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On the larva and the zooid of the pterobranch Rhabdopleura recondita Beli, Cameron and Piraino, 2018 (Hemichordata, Graptolithina)

  • F. Strano
  • V. Micaroni
  • E. Beli
  • S. Mercurio
  • G. Scarì
  • R. Pennati
  • S. Piraino
Original Paper
  • 40 Downloads

Abstract

Hemichordates (Enteropneusta and Pterobranchia) belong to a small deuterostome invertebrate group that may offer insights on the origin and evolution of the chordate nervous system. Among them, the colonial pterobranch Rhabdopleuridae are recognized as living representatives of Graptolithina, a taxon with a rich fossil record. New information is provided here on the substrate selection and the life cycle of Rhabdopleura recondita Beli, Cameron and Piraino, 2018, and for the first time, we describe the nervous system organization of the larva and the adult zooid, as well as the morphological, neuroanatomical and behavioural changes occurring throughout metamorphosis. Immunohistochemical analyses disclosed a centralized nervous system in the sessile adult zooid, characterized by different neuronal subsets with three distinct neurotransmitters, i.e. serotonin, dopamine and RFamide. The peripheral nervous system comprises GABA-, serotonin-, and dopamine-immunoreactive cells. These observations support and integrate previous neuroanatomical findings on the pterobranch zooid of Cephalodiscus gracilis. Indeed, this is the first evidence of dopamine, RFamide and GABA neurotransmitters in hemichordates pterobranchs. In contrast, the lecithotrophic larva is characterized by a diffuse basiepidermal plexus of GABAergic cells, coupled with a small group of serotonin-immunoreactive cells localized in the characteristic ventral depression. It is envisaged the use of R. recondita as a novel and easily accessible hemichordate model organism to shed light on the evolution of hemichordates and more generally on the origin of deuterostome developmental mechanisms.

Keywords

Pterobranchia Life cycle Nervous system Neurotransmitter Development Metamorphosis 

Notes

Acknowledgements

Special thanks to Silvia Messinetti, University of Milan, for laboratory support and to Ittiturismo Anime Sante (Tricase), DWD Diving (Diso), Giorgio Aglieri, and Christian Vaglio that helped us in sampling procedures. The in vivo observations were made at the laboratory of the Avamposto MARE, Tricase Porto (Lecce), in the framework of the project Biodiversity MARE Tricase (http://www.biodiversitymaretricase.org/). The authors thank Prof. Cameron and Prof Maletz for the intensive and fruitful revision of the manuscript.

Compliance with ethical standards

Ethical approval

All applicable international, national, and institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities.

References

  1. Arenas-Mena C (2010) Indirect development, transdifferentiation and the macroregulatory evolution of metazoans. Philos Trans R Soc Lond Ser B Biol Sci 365(1540):653–669.  https://doi.org/10.1098/rstb.2009.0253 CrossRefGoogle Scholar
  2. Arendt D, Denes AS, Jékely G, Tessmar-Raible K (2008) The evolution of nervous system centralization. Philos Trans R Soc Lond Ser B Biol Sci 363:1523–1528.  https://doi.org/10.1098/rstb.2007.2242 CrossRefGoogle Scholar
  3. Azmitia EC (2001) Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res Bull 56(5):413–424.  https://doi.org/10.1016/s0361-9230(01)00614-1 CrossRefPubMedGoogle Scholar
  4. Balser EJ, Ruppert EE (1990) Structure, ultrastructure and function of the preoral heart-kidney in Saccoglossus kowalevskii (Hemichordata, Enteropneusta) including new data on the stomochord. Acta Zool 71(4): 235-249Google Scholar
  5. Bateson W (1884) Note on the later stages in the development of Balanoglossus kowalevskii (Agassiz), and on the affinities of the Enteropneusta. Proc R Soc Lond B Biol Sci 38:23–30Google Scholar
  6. Bateson W (1885) Memoirs: the later stages in the development of Balanoglossus Kowalevskii, with a suggestion as to the affinities of the Enteropneusta. J Cell Sci 2(S1):81–122.  https://doi.org/10.1098/rspl.1884.0058 CrossRefGoogle Scholar
  7. Beli E, Aglieri G, Strano F, Maggioni D, Telford MJ, Piraino S, Cameron CB (2018) The zoogeography of extant rhabdopleurid hemichordates (Pterobranchia: Graptolithina), with a new species from the Mediterranean Sea. Invertebr Syst 32(1):100–110.  https://doi.org/10.1071/IS17021 CrossRefGoogle Scholar
  8. Benito J, Pardos F (1997) Hemichordata. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates. Wiley, Liss, pp 15–102Google Scholar
  9. Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Kohn AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85.  https://doi.org/10.1038/nature05241 CrossRefPubMedGoogle Scholar
  10. Brown FD, Prendergast A, Swalla BJ (2008) Man is but a worm: chordate origins. Genesis 46(11):605–613.  https://doi.org/10.1002/dvg.20471 CrossRefPubMedGoogle Scholar
  11. Bullock TH (1945) The anatomical organization of the nervous system of Enteropneusta. Q J Microsc Sci 86:55–111PubMedGoogle Scholar
  12. Burke RD (2011) Deuterostome neuroanatomy and the body plan paradox. Evol Dev 13(1):110–115.  https://doi.org/10.1111/j.1525-142X.2010.00460.x CrossRefPubMedGoogle Scholar
  13. Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 9(5):432–445.  https://doi.org/10.1111/j.1525-142X.2007.00189.x CrossRefPubMedGoogle Scholar
  14. Cameron CB (2018) Treatise on invertebrate paleontology, part V, chapter 2, class Enteropneusta: introduction, morphology, life habits, systematic descriptions, and future research. Treatise Online 109:1–22Google Scholar
  15. Cameron CB, Mackie GO (1996) Conduction pathways in the nervous system of Saccoglossus sp. (Enteropneusta). Can J Zool 74(1):15–19.  https://doi.org/10.1139/z96-003 CrossRefGoogle Scholar
  16. Cannon JT, Rychel AL, Eccleston H, Halanych KM, Swalla BJ (2009) Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Mol Phylogenetics Evol 52(1):17–24.  https://doi.org/10.1016/j.ympev.2009.03.027 CrossRefGoogle Scholar
  17. Couper JM, Leise EM (1996) Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol Bull 191(2):178–186.  https://doi.org/10.2307/1542921 CrossRefPubMedGoogle Scholar
  18. D’Aniello S, Delroisse J, Valero-Gracia A, Lowe EK, Byrne M, Cannon JT, Halanych KM, Elphick MR, Mallefet J, Kaul-Strehlow S, Lowe CJ, Flammang P, Ullrich-Lüter E, Wanninger A, Arnone MI (2015) Opsin evolution in the Ambulacraria. Mar Genomics 24:177–183.  https://doi.org/10.1016/j.margen.2015.10.001 CrossRefPubMedGoogle Scholar
  19. Dilly PN (1972) The structures of the tentacles of Rhabdopleura compacta (Hemichordata) with special reference to neurociliary control. Z Zellforch Microsk Anat Histochem 129(1):20–39.  https://doi.org/10.1007/bf00307107 CrossRefGoogle Scholar
  20. Dilly PN (1973) The larva of Rhabdopleura compacta (Hemichordata). Mar Biol 18(1):69–86.  https://doi.org/10.1007/bf00347923 CrossRefGoogle Scholar
  21. Dilly PN (1975) The pterobranch Rhabdopleura compacta: its nervous system and phylogenetic position. Symp Zool Soc London 36:1–16Google Scholar
  22. Dilly PN (1986) Modern pterobranchs: observations on their behaviour and tube building. Geol Soc 20:261–269.  https://doi.org/10.1144/GSL.SP.1986.020.01.27 CrossRefGoogle Scholar
  23. Dilly PN (1988) Tube building by Cephalodiscus gracilis. J Zool 216:465–468.  https://doi.org/10.1111/j.1469-7998.1988.tb02442.x CrossRefGoogle Scholar
  24. Dilly PN (2014) Cephalodiscus reproductive biology (Pterobranchia, Hemichordata). Acta Zool 95(1):111–124.  https://doi.org/10.1111/azo.12015 CrossRefGoogle Scholar
  25. Fan TP, Su YH (2015) FGF signaling repertoire of the indirect developing hemichordate Ptychodera flava. Mar Genomics 24:167–175.  https://doi.org/10.1016/j.margen.2015.07.006 CrossRefPubMedGoogle Scholar
  26. Garstang W (1894) Preliminary note on a new theory of the phylogeny of the Chordata. Zool Anz 17:122–125Google Scholar
  27. Gemmill JF (1914) The Development and Certain Points in the Adult Structure of the Starfish Asterias rubens, L. Philosophical Transactions of the Royal Society B: Biological Sciences 205 (313-324):213-294Google Scholar
  28. Hadfield MG (1975) Hemichordata. Reproduction of Marine Invertebrates. New York: Academic Press 2:185-240Google Scholar
  29. Halanych KM (1993) Suspension feeding by the lophophore-like apparatus of the pterobranch hemichordate Rhabdopleura normani. Biol Bull 185(3):417–427.  https://doi.org/10.2307/1542482 CrossRefPubMedGoogle Scholar
  30. Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B Biol Sci 267:1071–1079.  https://doi.org/10.1098/rspb.2000.1111 CrossRefGoogle Scholar
  31. Holland ND (2003) Early central nervous system evolution: an era of skin brains? Nat Rev Neurosci 4(8):617–627.  https://doi.org/10.1038/nrn1175 CrossRefPubMedGoogle Scholar
  32. Kaul S, Stach T (2010) Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. J Morphol 271(10):1240–1259.  https://doi.org/10.1002/jmor.10868 CrossRefPubMedGoogle Scholar
  33. Kaul-Strehlow S, Röttinger E (2015) In: Wanninger A (ed) Evolutionary developmental biology of invertebrates 6: Deuterostomia. Springer, Berlin, pp 59–90CrossRefGoogle Scholar
  34. Kaul-Strehlow S, Urata M, Praher D, Wanninger A (2017) Neuronal patterning of the tubular collar cord is highly conserved among enteropneusts but dissimilar to the chordate neural tube. Sci Rep 7(1):7003.  https://doi.org/10.1038/s41598-017-07052-8 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Knight-Jones EW (1952) On the nervous system of Saccoglossus cambrensis (Enteropneusta). Philos Trans R Soc Lond Ser B Biol Sci 236:315–354.  https://doi.org/10.1098/rstb.1952.0004 CrossRefGoogle Scholar
  36. Lester SM (1988a) Settlement and metamorphosis of Rhabdopleura normani (Hemichordata: Pterobranchia). Acta Zool 69(2):111–120.  https://doi.org/10.1111/j.1463-6395.1988.tb00907.x CrossRefGoogle Scholar
  37. Lester SM (1988b) Ultrastructure of adult gonads and development and structure of the larva of Rhabdopleura normani (Hemichordata: Pterobranchia). Acta Zool 69(2):95–109.  https://doi.org/10.1111/j.1463-6395.1988.tb00906.x CrossRefGoogle Scholar
  38. Maletz J (2014a) The classification of the Pterobranchia (Cephalodiscida and Graptolithina). B Geosci 89(3):477–540.  https://doi.org/10.3140/bull.geosci.1465 CrossRefGoogle Scholar
  39. Maletz J (2014b) Hemichordata (Pterobranchia, Enteropneusta) and the fossil record. Palaeogeogr Palaeoclimatol Palaeoecol 398:16–27.  https://doi.org/10.1016/j.palaeo.2013.06.010 CrossRefGoogle Scholar
  40. Maletz J, Cameron CB (2016) Treatise on invertebrate paleontology, part V, chapter 3: introduction to class Pterobranchia Lankester, 1877. Treatise Online 82:1–15Google Scholar
  41. Maletz J, Steiner M (2015) Graptolite (Hemichordata, Pterobranchia) preservation and identification in the Cambrian Series 3. Palaeontology 58(6):1073–1107.  https://doi.org/10.1111/pala.12200 CrossRefGoogle Scholar
  42. Micaroni V, Strano F, Di Franco D, Crocetta F, Grech D, Piraino S, Boero F (2018a) Project “Biodiversity MARE Tricase”: a biodiversity inventory of the coastal area of Tricase (Ionian Sea, Italy)–Mollusca: Heterobranchia. Eur Zool J 85(1):180–193.  https://doi.org/10.1080/24750263.2018.1462413 CrossRefGoogle Scholar
  43. Micaroni V, Strano F, Di Franco D, Langeneck J, Gravili C, Bertolino M, Costa G, Rindi F, Froglia C, Crocetta F, Giangrande A, Nicoletti L, Medagli P, Zuccarello V, Arzeni S, Bo M, Betti F, Mastrototaro F, Lattanzi L, Piraino S, Boero F (2018b) Project “Biodiversity MARE Tricase”: biodiversity research, monitoring and promotion at MARE Outpost (Apulia, Italy). Rend Lincei-Sci Fis Nat 29(3):599–604.  https://doi.org/10.1007/s12210-018-0726-3 CrossRefGoogle Scholar
  44. Mitchell CE, Melchin MJ, Cameron CB, Maletz J (2013) Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia 46(1):34–56.  https://doi.org/10.1111/j.1502-3931.2012.00319.x CrossRefGoogle Scholar
  45. Nezlin LP, Yushin VV (2004) Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology 123(1):1–13CrossRefGoogle Scholar
  46. Nielsen C (2012) Animal evolution: interrelationships of the living phyla. Oxford University Press, OxfordGoogle Scholar
  47. Nomaksteinsky M, Röttinger E, Dufour HD, Chettouh Z, Lowe CJ, Martindale MQ, Brunet JF (2009) Centralization of the deuterostome nervous system predates chordates. Curr Biol 19(15):1264–1269.  https://doi.org/10.1016/j.cub.2009.05.063 CrossRefPubMedGoogle Scholar
  48. Novosel M (2005) Bryozoans of the Adriatic Sea. Denisia 16:231–246Google Scholar
  49. Osugi T, Son YL, Ubuka T, Satake H, Tsutsui K (2016) RFamide peptides in agnathans and basal chordates. Gen Comp Endocrinol 227:94–100.  https://doi.org/10.1016/j.ygcen.2015.06.012 CrossRefPubMedGoogle Scholar
  50. Pennati R, Dell’Anna A, Zega G, De Bernardi F (2012) Immunohistochemical study of the nervous system of the tunicate Thalia democratica (Forsskal, 1775). Eur J Histochem 56(2):16.  https://doi.org/10.4081/ejh.2012.e16 CrossRefGoogle Scholar
  51. Peterson KJ, Cameron RA, Davidson EH (1997) Set aside cells in maximal indirect development: evolutionary and developmental significance. BioEssays 19(7):623–631.  https://doi.org/10.1002/bies.950190713 CrossRefPubMedGoogle Scholar
  52. Pickens PE (1970) Conduction along the ventral nerve cord of a hemichordate worm. J Exp Biol 53:515-528Google Scholar
  53. Rehkämper G, Welsch U, Dilly PN (1987) Fine structure of the ganglion of Cephalodiscus gracilis (Pterobranchia, Hemichordata). J Comp Neurol 259(2):308–315.  https://doi.org/10.1002/cne.902590210 CrossRefPubMedGoogle Scholar
  54. Röttinger E, Lowe CJ (2012) Evolutionary crossroads in developmental biology: hemichordates. Development 139(14):2463–2475.  https://doi.org/10.1242/dev.066712 CrossRefPubMedGoogle Scholar
  55. Sato A (2008) Seasonal reproductive activity in the pterobranch hemichordate Rhabdopleura compacta. J Mar Biol Assoc UK 88(5):1033–1041.  https://doi.org/10.1017/S0025315408001604 CrossRefGoogle Scholar
  56. Sato A, Bishop JD, Holland PW (2008a) Developmental biology of pterobranch hemichordates: history and perspectives. Genesis 46(11):587–591.  https://doi.org/10.1002/dvg.20395 CrossRefPubMedGoogle Scholar
  57. Sato A, Rickards B, Holland PW (2008b) The origins of graptolites and other pterobranchs: a journey from ‘Polyzoa’. Lethaia 41(4):303–316.  https://doi.org/10.1111/j.1502-3931.2008.00123.x CrossRefGoogle Scholar
  58. Satoh N, Rokhsar D, Nishikawa T (2014a) Chordate evolution and the three-phylum system. Proc R Soc B 281:20141729.  https://doi.org/10.1098/rspb.2014.1729 CrossRefPubMedGoogle Scholar
  59. Satoh N, Tagawa K, Lowe CJ, Yu JK, Kawashima T, Takahashi H, Ogasawara M, Kirschner M, Hisata K, Su YH, Gerhart J (2014b) On a possible evolutionary link of the stomochord of hemichordates to pharyngeal organs of chordates. Genesis 52(12):925–934.  https://doi.org/10.1002/dvg.22831 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, Hisata K, Bredeson J, Shoguchi E, Gyoja F, Yue J, Chen Y, Freeman RM, Sasaki A, Hikosaka-Katayama T, Sato A, Fujie M, Baughman KW, Levine J, Gonzalez P, Cameron C, Fritzenwanker JH, Pani AM, Goto H, Kanda M, Arakaki N, Yamasaki S, Qu J, Cree A, Ding Y, Dinh HH, Dugan S, Holder M, Jhangiani SM, Kovar CL, Lee SL, Lewis LR, Morton D, Nazareth LV, Okwuonu G, Santibanez J, Chen R, Richards S, Muzny DM, Gillis A, Peshkin L, Wu M, Humphreys T, Su Y, Putnam NH, Schmutz J, Fujiyama A, Yu J, Tagawa K, Worley KC, Gibbs RA, Kirschner MW, Lowe CJ, Satoh N, Rokhsar DS, Gerhart J (2015) Hemichordate genomes and deuterostome origins. Nature 527(7579):459.  https://doi.org/10.1038/nature16150 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Smith AB (2008) Deuterostomes in a twist: the origins of a radical new body plan. Evol Dev 10(4):493–503.  https://doi.org/10.1111/j.1525-142X.2008.00260.x CrossRefPubMedGoogle Scholar
  62. Stach T, Gruhl A, Kaul-Strehlow S (2012) The central and peripheral nervous system of Cephalodiscus gracilis (Pterobranchia, Deuterostomia). Zoomorphology 131(1):11–24.  https://doi.org/10.1007/s00435-011-0144-x CrossRefGoogle Scholar
  63. Stebbing ARD (1970) Aspects of the reproduction and life cycle of Rhabdopleura compacta (Hemichordata). Mar Biol 5(3):205–212.  https://doi.org/10.1007/bf00346908 CrossRefGoogle Scholar
  64. Stebbing ARD, Dilly PN (1972) Some observations on living Rhabdopveura Compacta (Hemichordata). J Mar Biol Assoc U.K 52(2):443–448.  https://doi.org/10.1017/S0025315400018804 CrossRefGoogle Scholar
  65. Tagawa K (2016) Hemichordate models. Curr Opin Genet Dev 39:71–78.  https://doi.org/10.1016/j.gde.2016.05.023 CrossRefPubMedGoogle Scholar
  66. Tassia MG, Cannon JT, Konikoff CE, Shenkar N, Halanych KM, Swalla BJ (2016) The global diversity of Hemichordata. PLoS One 11(10):0162564.  https://doi.org/10.1371/journal.pone.0162564 CrossRefGoogle Scholar
  67. Verlinden H (2018) Dopamine signalling in locusts and other insects. Insect biochemistry and molecular biology. Insect Biochem Mol Biol 97:40–52.  https://doi.org/10.1016/j.ibmb.2018.04.005 CrossRefPubMedGoogle Scholar

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© Senckenberg Gesellschaft für Naturforschung 2019

Authors and Affiliations

  1. 1.Department of Life SciencesUniversity of TriesteTriesteItaly
  2. 2.Department of Biology and Evolution of Marine OrganismsStazione Zoologica Anton Dohrn NapoliNaplesItaly
  3. 3.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  4. 4.Department of Biological and Environmental Sciences and TechnologiesUniversity of SalentoLecceItaly
  5. 5.Département de Sciences BiologiquesUniversité de MontréalMontrealCanada
  6. 6.Department of Environmental Science and PolicyUniversity of MilanMilanItaly
  7. 7.Department of BioscienceUniversity of MilanMilanItaly
  8. 8.National Inter-University Consortium for Marine SciencesRomeItaly

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