1932

Abstract

The goal of comparative developmental biology is identifying mechanistic differences in embryonic development between different taxa and how these evolutionary changes have led to morphological and organizational differences in adult body plans. Much of this work has focused on direct-developing species in which the adult forms straight from the embryo and embryonic modifications have direct effects on the adult. However, most animal lineages are defined by indirect development, in which the embryo gives rise to a larval body plan and the adult forms by transformation of the larva. Historically, much of our understanding of complex life cycles is viewed through the lenses of ecology and zoology. In this review, we discuss the importance of establishing developmental rather than morphological or ecological criteria for defining developmental mode and explicitly considering the evolutionary implications of incorporating complex life cycles into broad developmental comparisons of embryos across metazoans.

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2023-11-27
2024-06-20
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Literature Cited

  1. 1.
    Adachi S, Niimi I, Sakai Y, Sato F, Minokawa T et al. 2018. Anteroposterior molecular registries in ectoderm of the echinus rudiment. Dev. Dyn. 247:121297–307
    [Google Scholar]
  2. 2.
    Albuixech-Crespo B, López-Blanch L, Burguera D, Maeso I, Sánchez-Arrones L et al. 2017. Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain. PLOS Biol 15:4e2001573
    [Google Scholar]
  3. 3.
    Alvarado AS, Yamanaka S. 2014. Rethinking differentiation: stem cells, regeneration, and plasticity. Cell 157:1110–19
    [Google Scholar]
  4. 4.
    Anderson DT. 1973. Embryology and Phylogeny in Annelids and Arthropods Oxford, UK: Pergamon Press
    [Google Scholar]
  5. 5.
    Akam M. 1995. Hox genes and the evolution of diverse body plans. Philos. Trans. R. Soc. B 349:1329313–19
    [Google Scholar]
  6. 6.
    Angerer LM, Yaguchi S, Angerer RC, Burke RD. 2011. The evolution of nervous system patterning: insights from sea urchin development. Development 138:173613–23
    [Google Scholar]
  7. 7.
    Arenas-Mena C. 2010. Indirect development, transdifferentiation and the macroregulatory evolution of metazoans. Philos. Trans. R. Soc. B 365:1540653–69
    [Google Scholar]
  8. 8.
    Arenas-Mena C, Cameron RA, Davidson EH. 2000. Spatial expression of Hox cluster genes in the ontogeny of a sea urchin. Development 127:214631–43
    [Google Scholar]
  9. 9.
    Arenas-Mena C, Martinez P, Cameron RA, Davidson EH. 1998. Expression of the Hox gene complex in the indirect development of a sea urchin. PNAS 95:2213062–67
    [Google Scholar]
  10. 10.
    Arendt D, Nübler-Jung K. 1996. Common ground plans in early brain development in mice and flies. BioEssays 18:3255–59
    [Google Scholar]
  11. 11.
    Aronowicz J, Lowe CJ. 2006. Hox gene expression in the hemichordate Saccoglossus kowalevskii and the evolution of deuterostome nervous systems. Int. Comp. Biol. 46:6890–901
    [Google Scholar]
  12. 12.
    Bisgrove BW, Raff RA. 1989. Evolutionary conservation of the larval serotonergic nervous system in a direct developing sea urchin. Dev. Growth Differ. 31:4363–70
    [Google Scholar]
  13. 13.
    Byrne M, Koop D, Morris VB, Chui J, Wray GA, Cisternas P. 2018. Expression of genes and proteins of the pax-six-eya-dach network in the metamorphic sea urchin: insights into development of the enigmatic echinoderm body plan and sensory structures. Dev. Dyn. 247:1239–49
    [Google Scholar]
  14. 14.
    Cameron RA, Peterson KJ, Davidson EH. 1998. Developmental gene regulation and the evolution of large animal body plans. Am. Zool. 38:4609–20
    [Google Scholar]
  15. 15.
    Carroll SB. 1995. Homeotic genes and the evolution of arthropods and chordates. Nature 376:6540479–85
    [Google Scholar]
  16. 16.
    Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:125–36
    [Google Scholar]
  17. 17.
    Chea HK, Wright CV, Swalla BJ. 2005. Nodal signaling and the evolution of deuterostome gastrulation. Dev. Dyn. 234:2269–78
    [Google Scholar]
  18. 18.
    Colwin AL, Colwin LH. 1953. The normal embryology of Saccoglossus kowalevskii (Enteropneusta). J. Morphol. 92:3401–53
    [Google Scholar]
  19. 19.
    Darras S, Fritzenwanker JH, Uhlinger KR, Farrelly E, Pani AM et al. 2018. Anteroposterior axis patterning by early canonical Wnt signaling during hemichordate development. PLOS Biol. 16:1e2003698
    [Google Scholar]
  20. 20.
    Davidson EH. 1990. How embryos work: a comparative view of diverse modes of cell fate specification. Development 108:3365–89
    [Google Scholar]
  21. 21.
    Davidson EH. 1991. Spatial mechanisms of gene regulation in metazoan embryos. Development 113:11–26
    [Google Scholar]
  22. 22.
    Davidson EH, Peterson KJ, Cameron RA. 1995. Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270:52401319–25
    [Google Scholar]
  23. 23.
    Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C et al. 2002. A genomic regulatory network for development. Science 295:55601669–78
    [Google Scholar]
  24. 24.
    Davidson PL, Byrne M, Wray GA. 2022. Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins. Mol. Biol. Evol. 39:9msac172
    [Google Scholar]
  25. 25.
    Davidson PL, Guo H, Swart JS, Massri AJ, Edgar A et al. 2022. Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins. Nat. Ecol. Evol. 6:1907–20
    [Google Scholar]
  26. 26.
    Dobzhansky T. 1959. Evolution of genes and genes in evolution. Cold Spring Harb. Symp. Quant. Biol. 24:15–30
    [Google Scholar]
  27. 27.
    Domazet-Lošo T, Tautz D. 2010. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468:7325815–18
    [Google Scholar]
  28. 28.
    Duboc V, Röttinger E, Besnardeau L, Lepage T. 2004. Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev. Cell 6:3397–410
    [Google Scholar]
  29. 29.
    Duboc V, Röttinger E, Lapraz F, Besnardeau L, Lepage T. 2005. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 9:1147–58
    [Google Scholar]
  30. 30.
    Edgar A, Ponciano JM, Martindale MQ. 2022. Ctenophores are direct developers that reproduce continuously beginning very early after hatching. PNAS 119:18e2122052119
    [Google Scholar]
  31. 31.
    Emlet RB. 1986. Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea). J. Exp. Mar. Biol. Ecol. 95:2183–202
    [Google Scholar]
  32. 32.
    Emlet RB. 1990. World patterns of developmental mode in echinoid echinoderms. Adv. Invert. Reprod. 5:329–335
    [Google Scholar]
  33. 33.
    Emlet RB. 1995. Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 167:2405–15
    [Google Scholar]
  34. 34.
    Formery L, Peluso P, Kohnle I, Malnick J, Pitel M et al. 2023. Molecular evidence of anteroposterior patterning in adult echinoderms. bioRxiv 2023.02.05.527185. https://doi.org/10.1101/2023.02.05.527185
    [Crossref]
  35. 35.
    Fröbius AC, Matus DQ, Seaver EC. 2008. Genomic organization and expression demonstrate spatial and temporal Hox gene colinearity in the lophotrochozoan Capitella sp. I. PLOS ONE 3:12e4004
    [Google Scholar]
  36. 36.
    Gąsiorowski L, Hejnol A. 2020. Hox gene expression during development of the phoronid Phoronopsis harmeri. EvoDevo 11:2
    [Google Scholar]
  37. 37.
    Gonzalez P, Uhlinger KR, Lowe CJ. 2017. The adult body plan of indirect developing hemichordates develops by adding a Hox-patterned trunk to an anterior larval territory. Curr. Biol. 27:187–95
    [Google Scholar]
  38. 38.
    Graham A, Papalopulu N, Krumlauf R. 1989. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57:3367–78
    [Google Scholar]
  39. 39.
    Grahame J, Branch M. 1985. Reproductive patterns of marine invertebrates. Oceanogr. Mar. Biol. Annu. Rev. 23:373–98
    [Google Scholar]
  40. 40.
    Green SA, Norris RP, Terasaki M, Lowe CJ. 2013. FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii. Development 140:51024–33
    [Google Scholar]
  41. 41.
    Haeckel E. 1866. Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begrïndet durch die von Charles Darwin reformirte Descendenz-Theorie Berlin: Georg Reimer
    [Google Scholar]
  42. 42.
    Hall BK. 1997. Phylotypic stage or phantom: Is there a highly conserved embryonic stage in vertebrates?. Trends Ecol. Evol. 12:12461–63
    [Google Scholar]
  43. 43.
    Hall BK, Wake MH. 1999. The Origin and Evolution of Larval Forms San Diego, CA: Academic
    [Google Scholar]
  44. 44.
    Hara Y, Yamaguchi M, Akasaka K, Nakano H, Nonaka M, Amemiya S. 2006. Expression patterns of Hox genes in larvae of the sea lily Metacrinus rotundus. Dev. Genes Evol. 216:797–809
    [Google Scholar]
  45. 45.
    Harland R, Gerhart J. 1997. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13:611–67
    [Google Scholar]
  46. 46.
    Hart MW. 1996. Evolutionary loss of larval feeding: development, form and function in a facultatively feeding larva, Brisaster latifrons. Evolution 50:1174–87
    [Google Scholar]
  47. 47.
    Haug JT. 2020. Why the term “larva” is ambiguous, or what makes a larva?. Acta Zool. 101:2167–88
    [Google Scholar]
  48. 48.
    Hejnol A, Dunn CW. 2016. Animal evolution: Are phyla real?. Curr. Biol. 26:10R424–26
    [Google Scholar]
  49. 49.
    Hejnol A, Vellutini BC. 2017. Larval evolution: I'll tail you later…. Curr. Biol. 27:1R21–24
    [Google Scholar]
  50. 50.
    Held LJ. 2005. Imaginal Discs Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  51. 51.
    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 110:3875–84
    [Google Scholar]
  52. 52.
    Henry JQ, Tagawa K, Martindale MQ. 2001. Deuterostome evolution: early development in the enteropneust hemichordate, Ptychodera flava. Evol. Dev. 3:6375–90
    [Google Scholar]
  53. 53.
    Hiebert LS, Maslakova SA. 2015. Expression of Hox, Cdx, and Six3/6 genes in the hoplonemertean Pantinonemertes californiensis offers insight into the evolution of maximally indirect development in the phylum Nemertea. EvoDevo 6:26
    [Google Scholar]
  54. 54.
    Hiebert LS, Maslakova SA. 2015. Hox genes pattern the anterior-posterior axis of the juvenile but not the larva in a maximally indirect developing invertebrate, Micrura alaskensis (Nemertea). BMC Biol. 13:23
    [Google Scholar]
  55. 55.
    Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H. 2003. An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130:112365–73
    [Google Scholar]
  56. 56.
    Irie N, Kuratani S. 2011. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat. Commun. 2:1248
    [Google Scholar]
  57. 57.
    Irie N, Kuratani S. 2014. The developmental hourglass model: a predictor of the basic body plan?. Development 141:244649–55
    [Google Scholar]
  58. 58.
    Irvine SQ, Martindale MQ. 2000. Expression patterns of anterior Hox genes in the polychaete Chaetopterus: correlation with morphological boundaries. Dev. Biol. 217:2333–51
    [Google Scholar]
  59. 59.
    Israel JW, Martik ML, Byrne M, Raff EC, Raff RA et al. 2016. Comparative developmental transcriptomics reveals rewiring of a highly conserved gene regulatory network during a major life history switch in the sea urchin genus Heliocidaris. PLOS Biol. 14:3e1002391
    [Google Scholar]
  60. 60.
    Jägersten G. 1972. Evolution of the Metazoan Life Cycle London: Academic
    [Google Scholar]
  61. 61.
    Kalinka AT, Tomancak P. 2012. The evolution of early animal embryos: conservation or divergence?. Trends Ecol. Evol. 27:7385–93
    [Google Scholar]
  62. 62.
    Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL et al. 2010. Gene expression divergence recapitulates the developmental hourglass model. Nature 468:7325811–14
    [Google Scholar]
  63. 63.
    Kauffman JS, Raff RA. 2003. Patterning mechanisms in the evolution of derived developmental life histories: the role of Wnt signaling in axis formation of the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Gene Evol. 213:612–24
    [Google Scholar]
  64. 64.
    Kikuchi M, Omori A, Kurokawa D, Akasaka K. 2015. Patterning of anteroposterior body axis displayed in the expression of Hox genes in sea cucumber Apostichopus japonicus. Dev. Genes Evol. 225:275–86
    [Google Scholar]
  65. 65.
    Koop D, Cisternas P, Morris VB, Strbenac D, Yang JYH et al. 2017. Nodal and BMP expression during the transition to pentametry in the sea urchin Heliocidaris erythrogramma: insights into patterning the enigmatic echinoderm body plan. BMC Dev. Biol. 17:4
    [Google Scholar]
  66. 66.
    Krumlauf R. 1994. Hox genes in vertebrate development. Cell 78:2191–201
    [Google Scholar]
  67. 67.
    Kulakova M, Bakalenko N, Novikova E, Cook CE, Eliseeva E et al. 2007. Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Dev. Genes Evol. 217:39–54
    [Google Scholar]
  68. 68.
    Lacalli TC. 1993. Ciliary bands in echinoderm larvae: evidence for structural homologies and a common plan. Acta Zool 74:2127–33
    [Google Scholar]
  69. 69.
    Lacalli TC. 2005. Protochordate body plan and the evolutionary role of larvae: old controversies resolved?. Can. J. Zool. 83:1216–24
    [Google Scholar]
  70. 70.
    Lapraz F, Haillot E, Lepage T. 2015. A deuterostome origin of the Spemann organiser suggested by Nodal and ADMPs functions in Echinoderms. Nat. Commun. 6:18434
    [Google Scholar]
  71. 71.
    Levin M, Anavy L, Cole AG, Winter E, Mostov N et al. 2016. The mid-developmental transition and the evolution of animal body plans. Nature 531:7596637–41
    [Google Scholar]
  72. 72.
    Levin M, Hashimshony T, Wagner F, Yanai I. 2012. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev. Cell 22:51101–8
    [Google Scholar]
  73. 73.
    Li Y, Omori A, Flores RL, Satterfield S, Nguyen C et al. 2020. Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms. Commun. Biol. 3:371
    [Google Scholar]
  74. 74.
    Linnaeus C. 1767. Systema Naturæ, Vol. 1 Part 2 Regnum Animale Stockholm: Laurentii Salvii
    [Google Scholar]
  75. 75.
    Lowe CJ, Clarke DN, Medeiros DM, Rokhsar DS, Gerhart J. 2015. The deuterostome context of chordate origins. Nature 520:7548456–65
    [Google Scholar]
  76. 76.
    Lowe CJ, Wu M, Salic A, Evans L, Lander E et al. 2003. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113:7853–65
    [Google Scholar]
  77. 77.
    Luo Y-J, Kanda M, Koyanagi R, Hisata K, Akiyama T et al. 2018. Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads. Nat. Ecol. Evol. 2:141–51
    [Google Scholar]
  78. 78.
    Malik A, Gildor T, Sher N, Layous M, de-Leon SB-T. 2017. Parallel embryonic transcriptional programs evolve under distinct constraints and may enable morphological conservation amidst adaptation. Dev. Biol. 430:1202–13
    [Google Scholar]
  79. 79.
    Marlow H 2018. Evolutionary development of marine larvae. Evolutionary Ecology of Marine Invertebrate Larvae TJ Carrier, AM Reitzel, A Heyland 16–33. Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  80. 80.
    Martin BL, Kimelman D. 2009. Wnt signaling and the evolution of embryonic posterior development. Curr. Biol. 19:5215–19
    [Google Scholar]
  81. 81.
    Martindale MQ. 1987. Larval reproduction in the ctenophore Mnemiopsis mccradyi (order Lobata). Mar. Biol. 94:409–14
    [Google Scholar]
  82. 82.
    Martín-Zamora FM, Liang Y, Guynes K, Carrillo-Baltodano AM, Davies BE et al. 2023. Annelid functional genomics reveal the origins of bilaterian life cycles. Nature 615:7950105–10
    [Google Scholar]
  83. 83.
    McEdward LR. 1995. Ecology of Marine Invertebrate Larvae Boca Raton, FL: CRC Press. , 1st ed..
    [Google Scholar]
  84. 84.
    McEdward LR, Janies DA. 1993. Life cycle evolution in asteroids: What is a larva?. Biol. Bull. 184:3255–68
    [Google Scholar]
  85. 85.
    McEdward LR, Janies DA. 1997. Relationships among development, ecology, and morphology in the evolution of Echinoderm larvae and life cycles. Biol. J. Linn. Soc. 60:3381–400
    [Google Scholar]
  86. 86.
    McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 68:2283–302
    [Google Scholar]
  87. 87.
    McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ. 1984. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308:5958428–33
    [Google Scholar]
  88. 88.
    Mileikovsky SA. 1971. Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Mar. Biol. 10:193–213
    [Google Scholar]
  89. 89.
    Minelli A. 2003. The Development of Animal Form: Ontogeny, Morphology, and Evolution Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  90. 90.
    Minsuk SB, Raff RA. 2005. Co-option of an oral–aboral patterning mechanism to control left–right differentiation: The direct-developing sea urchin Heliocidaris erythrogramma is sinistralized, not ventralized, by NiCl2. Evol. Dev. 7:4289–300
    [Google Scholar]
  91. 91.
    Morris VB. 1995. Apluteal development of the sea urchin Holopneustes purpurescens Agassiz (Echinodermata: Echinoidea: Euechinoidea). Zool. J. Linn. Soc. 114:4349–64
    [Google Scholar]
  92. 92.
    Nielsen C. 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool 68:4205–62
    [Google Scholar]
  93. 93.
    Nielsen C. 2008. Six major steps in animal evolution: Are we derived sponge larvae?. Evol. Dev. 10:2241–57
    [Google Scholar]
  94. 94.
    Nielsen C. 2012. Animal Evolution: Interrelationships of the Living Phyla Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  95. 95.
    Novikova EL, Bakalenko NI, Nesterenko AY, Kulakova MA. 2013. Expression of Hox genes during regeneration of nereid polychaete Alitta (Nereis) virens (Annelida, Lophotrochozoa). EvoDevo 4:14
    [Google Scholar]
  96. 96.
    Okazaki K, Dan K. 1954. The metamorphosis of partial larvae of Peronella japonica Mortensen, a sand dollar. Biol. Bull. 106:183–99
    [Google Scholar]
  97. 97.
    Olson RR, Cameron JL, Young CM. 1993. Larval development (with observations on spawning) of the pencil urchin Phyllacanthus imperialis: a new intermediate larval form?. Biol. Bull. 185:177–85
    [Google Scholar]
  98. 98.
    Page LR. 2009. Molluscan larvae: pelagic juveniles or slowly metamorphosing larvae?. Biol. Bull. 216:3216–25
    [Google Scholar]
  99. 99.
    Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ. 2012. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483:7389289–94
    [Google Scholar]
  100. 100.
    Pearson JC, Lemons D, McGinnis W. 2005. Modulating Hox gene functions during animal body patterning. Nat. Rev. Genet. 6:12893–904
    [Google Scholar]
  101. 101.
    Peterson KJ, Cameron RA, Davidson EH. 1997. Set-aside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19:7623–31
    [Google Scholar]
  102. 102.
    Peterson KJ, Cameron RA, Davidson EH. 2000. Bilaterian origins: significance of new experimental observations. Dev. Biol. 219:11–17
    [Google Scholar]
  103. 103.
    Peterson KJ, Davidson EH. 2000. Regulatory evolution and the origin of the bilaterians. PNAS 97:94430–33
    [Google Scholar]
  104. 104.
    Peterson KJ, Irvine SQ, Cameron RA, Davidson EH. 2000. Quantitative assessment of Hox complex expression in the indirect development of the polychaete annelid Chaetopterus sp. PNAS 97:94487–92
    [Google Scholar]
  105. 105.
    Raff RA. 1987. Constraint, flexibility, and phylogenetic history in the evolution of direct development in sea urchins. Dev. Biol. 119:16–19
    [Google Scholar]
  106. 106.
    Raff RA. 1996. The Shape of Life: Genes, Development, and the Evolution of Animal Form Chicago: Univ. Chicago Press
    [Google Scholar]
  107. 107.
    Raff RA. 2008. Origins of the other metazoan body plans: the evolution of larval forms. Philos. Trans. R. Soc. B 363:14961473–79
    [Google Scholar]
  108. 108.
    Range RC, Angerer RC, Angerer LM. 2013. Integration of canonical and noncanonical Wnt signaling pathways patterns the neuroectoderm along the anterior–posterior axis of sea urchin embryos. PLOS Biol 11:1e1001467
    [Google Scholar]
  109. 109.
    Reichert H, Simeone A. 2001. Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philos. Trans. R. Soc. B 356:14141533–44
    [Google Scholar]
  110. 110.
    Röttinger E, DuBuc TQ, Amiel AR, Martindale MQ. 2015. Nodal signaling is required for mesodermal and ventral but not for dorsal fates in the indirect developing hemichordate, Ptychodera flava. Biol. Open 4:7830–42
    [Google Scholar]
  111. 111.
    Röttinger E, Lowe CJ. 2012. Evolutionary crossroads in developmental biology: hemichordates. Development 139:142463–75
    [Google Scholar]
  112. 112.
    Rouse G, Pleijel F, Tilic E. 2022. Annelida Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  113. 113.
    Roux N, Salis P, Lambert A, Logeux V, Soulat O et al. 2019. Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris). Dev. Dyn. 248:7545–68
    [Google Scholar]
  114. 114.
    Santagata S, Resh C, Hejnol A, Martindale MQ, Passamaneck YJ. 2012. Development of the larval anterior neurogenic domains of Terebratalia transversa (Brachiopoda) provides insights into the diversification of larval apical organs and the spiralian nervous system. EvoDevo 3:3
    [Google Scholar]
  115. 115.
    Satoh N. 2003. The ascidian tadpole larva: comparative molecular development and genomics. Nat. Rev. Genet. 4:4285–95
    [Google Scholar]
  116. 116.
    Saudemont A, Haillot E, Mekpoh F, Bessodes N, Quirin M et al. 2010. Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLOS Genet 6:12e1001259
    [Google Scholar]
  117. 117.
    Slack JM, Holland PW, Graham CF. 1993. The zootype and the phylotypic stage. Nature 361:6412490–92
    [Google Scholar]
  118. 118.
    Sly BJ, Snoke MS, Raff RA. 2003. Who came first—larvae or adults? Origins of bilaterian metazoan larvae. Int. J. Dev. Biol. 47:7–8623–32
    [Google Scholar]
  119. 119.
    Soto-Angel JJ, Jaspers C, Hosia A, Majaneva S, Martell L, Burkhardt P. 2023. Are we there yet to eliminate the terms larva, metamorphosis, and dissogeny from the ctenophore literature?. PNAS 120:4e2218317120
    [Google Scholar]
  120. 120.
    Steinmetz PR, Kostyuchenko RP, Fischer A, Arendt D. 2011. The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol. Dev. 13:172–79
    [Google Scholar]
  121. 121.
    Strathmann RR. 1971. The feeding behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. J. Exp. Mar. Biol. Ecol. 6:2109–60
    [Google Scholar]
  122. 122.
    Strathmann RR. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:4894–906
    [Google Scholar]
  123. 123.
    Strathmann RR. 2020. Multiple origins of feeding head larvae by the Early Cambrian. Can. J. Zool. 98:12761–76
    [Google Scholar]
  124. 124.
    Strathmann RR, Bonar D. 1976. Ciliary feeding of tornaria larvae of Ptychodera flava (Hemichordata: Enteropneusta). Mar. Biol. 34:317–24
    [Google Scholar]
  125. 125.
    Thorson G. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 25:11–45
    [Google Scholar]
  126. 126.
    Tomer R, Denes AS, Tessmar-Raible K, Arendt D. 2010. Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142:5800–9
    [Google Scholar]
  127. 127.
    Truman JW, Price J, Miyares RL, Lee T. 2023. Metamorphosis of memory circuits in Drosophila reveals a strategy for evolving a larval brain. eLife 12:e80594
    [Google Scholar]
  128. 128.
    Tsuchimoto J, Yamaguchi M. 2014. Hox expression in the direct-type developing sand dollar Peronella japonica. Dev. Dyn. 243:81020–29
    [Google Scholar]
  129. 129.
    Valentine JW, Collins AG. 2000. The significance of moulting in Ecdysozoan evolution. Evol. Dev. 2:3152–56
    [Google Scholar]
  130. 130.
    von Baer KE. 1828. Über Entwickelungsgeschichte der Thiere. Beobachtung und Reflexion Königsberg, Ger.: Bornträger
    [Google Scholar]
  131. 131.
    Vyas H, Schrankel CS, Espinoza JA, Mitchell KL, Nesbit KT et al. 2022. Generation of a homozygous mutant drug transporter (ABCB1) knockout line in the sea urchin Lytechinus pictus. Development 149:11dev200644
    [Google Scholar]
  132. 132.
    Wada H, Garcia-Fernàndez J, Holland PWH. 1999. Colinear and segmental expression of amphioxus Hox genes. Dev. Biol. 213:1131–41
    [Google Scholar]
  133. 133.
    Wei M, Qin Z, Kong D, Liu D, Zheng Q et al. 2022. Echiuran Hox genes provide new insights into the correspondence between Hox subcluster organization and collinearity pattern. Proc. Royal Soc. B 289:20220705
    [Google Scholar]
  134. 134.
    Weissbourd B, Momose T, Nair A, Kennedy A, Hunt B, Anderson DJ. 2021. A genetically tractable jellyfish model for systems and evolutionary neuroscience. Cell 184:245854–68
    [Google Scholar]
  135. 135.
    Wilson DP. 1932. On the mitraria larva of Owenia fusiformis Delle Chiaje. Philos. Trans. R. Soc. B 221:474–82231–34
    [Google Scholar]
  136. 136.
    Wlizla M. 2011. Evolution of Nodal signaling in deuterostomes: insights from Saccoglossus kowalevskii PhD Thesis Univ. Chicago
    [Google Scholar]
  137. 137.
    Wray GA. 1996. Parallel evolution of nonfeeding larvae in echinoids. Syst. Biol. 45:3308–22
    [Google Scholar]
  138. 138.
    Wray GA. 2000. The evolution of embryonic patterning mechanisms in animals. Semin. Cell Dev. Biol. 11:6385–93
    [Google Scholar]
  139. 139.
    Wray GA, Raff RA. 1990. Novel origins of lineage founder cells in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 141:141–54
    [Google Scholar]
  140. 140.
    Wygoda JA, Yang Y, Byrne M, Wray GA. 2014. Transcriptomic analysis of the highly derived radial body plan of a sea urchin. Genome Biol. Evol. 6:4964–73
    [Google Scholar]
  141. 141.
    Yaguchi S, Yaguchi J, Suzuki H, Kinjo S, Kiyomoto M et al. 2020. Establishment of homozygous knock-out sea urchins. Curr. Biol. 30:10R427–29
    [Google Scholar]
  142. 142.
    Yanai I. 2018. Development and evolution through the lens of global gene regulation. Trends Genet 34:111–20
    [Google Scholar]
  143. 143.
    Yankura KA, Martik ML, Jennings CK, Hinman VF. 2010. Uncoupling of complex regulatory patterning during evolution of larval development in echinoderms. BMC Biol 8:143
    [Google Scholar]
  144. 144.
    Zigler KS, Raff EC, Popodi E, Raff RA, Lessios HA. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57:102293–302
    [Google Scholar]
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