Sea Urchin Larvae as a Model for Postembryonic Development

  • Andreas HeylandEmail author
  • Nicholas Schuh
  • Jonathan Rast
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)


Larvae are a diverse set of postembryonic life forms distinct from juveniles or adults that have evolved in many animal phyla. Echinoids (sea urchins and sand dollars) generate rapidly developing, morphologically simple, and optically transparent larvae and are a well-established model system supported by a broad array of genomic resources, experimental approaches, and imaging techniques. As such, they provide a unique opportunity to study postembryonic processes such as endocrine signaling, immunity, host–microbe interactions, and regeneration. Here we review a broad array of literature focusing on these important processes in sea urchin larvae, providing support for the claim that they represent excellent experimental study systems. Specifically, there is strong evidence emerging that endocrine signaling, immunity, and host–microbe interactions play major roles in larval development and physiology. Future research should take advantage of sea urchin larvae as a model to study these processes in more detail.


Thyroid hormones Nitric oxide Histamine Microbiota IL-17 Signaling Phagocytosis Innate immunity 


  1. Adams DK, Sewell MA, Angerer RC, Angerer LM (2011) Rapid adaptation to food availability by a dopamine-mediated morphogenetic response. Nat Commun 2:592CrossRefPubMedPubMedCentralGoogle Scholar
  2. Allen JD, Reitzel AM, Jaeckle W (2018) Asexual reproduction of marine invertebrate embryos and larvae. In: Carrier T, Reitzel A, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, Oxford, pp 67–82Google Scholar
  3. Balakirev ES, Pavlyuchkov VA, Ayala FJ (2008) DNA variation and symbiotic associations in phenotypically diverse sea urchin Strongylocentrotus intermedius. Proc Natl Acad Sci USA 105:16218–16223CrossRefPubMedGoogle Scholar
  4. Balser EJ (1998) Cloning by ophiuroid echinoderm larvae. Biol Bull 194:187–193CrossRefPubMedGoogle Scholar
  5. Bishop CD, Brandhorst BP (2001a) NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull 201:394–404CrossRefPubMedGoogle Scholar
  6. Bishop CD, Brandhorst BP (2001b) The role of NO/cGMP and HSP90 in regulating metamorphosis of the sea urchin Lytechinus pictus. Dev Biol 235:251Google Scholar
  7. Bishop CD, Erezyilmaz DF, Flatt T, Georgiou CD, Hadfield MG, Heyland A, Hodin J, Jacobs MW, Maslakova SA, Pires A, Reitzel AM, Santagata S, Tanaka K, Youson JH (2006a) What is metamorphosis? Integr Comp Biol 46:655–661CrossRefPubMedGoogle Scholar
  8. Bishop CD, Huggett MJ, Heyland A, Hodin J, Brandhorst BP (2006b) Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis. Integr Comp Biol 46:662–682CrossRefPubMedGoogle Scholar
  9. Bodnar AG, Coffman JA (2016) Maintenance of somatic tissue regeneration with age in short- and long-lived species of sea urchins. Aging Cell 15:778–787CrossRefPubMedPubMedCentralGoogle Scholar
  10. Buckley KM, Rast JP (2012) Dynamic evolution of toll-like receptor multigene families in echinoderms. Front Immunol 3:136CrossRefPubMedPubMedCentralGoogle Scholar
  11. Buckley KM, Rast JP (2017) An organismal model for gene regulatory networks in the gut-associated immune response. Front Immunol 8:1297CrossRefPubMedPubMedCentralGoogle Scholar
  12. Buckley KM, Ho ECH, Hibino T, Schrankel CS, Schuh NW, Wang G, Rast JP (2017) IL17 factors are early regulators in the gut epithelium during inflammatory response to Vibrio in the sea urchin larva. Elife 6:e23481CrossRefPubMedPubMedCentralGoogle Scholar
  13. Buszczak M, Segraves WA (2000) Insect metamorphosis: out with the old, in with the new. Curr Biol 10(22):R830–R833CrossRefPubMedGoogle Scholar
  14. Cameron RA, Holland ND (1983) Electron-microscopy of extracellular materials during the development of a sea star, Patiria-miniata (echinodermata, asteroidea). Cell Tissue Res 234:193–200CrossRefPubMedGoogle Scholar
  15. Cameron RA, Holland ND (1985) Demonstration of the granular layer and the fate of the hyaline layer during the development of a sea-urchin (Lytechinus-variegatus). Cell Tissue Res 239:455–458CrossRefPubMedGoogle Scholar
  16. Candia CMD, Paolo B (2010) Regeneration in echinoderms and ascidians, encyclopedia of life sciences (ELS). Wiley, ChichesterGoogle Scholar
  17. Carrier TJ, Reitzel AM (2018) Convergent shifts in host-associated microbial communities across environmentally elicited phenotypes. Nature Communications 9:952CrossRefPubMedPubMedCentralGoogle Scholar
  18. Carrier TJ, Reitzel A, Heyland A (2017) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, OxfordGoogle Scholar
  19. Cerra A, Byrne M, Hoegh-Guldberg O (1997) Development of the hyaline layer around the planktonic embryos and larvae of the asteroid and the presence of associated bacteria. Invertebrate Reproduction & Development 31(1–3):337–343CrossRefGoogle Scholar
  20. De Ridder C, Foret TW (2006) Non-parasitc symbioses between echinoderms and bacteria. In: Jangoux M, Lawrence JM (eds) Echinoderm studies. Balkema Publishers, Leiden, pp 111–169Google Scholar
  21. Decker GL, Lennarz WJ (1988) Skeletogenesis in the sea-urchin embryo. Development 103:231–247PubMedGoogle Scholar
  22. Dworjanyn SA, Pirozzi I (2008) Induction of settlement in the sea urchin Tripneustes gratilla by macroalgae, biofilms and conspecifics: a role for bacteria? Aquaculture 274:268–274CrossRefGoogle Scholar
  23. Eaves AA, Palmer AR (2003) Reproduction: widespread cloning in echinoderm larvae. Nature 425:146CrossRefPubMedGoogle Scholar
  24. Ebert TA, Southon JR (2013) Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fish Bull 101:915–922Google Scholar
  25. Flatt T, Moroz LL, Tatar M, Heyland A (2006) Comparing thyroid and insect hormone signaling. Integr Comp Biol 46:777–794CrossRefPubMedGoogle Scholar
  26. Gibson AW, Burke RD (1987) Migratory and invasive behavior of pigment cells in normal and animalized sea urchin embryos. Exp Cell Res 173:546–557CrossRefPubMedGoogle Scholar
  27. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341CrossRefGoogle Scholar
  28. Guerinot ML, West PA, Lee JV, Colwell RR (1982) Vibrio-diazotrophicus sp-nov, a marine nitrogen-fixing bacterium. Int J Syst Bacteriol 32:350–357CrossRefGoogle Scholar
  29. Hakim JA, Koo H, Dennis LN, Kumar R, Ptacek T, Morrow CD, Lefkowitz EJ, Powell ML, Bej AK, Watts SA (2015) An abundance of Epsilonproteobacteria revealed in the gut microbiome of the laboratory cultured sea urchin, Lytechinus variegatus. Front Microbiol 6:1047CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hakim JA, Koo H, Kumar R, Lefkowitz EJ, Morrow CD, Powell ML, Watts SA, Bej AK (2016) The gut microbiome of the sea urchin, Lytechinus variegatus, from its natural habitat demonstrates selective attributes of microbial taxa and predictive metabolic profiles. Fems Microbiol Ecol 92(9):fiw146CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hart MW, Strathmann RR (1994) Functional consequences of phenotypic plasticity in echinoid larvae. Biol Bull 186:291–299CrossRefPubMedGoogle Scholar
  32. Herren B, Levkau B, Raines EW, Ross R (1998) Cleavage of beta catenin and plakoglobin and shedding of VE-cadherin during endothelial apoptosis: evidence for a role for caspases and metalloproteinases. Mol Biol Cell 9:1589–1601CrossRefPubMedPubMedCentralGoogle Scholar
  33. Heyland A, Hodin J (2004) Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development. Evolution 58:524–538CrossRefPubMedGoogle Scholar
  34. Heyland A, Moroz LL (2006) Signaling mechanisms underlying metamorphic transitions in animals. Integr Comp Biol 46:743–759CrossRefPubMedGoogle Scholar
  35. Heyland A, Reitzel AM, Hodin J (2001) Facultative feeding in an obligatorily feeding sand dollar larva: the role of thyroid hormones in echinoderm life history evolution. Am Zool 41:1470–1471Google Scholar
  36. Heyland A, Reitzel AM, Hodin J (2004) Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). Evol Dev 6:382–392CrossRefPubMedGoogle Scholar
  37. Heyland A, Hodin J, Reitzel AM (2005) Hormone signaling in evolution and development: a non-model system approach. Bioessays 27:64–75CrossRefPubMedGoogle Scholar
  38. Heyland A, Price DA, Bodnarova-Buganova M, Moroz LL (2006) Thyroid hormone metabolism and peroxidase function in two non-chordate animals. J Exp Zool B Mol Dev Evol 306:551–566CrossRefPubMedGoogle Scholar
  39. Heyland A, Reitzel A, Hodin J (2009) Thyroid hormone signaling in echinoderms: comparative genomics, cross-kingdom signaling and life history evolution. Integr Comp Biol 49:E242Google Scholar
  40. Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365CrossRefPubMedGoogle Scholar
  41. Hinman V, Cary G (2017) Conserved processes of metazoan whole-body regeneration identified in sea star larvae. bioRxiv.
  42. Ho EC, Buckley KM, Schrankel CS, Schuh NW, Hibino T, Solek CM, Bae K, Wang G, Rast JP (2017) Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 95:647CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hodin J, Bishop CD, Heyland A (2010) Towards a metamorphic and settlement signaling network in echinoids. Integr Comp Biol 50:E76Google Scholar
  44. Holland ND, Nealson KH (1978) The fine structure of the echinoderm cuticle and the subcuticular space of echinoderms. Acta Zool 59:169–185CrossRefGoogle Scholar
  45. Holstein TW, Hobmayer E, Technau U (2003) Cnidarians: an evolutionarily conserved model system for regeneration? Dev Dyn 226:257–267CrossRefPubMedGoogle Scholar
  46. Huggett MJ, Williamson JE, de Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619CrossRefPubMedGoogle Scholar
  47. Ingersoll EP, Pendharkar NC (2005) Characterization and expression of two matrix metalloproteinase genes during sea urchin development. Gene Expr Patterns 5:727–732CrossRefPubMedGoogle Scholar
  48. Ingersoll EP, Wilt FH (1998) Matrix metalloproteinase inhibitors disrupt spicule formation by primary mesenchyme cells in the sea urchin embryo. Dev Biol 196:95–106CrossRefPubMedGoogle Scholar
  49. Ishizuya-Oka A, Hasebe T, Shi YB (2010) Apoptosis in amphibian organs during metamorphosis. Apoptosis 15:350–364CrossRefPubMedPubMedCentralGoogle Scholar
  50. Johnson CR, Sutton DC, Olson RR, Giddins R (1991) Settlement of crown-of-thorns starfish: role of bacteria on surfaces of coralline algae and a hypothesis for deep-water recruitment. Mar Ecol Prog Ser 71:143–162CrossRefGoogle Scholar
  51. Kiselev KV, Ageenko NV, Kurilenko VV (2013) Involvement of the cell-specific pigment genes pks and sult in bacterial defense response of sea urchins Strongylocentrotus intermedius. Dis Aquat Organ 103:121–132CrossRefPubMedGoogle Scholar
  52. Koga H, Fujitani H, Morino Y, Miyamoto N, Tsuchimoto J, Shibata TF, Nozawa M, Shigenobu S, Ogura A, Tachibana K, Kiyomoto M, Amemiya S, Wada H (2016) Experimental approach reveals the role of alx1 in the evolution of the echinoderm larval skeleton. PLoS One 11(2):e0149067CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kyriakidis DA, Theodorou MC, Tiligada E (2012) Histamine in two component system-mediated bacterial signaling. Front Biosci Landmark 17:1108–1119CrossRefGoogle Scholar
  54. Leguia M, Wessel GM (2006) The histamine H1 receptor activates the nitric oxide pathway at fertilization. Mol Reprod Dev 73:1550–1563CrossRefPubMedGoogle Scholar
  55. Li C, Blencke HM, Haug T, Jorgensen O, Stensvag K (2014) Expression of antimicrobial peptides in coelomocytes and embryos of the green sea urchin (Strongylocentrotus droebachiensis). Dev Comp Immunol 43:106–113CrossRefPubMedGoogle Scholar
  56. Lutek K, Dhaliwal RS, Van Raay TJ, Heyland A (2018) Sea urchin histamine receptor 1 regulates programmed cell death in larval Strongylocentrotus purpuratus. Scientific Reports 8:4002CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mathew S, Fu LZ, Hasebe T, Ishizuya-Oka A, Shi YB (2010) Tissue-dependent induction of apoptosis by matrix metalloproteinase stromelysin-3 during amphibian metamorphosis. Birth Defects Res C 90:55–66CrossRefGoogle Scholar
  58. McAlister JS, Miner BG (2018) Phenotypic plasticity of feeding structures in marine invertebrate larvae. In: Carrier T, Reitzel A, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, Oxford, pp 103–123Google Scholar
  59. McEdward LR (2000) Adaptive evolution of larvae and life cycles. Semin Cell Dev Biol 11:403–409CrossRefPubMedGoogle Scholar
  60. McEdward LR, Janies DA (1993) Life-cycle evolution in asteroids: what is a larva. Biol Bull 184:255–268CrossRefPubMedGoogle Scholar
  61. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236CrossRefPubMedGoogle Scholar
  62. McIntyre DC, Lyons DC, Martik M, McClay DR (2014) Branching out: origins of the sea urchin larval skeleton in development and evolution. Genesis 52:173–185CrossRefPubMedPubMedCentralGoogle Scholar
  63. Metchnikoff E (1893) Lectures on the comparative pathology of inflammation: delivered at the Pasteur Institute in 1891. In: Starling FA, Starling EH (eds). Kegan Paul, Trench, Trubner & Co. Ltd., LondonGoogle Scholar
  64. Miller AE, Heyland A (2010) Endocrine interactions between plants and animals: implications of exogenous hormone sources for the evolution of hormone signaling. Gen Comp Endocrinol 166:455–461CrossRefPubMedGoogle Scholar
  65. Miller AE, Heyland A (2013) Iodine accumulation in sea urchin larvae is dependent on peroxide. J Exp Biol 216:915–926CrossRefPubMedGoogle Scholar
  66. Miner BG (2005) Evolution of feeding structure plasticity in marine invertebrate larvae: a possible trade-off between arm length and stomach size. J Exp Mar Biol Ecol 315:117–125CrossRefGoogle Scholar
  67. Miner BG, Vonesh JR (2004) Effects of fine grain environmental variability on morphological plasticity. Ecol Lett 7:794–801CrossRefGoogle Scholar
  68. Mos B, Cowden KL, Nielsen SJ, Dworjanyn SA (2011) Do cues matter? Highly inductive settlement cues don’t ensure high post-settlement survival in sea urchin aquaculture. PLoS One 6(12):e28054CrossRefPubMedPubMedCentralGoogle Scholar
  69. Nassel DR (1999) Histamine in the brain of insects: a review. Microsc Res Tech 44:121–136CrossRefPubMedGoogle Scholar
  70. Nielsen SJ, Harder T, Steinberg PD (2015) Sea urchin larvae decipher the epiphytic bacterial community composition when selecting sites for attachment and metamorphosis. Fems Microbiol Ecol 91:1–9CrossRefPubMedGoogle Scholar
  71. Oulhen N, Heyland A, Carrier TJ, Zazueta-Novoa V, Fresques T, Laird J, Onorato TM, Janies D, Wessel G (2016) Regeneration in bipinnaria larvae of the bat star Patina miniata induces rapid and broad new gene expression. Mech Dev 142:10–21CrossRefPubMedPubMedCentralGoogle Scholar
  72. Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Bio 8:221–233CrossRefGoogle Scholar
  73. Rao PS, Rao KH, Shyamasundari K (1993) A rare condition of budding in bipinaria larva (Asteroidea). Curr Sci 65:792–793Google Scholar
  74. Ribeiro AR, Barbaglio A, Oliveira MJ, Ribeiro CC, Wilkie IC, Carnevali MDC, Barbosa MA (2012) Matrix metalloproteinases in a sea urchin ligament with adaptable mechanical properties. PLoS One 7(11):e49016CrossRefPubMedPubMedCentralGoogle Scholar
  75. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, McClay DR, Coffman JA (2006) The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev Biol 300:321–334CrossRefPubMedGoogle Scholar
  76. Roeder T (2003) Metabotropic histamine receptors: nothing for invertebrates? Eur J Pharmacol 466:85–90CrossRefPubMedGoogle Scholar
  77. Ruffins SW, Ettensohn CA (1993) A clonal analysis of secondary mesenchyme cell fates in the sea urchin embryo. Dev Biol 160:285–288CrossRefPubMedGoogle Scholar
  78. Schrankel CS, Solek CM, Buckley KM, Anderson MK, Rast JP (2016) A conserved alternative form of the purple sea urchin HEB/E2-2/E2A transcription factor mediates a switch in E-protein regulatory state in differentiating immune cells. Dev Biol 416:149–161CrossRefPubMedGoogle Scholar
  79. Sea Urchin Genome Sequencing Consortium, Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, Elphick MR, Ettensohn CA, Foltz KR, Hamdoun A, Hynes RO, Klein WH, Marzluff W, McClay DR, Morris RL, Mushegian A, Rast JP, Smith LC, Thorndyke MC, Vacquier VD, Wessel GM, Wray G, Zhang L, Elsik CG, Ermolaeva O, Hlavina W, Hofmann G, Kitts P, Landrum MJ, Mackey AJ, Maglott D, Panopoulou G, Poustka AJ, Pruitt K, Sapojnikov V, Song X, Souvorov A, Solovyev V, Wei Z, Whittaker CA, Worley K, Durbin KJ, Shen Y, Fedrigo O, Garfield D, Haygood R, Primus A, Satija R, Severson T, Gonzalez-Garay ML, Jackson AR, Milosavljevic A, Tong M, Killian CE, Livingston BT, Wilt FH, Adams N, Belle R, Carbonneau S, Cheung R, Cormier P, Cosson B, Croce J, Fernandez-Guerra A, Geneviere AM, Goel M, Kelkar H, Morales J, Mulner-Lorillon O, Robertson AJ, Goldstone JV, Cole B, Epel D, Gold B, Hahn ME, Howard-Ashby M, Scally M, Stegeman JJ, Allgood EL, Cool J, Judkins KM, McCafferty SS, Musante AM, Obar RA, Rawson AP, Rossetti BJ, Gibbons IR, Hoffman MP, Leone A, Istrail S, Materna SC, Samanta MP, Stolc V, Tongprasit W, Tu Q, Bergeron KF, Brandhorst BP, Whittle J, Berney K, Bottjer DJ, Calestani C, Peterson K, Chow E, Yuan QA, Elhaik E, Graur D, Reese JT, Bosdet I, Heesun S, Marra MA, Schein J, Anderson MK, Brockton V, Buckley KM, Cohen AH, Fugmann SD, Hibino T, Loza-Coll M, Majeske AJ, Messier C, Nair SV, Pancer Z, Terwilliger DP, Agca C, Arboleda E, Chen N, Churcher AM, Hallbook F, Humphrey GW, Idris MM, Kiyama T, Liang S, Mellott D, Mu X, Murray G, Olinski RP, Raible F, Rowe M, Taylor JS, Tessmar-Raible K, Wang D, Wilson KH, Yaguchi S, Gaasterland T, Galindo BE, Gunaratne HJ, Juliano C, Kinukawa M, Moy GW, Neill AT, Nomura M, Raisch M, Reade A, Roux MM, Song JL, Su YH, Townley IK, Voronina E, Wong JL, Amore G, Branno M, Brown ER, Cavalieri V, Duboc V, Duloquin L, Flytzanis C, Gache C, Lapraz F, Lepage T, Locascio A, Martinez P, Matassi G, Matranga V, Range R, Rizzo F, Rottinger E, Beane W, Bradham C, Byrum C, Glenn T, Hussain S, Manning G, Miranda E, Thomason R, Walton K, Wikramanayke A, Wu SY, Xu R, Brown CT, Chen L, Gray RF, Lee PY, Nam J, Oliveri P, Smith J, Muzny D, Bell S, Chacko J, Cree A, Curry S, Davis C, Dinh H, Dugan-Rocha S, Fowler J, Gill R, Hamilton C, Hernandez J, Hines S, Hume J, Jackson L, Jolivet A, Kovar C, Lee S, Lewis L, Miner G, Morgan M, Nazareth LV, Okwuonu G, Parker D, Pu LL, Thorn R, Wright R (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952CrossRefPubMedCentralGoogle Scholar
  80. Shah M, Brown KM, Smith LC (2003) The gene encoding the sea urchin complement protein, SpC3, is expressed in embryos and can be upregulated by bacteria. Dev Comp Immunol 27:529–538CrossRefPubMedGoogle Scholar
  81. Silva JR (2000) The onset of phagocytosis and identity in the embryo of Lytechinus variegatus. Dev Comp Immunol 24:733–739CrossRefPubMedGoogle Scholar
  82. Smith LC, Arizza V, Barela Hudgell MA, Barone G, Bodnar AG, Buckley KM, Cunsolo V, Dheilly NM, Franchi N, Fugmann SD, Furukawa R, Garcia-Arraras J, Henson JH, Hibino T, Irons ZH, Li C, Lun CM, Majeske AJ, Oren M, Pagliara P, Pinsino A, Raftos, DA, Rast JP, Samasa B, Schillaci D, Schrankel CS, Stabili L, Stensväg K, Sutton E (2018) The complex immune system in echinoderms. Springer (in press)Google Scholar
  83. Smith MM, Smith LC, Cameron RA, Urry LA (2008) The larval stages of the sea urchin, Strongylocentrotus purpuratus. J Morphol 269:713–733CrossRefPubMedGoogle Scholar
  84. Solek CM, Oliveri P, Loza-Coll M, Schrankel CS, Ho ECH, Wang GZ, Rast JR (2013) An ancient role for Gata-1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol 382:280–292CrossRefPubMedGoogle Scholar
  85. Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea-urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986CrossRefPubMedGoogle Scholar
  86. Sutherby J, Giardini JL, Nguyen J, Wessel G, Leguia M, Heyland A (2012) Histamine is a modulator of metamorphic competence in Strongylocentrotus purpuratus (Echinodermata: Echinoidea). BMC Dev Biol 12:14CrossRefPubMedPubMedCentralGoogle Scholar
  87. Swanson RL, Williamson JE, De Nys R, Kumar N, Bucknall MP, Steinberg PD (2004) Induction of settlement of larvae of the sea urchin Holopneustes purpurascens by histamine from a host alga. Biol Bull 206:161–172CrossRefPubMedGoogle Scholar
  88. Swanson RL, de Nys R, Huggett MJ, Green JK, Steinberg PD (2006) In situ quantification of a natural settlement cue and recruitment of the Australian sea urchin Holopneustes purpurascens. Marine Ecology Progress Series 314:1–14CrossRefGoogle Scholar
  89. Swanson RL, Byrne M, Prowse TAA, Mos B, Dworjanyn SA, Steinberg PD (2012) Dissolved histamine: a potential habitat marker promoting settlement and metamorphosis in sea urchin larvae. Mar Biol 159:915–925CrossRefGoogle Scholar
  90. Tabarean IV (2016) Histamine receptor signaling in energy homeostasis. Neuropharmacology 106:13–19CrossRefPubMedGoogle Scholar
  91. Tamboline CR, Burke RD (1992) Secondary mesenchyme of the sea urchin embryo: ontogeny of blastocoelar cells. J Exp Zool 262:51–60CrossRefPubMedGoogle Scholar
  92. Tata JR (1996) Metamorphosis: an exquisite model for hormonal regulation of post-embryonic development. Biochem Soc Symp:123–136Google Scholar
  93. Tauber AI (2003) Metchnikoff and the phagocytosis theory. Nat Rev Mol Cell Bio 4:897–901CrossRefGoogle Scholar
  94. Taylor E, Heyland A (2017) Evolution of thyroid hormone signaling in animals: non-genomic and genomic modes of action. Mol Cell Endocrinol 459:14–20CrossRefPubMedGoogle Scholar
  95. Taylor E, Wynen H, Heyland A (in review) Thyroid hormone exposure of sea urchin embryos and larvae leads to acceleration of skeletogenesis. Front EndoGoogle Scholar
  96. Tu Q, Cameron RA, Davidson EH (2014) Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus. Dev Biol 385:160–167CrossRefPubMedGoogle Scholar
  97. Unkles SE (1977) Bacterial flora of the sea urchin Echinus esculentus. Appl Env Microbiol 34:347–350Google Scholar
  98. Vaughn D, Strathmann RR (2008) Predators induce cloning in echinoderm larvae. Science 319:1503CrossRefPubMedGoogle Scholar
  99. Vickery MS, McClintock JB (1998) Regeneration in metazoan larvae. Nature 394:140–140CrossRefGoogle Scholar
  100. Vickery MCL, Vickery MS, Amsler CD, McClintock JB (1999a) Characterization of novel genes expressed during regeneration in larval sea stars. Am Zool 39:51aGoogle Scholar
  101. Vickery MS, Vickery MCL, McClintock JB (1999b) Regeneration in echinoid larvae. Am Zool 39:50a–51aGoogle Scholar
  102. Vickery MCL, Vickery MS, Amsler CD, McClintock JB (2001a) Regeneration in echinoderm larvae. Microsc Res Tech 55:464–473CrossRefPubMedGoogle Scholar
  103. Vickery MCL, Vickery MS, McClintock JB, Amsler CD (2001b) Utilization of a novel deuterostome model for the study of regeneration genetics: molecular cloning of genes that are differentially expressed during early stages of larval sea star regeneration. Gene 262:73–80CrossRefPubMedGoogle Scholar
  104. Williams EA, Carrier TJ (2018) An -omics perspective on marine invertebrate larvae. In: Carrier T, Reitzel A, Heyland A (eds) Evolutionary ecology of marine invertebrate larvae. Oxford University Press, Oxford, pp 284–300Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Andreas Heyland
    • 1
    Email author
  • Nicholas Schuh
    • 1
    • 2
  • Jonathan Rast
    • 2
    • 3
  1. 1.Integrative BiologyUniversity of GuelphGuelphCanada
  2. 2.Department of Medical BiophysicsUniversity of TorontoTorontoCanada
  3. 3.Department of Pathology and Laboratory MedicineEmory University School of MedicineAtlantaUSA

Personalised recommendations