Ott MO, Gradwohl G, Cereghini S (2005) Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proc Natl Acad Sci U S A 102:1490–1495CrossRefGoogle Scholar
  45. He C, Han T, Liao X, Zhou Y, Wang X, Guan R, Tian T, Li Y, Bi C, Lu N, He Z, Hu B, Zhou Q, Hu Y, Lu Z, Chen J-Y (2018) hagocytic intracellular digestion in amphioxus (Branchiostoma). Proc Biol Sci 285Google Scholar
  46. Herrmann BG, Kispert A (1994) The T genes in embryogenesis. Trends Genet 10:280–286Google Scholar
  47. Hernandez-Samano AC, Guzman-Garcia X, Garcia-Barrientos R, Ascencio-Valle F, Sierra-Beltran A, Guerrero-Legarreta I (2017) Characterization of protease activity from the digestive tract and tentacles of Isostichopus fuscus sea cucumber. ISJ 14:282-294Google Scholar
  48. Hesselson D, Anderson RM, Stainier DY (2011) Suppression of Ptf1a activity induces acinar-to-endocrine conversion. Curr Biol 21:712–717CrossRefGoogle Scholar
  49. Hinman VF, Davidson EH (2007) Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci U S A 104:19404–19409CrossRefGoogle Scholar
  50. Hinman VF, Nguyen AT, Cameron RA, Davidson EH (2003) Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci U S A 100:13356–13361CrossRefGoogle Scholar
  51. Holland LZ (2000) Body-plan evolution in the Bilateria: early antero-posterior patterning and the deuterostome-protostome dichotomy. Curr Opin Genet Dev 10:434–442CrossRefGoogle Scholar
  52. Holland PW, Koschorz B, Holland LZ, Herrmann BG (1995) Conservation of Brachyury (T) genes in amphioxus and vertebrates: developmental and evolutionary implications. Development 121:4283–4291Google Scholar
  53. Hui JH, Raible F, Korchagina N, Dray N, Samain S, Magdelenat G, Jubin C, Segurens B, Balavoine G, Arendt D, Ferrier DE (2009) Features of the ancestral bilaterian inferred from Platynereis dumerilii ParaHox genes. BMC Biol 7:43Google Scholar
  54. Ishimoda-Takagi T, Chino I, Sato H (1984) Evidence for the involvement of muscle tropomyosin in the contractile elements of the coelom-esophagus complex in sea urchin embryos. Dev Biol 105:365–376CrossRefGoogle Scholar
  55. Kaneko H, Kawahara Y, Okamoto M, Dan-Sohkawa M (2009) Study on the nature of starfish larval muscle cells in vitro. Zool Sci 14: 287-296Google Scholar
  56. Krapp A, Knöfler M, Ledermann B, Bürki K, Berney C, Zoerkler N, Hagenbüchle O, Wellauer PK (1998) The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev 12:3752–3763CrossRefGoogle Scholar
  57. Kudtarkar P, Cameron RA (2017) Echinobase: an expanding resource for echinoderm genomic information. Database 2017:bax074Google Scholar
  58. Kulakova MA, Cook CE, Andreeva TF (2008) ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Dev Biol 8:61Google Scholar
  59. Kungurtzeva LA, Dautov SS (2001) Ultrastructure of the digestive tract in the ophiopluteus of Ophiura sarsi. Invertebr Reprod Dev 39:209–220Google Scholar
  60. Le Douarin NM (1988) On the origin of pancreatic endocrine cells. Cell 53:169–171CrossRefGoogle Scholar
  61. Lecroisey C, Le Pétillon Y, Escriva H, Lammert E, Laudet V (2015) Identification, evolution and expression of an insulin-like peptide in the cephalochordate Branchiostoma lanceolatum. PLoS One 10:e0119461Google Scholar
  62. Lee PY, Davidson EH (2004) Expression of Spgatae, the Strongylocentrotus purpuratus ortholog of vertebrate GATA4/5/6 factors. Gene Expr Patterns 5:161–165Google Scholar
  63. Lemaitre B, Miguel-Aliaga I (2013) The digestive tract of Drosophila melanogaster. Annu Rev Genet 47:377–404Google Scholar
  64. Lengyel JA, Iwaki DD (2002) It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev Biol 243:1–19CrossRefGoogle Scholar
  65. Lentz TL (1966) Intramitochondrial glycogen granules in digestive cells of Hydra. J Cell Biol 29:162–167CrossRefGoogle Scholar
  66. Lowe EK, Cuomo C, Arnone MI (2017) Omics approaches to study gene regulatory networks for development in echinoderms. Brief Funct Genomics 16:299–308CrossRefGoogle Scholar
  67. Malakhov V (1998) Embryological and histological peculiarities of the order Enoplida, a primitive group of nematodes. Russ J Nematol 6:41-46 Google Scholar
  68. Martin-Duran JM, Hejnol A (2015) The study of Priapulus caudatus reveals conserved molecular patterning underlying different gut morphogenesis in the Ecdysozoa. BMC Biol 13:29CrossRefGoogle Scholar
  69. Martin-Duran JM, Passamaneck YJ, Martindale MQ, Hejnol A (2016) The developmental basis for the recurrent evolution of deuterostomy and protostomy. Nat Ecol Evol 1:5CrossRefGoogle Scholar
  70. Masui T, Long Q, Beres TM, Magnuson MA, MacDonald RJ (2007) Early pancreatic development requires the vertebrate suppressor of hairless (RBPJ) in the PTF1 bHLH complex. Genes Dev 21:2629–2643CrossRefGoogle Scholar
  71. McEdward LR, Miner BG (2001) Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–1170CrossRefGoogle Scholar
  72. McGhee JD (2000) Homologous tails? Or tales of homology? BioEssays 22:781–785CrossRefGoogle Scholar
  73. McGhee JD (2013) The Caenorhabditis elegans intestine. Wiley Interdiscip Rev Dev Biol 2:347–367Google Scholar
  74. Monaghan AP, Kaestner KH, Grau E, Schutz G (1993) Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119:567–578Google Scholar
  75. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA (2003) Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A 100:14920–14925CrossRefGoogle Scholar
  76. Nezlin LP, Yushin VV (1994) The digestive tract of the echinopluteus of Echinocardium cordatum (Echinodermata, Echinoida): its ultrastructure and innervation. Can J Zool 72:2090–2099Google Scholar
  77. Nielsen C (2017) Evolution of deuterostomy and origin of the chordates. Biol Rev Camb Philos Soc 92:316–325Google Scholar
  78. Nielsen C (2019) Blastopore fate: amphistomy, protostomy or deuterostomy. In: eLS. John Wiley & Sons Ltd, Chichester. [DOI: 10.1002/9780470015902.a0027481]Google Scholar
  79. Nielsen C, Brunet T, Arendt D (2018) Evolution of the bilaterian mouth and anus. Nat Ecol Evol 2:1358–1376CrossRefGoogle Scholar
  80. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, Wright CV (1996) PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122:983–995Google Scholar
  81. Ogawa M, Ishikawa T, Irimajiri A (1984) Adrenal chromaffin cells form functional cholinergic synapses in culture. Nature 307:66–68CrossRefGoogle Scholar
  82. Olinski RP, Dahlberg C, Thorndyke M, Hallböök F (2006) Three insulin-relaxin-like genes in Ciona intestinalis. Peptides 27:2535–2546Google Scholar
  83. Oliveri P, Walton KD, Davidson EH, McClay DR (2006) Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133:4173–4181CrossRefGoogle Scholar
  84. Osborne PW, Benoit G, Laudet V, Schubert M, Ferrier DE (2009) Differential regulation of ParaHox genes by retinoic acid in the invertebrate chordate amphioxus (Branchiostoma floridae). Dev Biol 327:252–262Google Scholar
  85. Ostberg Y, Van Noorden S, Pearse AG, Thomas NW (1976) Cytochemical, immunofluorescence, and ultrastructural investigations on polypeptide hormone containing cells in the intestinal mucosa of a cyclostome, Myxine glutinosa. Gen Comp Endocrinol 28:213–227Google Scholar
  86. de Pablo F, Chambers SA, Ota A (1988) Insulin-related molecules and insulin effects in the sea urchin embryo. Dev Biol 130:304–310CrossRefGoogle Scholar
  87. Pearse AGE, Polak JM (1971) Neural crest origin of the endocrine polypeptide (APUD) cells of the gastrointestinal tract and pancreas. Gut 12:783–788CrossRefGoogle Scholar
  88. Perillo M, Arnone MI (2014) Characterization of insulin-like peptides (ILPs) in the sea urchin Strongylocentrotus purpuratus: insights on the evolution of the insulin family. Gen Comp Endocrinol 205:68–79Google Scholar
  89. Perillo M, Wang YJ, Leach SD, Arnone MI (2016) A pancreatic exocrine-like cell regulatory circuit operating in the upper stomach of the sea urchin Strongylocentrotus purpuratus larva. BMC Evol Biol 16:117CrossRefGoogle Scholar
  90. Perillo M, Paganos P, Mattiello T, Cocurullo M, Oliveri P, Arnone MI (2018) New neuronal subtypes with a “pre-pancreatic” signature in the sea urchin Stongylocentrotus purpuratus. Front Endocrinol (Lausanne) 9:650Google Scholar
  91. Peter IS, Davidson EH (2010) The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Dev Biol 340:188–199CrossRefGoogle Scholar
  92. Peterson KJ, Cameron RA, Tagawa K, Satoh N, Davidson EH (1999a) A comparative molecular approach to mesodermal patterning in basal deuterostomes: the expression pattern of Brachyury in the enteropneust hemichordate Ptychodera flava. Development 126:85Google Scholar
  93. Peterson KJ, Harada Y, Cameron RA, Davidson EH (1999b) Expression Pattern of Brachyury and Not in the Sea Urchin: Comparative Implications for the Origins of Mesoderm in the Basal Deuterostomes. Dev Biol  207:419–431Google Scholar
  94. Petrucco S, Wellauer PK, Hagenbüchle O (1990) The DNA-binding activity of transcription factor PTF1 parallels the synthesis of pancreas-specific mRNAs during mouse development. Mol Cell Biol 10:254–264CrossRefGoogle Scholar
  95. Rast JP, Cameron RA, Poustka AJ, Davidson EH (2002) Brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev Biol 246:191–208CrossRefGoogle Scholar
  96. Reece-Hoyes JS, Keenan ID, Isaacs HV (2002) Cloning and expression of the cdx family from the frog Xenopus tropicalis. Dev Dyn 223:134–140Google Scholar
  97. Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183:1–94CrossRefGoogle Scholar
  98. de Rosa R, Prud'homme B, Balavoine G (2005) Caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol Dev 7:574–587Google Scholar
  99. Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  100. Shashikant T, Khor JM, Ettensohn CA (2018) Global analysis of primary mesenchyme cell cis-regulatory modules by chromatin accessibility profiling. BMC Genomics 19:206CrossRefGoogle Scholar
  101. Shoguchi E, Satoh N, Maruyama YK (1999) Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech Dev 82:185–189Google Scholar
  102. Slack JM (1995) Developmental biology of the pancreas. Development 121:1569–1580Google Scholar
  103. Stainier DY (2002) A glimpse into the molecular entrails of endoderm formation. Genes Dev 16:893–907CrossRefGoogle Scholar
  104. Stern CD (2004) Gastrulation: from cells to embryo. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  105. Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, Habener JF (1997) Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 15:106–110CrossRefGoogle Scholar
  106. Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730CrossRefGoogle Scholar
  107. Sun J, Zhang L, Pan Y, Lin C, Wang F, Kan R, Yang H (2015) Feeding behavior and digestive physiology in sea cucumber Apostichopus japonicus. Physiol Behav 139:336–343Google Scholar
  108. Tagawa K, Humphreys T, Satoh N (1998) Novel pattern of Brachyury gene expression in hemichordate embryos. Mech Dev 75:139–143 Google Scholar
  109. Thor S, Ericson J, Brännström T, Edlund T (1991) The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7:881–889CrossRefGoogle Scholar
  110. Treadwell AL (1901) The cytogeny of Podarke obscura Verrill. J Morphol 17:399–486Google Scholar
  111. Trenzado CE, Hidalgo F, Villanueva D, Furné M, Díaz-Casado ME, Merino R, Sanz A (2012) Study of the enzymatic digestive profile in three species of Mediterranean sea urchins. Aquaculture 344-349:174–180CrossRefGoogle Scholar
  112. Vacquier VD (1971a) The appearance of -1,3-glucanohydrolase activity during the differentiation of the gut of sand dollar plutei. Dev Biol 26:1–10CrossRefGoogle Scholar
  113. Vacquier VD (1971b) The effects of glucose and lithium chloride on the appearance of -1,3-glucanohydrolase activity in sand dollar plutei. Dev Biol 26:11–16CrossRefGoogle Scholar
  114. Vacquier VD, Korn LJ, Epel D (1971) The appearance of -amylase activity during gut differentiation in sand dollar plutei. Dev Biol 26:393–399CrossRefGoogle Scholar
  115. Wang L, Hiebert SW (2001) TEL contacts multiple co-repressors and specifically associates with histone deacetylase-3. Oncogene 20:3716–3725CrossRefGoogle Scholar
  116. Wei Z, Angerer RC, Angerer LM (2011) Direct development of neurons within foregut endoderm of sea urchin embryos. Proc Natl Acad Sci U S A 108:9143–9147CrossRefGoogle Scholar
  117. Wessel GM, Zhang W, Klein WH (1990) Myosin heavy chain accumulates in dissimilar cell types of the macromere lineage in the sea urchin embryo. Dev Biol 140:447–454CrossRefGoogle Scholar
  118. Williams DC (1975) The occurrence and distribution of digestive enzymes in the pyloric caecum of the purple starfish Pisaster ochraceus. Comp Biochem Physiol A Comp Physiol 52:85–90Google Scholar
  119. Winter WP, Neurath H (1970) Purification and properties of a trypsin-like enzyme from the starfish Evasterias trochelii. Biochemistry 9:4673–4679Google Scholar
  120. Wood NJ, Mattiello T, Rowe ML, Ward L, Perillo M, Arnone MI, Elphick MR, Oliveri P (2018) Neuropeptidergic systems in pluteus larvae of the sea urchin Strongylocentrotus purpuratus: neurochemical complexity in a “simple” nervous system. Front Endocrinol (Lausanne) 9:628Google Scholar
  121. Wu Q, Brown MR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51:1–24CrossRefGoogle Scholar
  122. Wu LH, Lengyel JA (1998) Role of caudal in hindgut specification and gastrulation suggests homology between Drosophila amnioproctodeal invagination and vertebrate blastopore. Development 125:2433Google Scholar
  123. Yaguchi J, Yaguchi S (2019) Evolution of nitric oxide regulation of gut function. Proc Natl Acad Sci U S A 116:5607–5612CrossRefGoogle Scholar
  124. Youson JH, Al-Mahrouki AA (1999) Ontogenetic and phylogenetic development of the endocrine pancreas (islet organ) in fish. Gen Comp Endocrinol 116:303–335CrossRefGoogle Scholar
  125. Youson JH, Al-Mahrouki AA, Amemiya Y, Graham LC, Montpetit CJ, Irwin DM (2006) The fish endocrine pancreas: review, new data, and future research directions in ontogeny and phylogeny. Gen Comp Endocrinol 148:105–115CrossRefGoogle Scholar
  126. Yui R, Fujita T (1986) Immunocytochemical studies on the pancreatic islets of the ratfish Chimaera monstrosa. Arch Histol Jpn 49:369–377Google Scholar
  127. Zorn AM, Wells JM (2009) Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol 25:221–251CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biology and Evolution of Marine OrganismsStazione Zoologica Anton DohrnNaplesItaly
  2. 2.Sars International Centre for Marine Molecular BiologyUniversity of BergenBergenNorway
  3. 3.Department of Molecular and Cell Biology and BiochemistryBrown UniversityProvidenceUSA

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