Abstract
Arthropod early neurogenesis shows distinct patterns that have been interpreted in an evolutionary framework. For instance, crustaceans and Hexapoda form the taxon Tetraconata and share the differentiation of specific neural precursors, the neuroblasts, a character which sets them apart from Chelicerata and Myriapoda. Neuroblasts are relatively large stem cells that generate ganglion mother cells by asymmetric divisions. Ganglion mother cells typically divide once to give rise to neurons and glia cells. In hexapods, neuroblasts segregate from the neuroectoderm before they begin their characteristic proliferative activity. In the crustaceans studied so far, neuroblasts remain in the neuroectoderm. Yet, detailed studies on early neurogenesis of crustaceans at the cellular level are largely restricted to some malacostracan and branchiopod species. Crustaceans are very diverse and likely paraphyletic with respect to hexapods. Hence, knowledge about neural differentiation in other crustacean taxa might contribute to the understanding of evolution of neurogenesis in Tetraconata. Here, we describe the early neurogenesis during naupliar development of the copepod Tigriopus californicus. We show that neuroblasts are present that generate ganglion mother cells, which in turn divide to give rise to neurons of the ventral nerve cord. These two neural precursor cell types and their specific arrangement correspond to what has been found in other crustaceans. One obvious difference concerns the relative size of the neuroblasts, which are not much larger than their progeny. Our results complement the picture of neural differentiation in crustaceans and suggest that superficially located neuroblasts are likely the ancestral condition in Tetraconata.
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References
Andrew DR, Brown SM, Strausfeld NJ (2012) The minute brain of the copepod Tigriopus californicus supports a complex ancestral ground pattern of the tetraconate cerebral nervous systems. J Comp Neurol 520:3446–3470. https://doi.org/10.1002/cne.23099
Bate CM (1976) Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. J Embryol Exp Morphol 35:107–123
Bergh RS (1893) Beiträge zur Embryologie der Crustaceen. I. Zur Bildungsgeschichte des Keimstreifens von Mysis. Zool Jb Anat 6:491–528
Biffar L, Stollewerk A (2014) Conservation and evolutionary modifications of neuroblast expression patterns in insects. Dev Biol 388:103–116. https://doi.org/10.1016/j.ydbio.2014.01.028
Biffis C (2017) Comparative studies in the development of the nervous system in malacostracan crustaceans. Humboldt University Berlin, Dissertation
Blanchard CE (1986) Early development of the thorax and the nervous system of the brine shrimp Artemia. University of Leicester, Dissertation
Bossing T, Udolph G, Doe CQ, Technau GM (1996) The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 179:41–64. https://doi.org/10.1006/dbio.1996.0240
Brenneis G, Stollewerk A, Scholtz G (2013) Embryonic neurogenesis in Pseudopallene sp. (Arthropoda, Pycnogonida) includes two subsequent phases with similarities to different arthropod groups. EvoDevo 4:32. https://doi.org/10.1186/2041-9139-4-32
Dahms HU, Chullasorn S, Kangtia P et al (2007) Naupliar development of Tigriopus japonicus Mori, 1932 (Copepoda: Harpacticidae). Zool Stud 46:746–759
Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205. https://doi.org/10.1016/0012-1606(85)90445-2
Dohle W (1976) Die Bildung und Differenzierung des postnauplialen Keimstreifs von Diastylis rathkei (Crustacea, Cumacea). Zoomorphologie 84:235–277. https://doi.org/10.1007/BF01578696
Dohle W (2001) Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name “Tetraconata” for the monophyletic unit Crustacea + Hexapoda. Ann Soc Entomol Fr 37:85–103
Dohle W, Scholtz G (1988) Clonal analysis of the crustacean segment: the discordance between genealogical and segmental borders. Development 104:147 LP–147160
Dove H, Stollewerk A (2003) Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development 130:2161–2171. https://doi.org/10.1242/dev.00442
Duman-Scheel M, Patel NH (1999) Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126:2327–2334
Fabritius-Vilpoux K, Bisch-Knaden S, Harzsch S (2008) Engrailed-like immunoreactivity in the embryonic ventral nerve cord of the marbled crayfish (Marmorkrebs). Invertebr Neurosci 8:177–197. https://doi.org/10.1007/s10158-008-0081-7
Fischer AHL, Scholtz G (2010) Axogenesis in the stomatopod crustacean Gonodactylaceus falcatus (Malacostraca). Invertebr Biol 129:59–76. https://doi.org/10.1111/j.1744-7410.2010.00192.x
Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1–22. https://doi.org/10.1016/0168-9525(89)90120-0
Foley BR, Rose CG, Rundle DE, Leong W, Edmands S (2013) Postzygotic isolation involves strong mitochondrial and sex-specific effects in Tigriopus californicus, a species lacking heteromorphic sex chromosomes. Heredity (Edinb) 111:391–401. https://doi.org/10.1038/hdy.2013.61
Fuse N, Hisata K, Katzen AL, Matsuzaki F (2003) Heterotrimeric G proteins regulate daughter cell size asymmetry in Drosophila neuroblast divisions. Curr Biol 13:947–954. https://doi.org/10.1016/S0960-9822(03)00334-8
Gerberding M (1997) Germ band formation and early neurogenesis of Leptodora kindti (Cladocera): first evidence for neuroblasts in the entomostracan crustaceans. Invertebr Reprod Dev 32:63–73. https://doi.org/10.1080/07924259.1997.9672605
Gerberding M, Scholtz G (2001) Neurons and glia in the midline of the higher crustacean Orchestia cavimana are generated via an invariant cell lineage that comprises a median neuroblast and glial progenitors. Dev Biol 235:397–409. https://doi.org/10.1006/dbio.2001.0302
Giribet G, Edgecombe GD (2012) Reevaluating the arthropod tree of life. Annu Rev Entomol 57:167–186. https://doi.org/10.1146/annurev-ento-120710-100659
Glenner H, Thomsen PF, Hebsgaard MB, Sorensen MV, Willerslev E (2006) Evolution. The origin of insects. Science 314:1883–1884. https://doi.org/10.1126/science.1129844
Hartenstein V, Campos-Ortega JA (1984) Early neurogenesis in wild-type Drosophila melanogaster. Wilhelm Roux’s Arch Dev Biol 193:308–325. https://doi.org/10.1007/BF00848159
Hartenstein V, Stollewerk A (2015) The evolution of early neurogenesis. Dev Cell 32:390–407. https://doi.org/10.1016/j.devcel.2015.02.004
Hartenstein V, Younossi-Hartenstein A, Lekven A (1994) Delamination and division in the Drosophila neurectoderm: spatiotemporal pattern, cytoskeletal dynamics, and common control by neurogenic and segment polarity genes. Dev Biol 165:480–499. https://doi.org/10.1006/dbio.1994.1269
Harzsch S (2001) Neurogenesis in the crustacean ventral nerve cord: homology of neuronal stem cells in Malacostraca and Branchiopoda? Evol Dev 3:154–169. https://doi.org/10.1046/j.1525-142x.2001.003003154.x
Harzsch S (2006) Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny. Integr Comp Biol 46:162–194. https://doi.org/10.1093/icb/icj011
Harzsch S, Dawirs RR (1994) Neurogenesis in larval stages of the spider crab Hyas araneus (Decapoda, Brachyura): proliferation of neuroblasts in the ventral nerve cord. Roux’s Arch Dev Biol Off Organ EDBO 204:93–100. https://doi.org/10.1007/BF00361103
Harzsch S, Miller J, Benton J et al (1998) Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. J Exp Biol 201:2465–2479
Kitajima A, Fuse N, Isshiki T, Matsuzaki F (2010) Progenitor properties of symmetrically dividing Drosophila neuroblasts during embryonic and larval development. Dev Biol 347:9–23. https://doi.org/10.1016/j.ydbio.2010.06.029
Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA (1996) Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383:50–55
Lacalli TC (2009) Serial EM analysis of a copepod larval nervous system: naupliar eye, optic circuitry, and prospects for full CNS reconstruction. Arthropod Struct Dev 38:361–375. https://doi.org/10.1016/j.asd.2009.04.002
McMurrich JP (1895) Embryology of the isopod crustacea. J Morphol 11:63–154. https://doi.org/10.1002/jmor.1050110103
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspock U, Aspock H, Bartel D, Blanke A, Berger S, Bohm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schutte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TKF, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767. https://doi.org/10.1126/science.1257570
Müller HAJ, Wieschaus E (1996) Armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J Cell Biol 134:149–163. https://doi.org/10.1083/jcb.134.1.149
Oakley TH, Wolfe JM, Lindgren AR, Zaharoff AK (2013) Phylotranscriptomics to bring the understudied into the fold: monophyletic ostracoda, fossil placement, and pancrustacean phylogeny. Mol Biol Evol 30:215–233. https://doi.org/10.1093/molbev/mss216
Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW, Cunningham CW (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463:1079–1083. https://doi.org/10.1038/nature08742
Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Döring C, Faller S, Fritsch M, Grobe P, Heuer CM, Kaul S, Møller OS, Müller CHG, Rieger V, Rothe BH, Stegner MEJ, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29. https://doi.org/10.1186/1742-9994-7-29
Scholtz G (1990) The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peracarida). Proc R Soc B Biol Sci 239:163–211. https://doi.org/10.1098/rspb.1990.0013
Scholtz G (1992) Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation, and early neurogenesis. Roux’s Arch Dev Biol 202:36–48. https://doi.org/10.1007/BF00364595
Schwentner M, Combosch DJ, Pakes Nelson J, Giribet G (2017) A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships. Curr Biol 27:1818–1824. https://doi.org/10.1016/j.cub.2017.05.040
Stegner MEJ, Richter S (2015) Development of the nervous system in Cephalocarida (Crustacea): early neuronal differentiation and successive patterning. Zoomorphology 134:183–209. https://doi.org/10.1007/s00435-014-0248-1
Stollewerk A, Weller M, Tautz D (2001) Neurogenesis in the spider Cupiennius salei. Dev Genes Evol 211:76–82. https://doi.org/10.1007/s004270000121
Strausfeld NJ, Andrew DR (2011) A new view of insect-crustacean relationships I. Inferences from neural cladistics and comparative neuroanatomy. Arthropod Struct Dev 40:276–288. https://doi.org/10.1016/j.asd.2011.02.002
Tamarelle M, Haget A, Ressouches A (1985) Segregation, division, and early patterning of lateral thoracic neuroblasts in the embryos of Carausius morosus Br. (Phasmida: Lonchodidae). Int J Insect Morphol Embryol 14:307–317. https://doi.org/10.1016/0020-7322(85)90045-5
Truman JW, Ball EE (1998) Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects. Dev Genes Evol 208:357–368
Ungerer P, Scholtz G (2008) Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata. Proc Biol Sci 275:369–376. https://doi.org/10.1098/rspb.2007.1391
Ungerer P, Eriksson BJ, Stollewerk A (2011) Neurogenesis in the water flea Daphnia magna (Crustacea, Branchiopoda) suggests different mechanisms of neuroblast formation in insects and crustaceans. Dev Biol 357:42–52. https://doi.org/10.1016/j.ydbio.2011.05.662
Ungerer P, Eriksson BJ, Stollewerk A (2012) Unravelling the evolution of neural stem cells in arthropods: notch signalling in neural stem cell development in the crustacean Daphnia magna. Dev Biol 371:302–311. https://doi.org/10.1016/j.ydbio.2012.08.025
von Reumont BM, Jenner RA, Wills MA et al (2012) Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Mol Biol Evol 29:1031–1045. https://doi.org/10.1093/molbev/msr270
Wheeler WM (1891) Neuroblasts in the arthropod embryo. J Morphol 4:337–343
Whitington F (2004) The development of the crustacean nervous system. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. AA Balkema Publishers, Lisse, pp 135–167
Whitington PM, Mayer G (2011) The origins of the arthropod nervous system: insights from the Onychophora. Arthropod Struct Dev 40:193–209. https://doi.org/10.1016/j.asd.2011.01.006
Wodarz A, Ramrath A, Kuchinke U, Knust E (1999) Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402:544–547. https://doi.org/10.1038/990128
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Hein, H., Scholtz, G. Larval neurogenesis in the copepod Tigriopus californicus (Tetraconata, Multicrustacea). Dev Genes Evol 228, 119–129 (2018). https://doi.org/10.1007/s00427-018-0610-2
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DOI: https://doi.org/10.1007/s00427-018-0610-2