Evolution of eye development in arthropods: Phylogenetic aspects

Arthropod Structure and Development

Volumn 35, Issue 4, 2006, Pages 319-340

  Harzsch, Steffen ^a,b,c   Hafner, Gary ^b,c  

^a UNIVERSITY OF ULM   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c INDIANA UNIVERSITY   (United States)

Author keywords

Arthropod phylogeny; Compound eye; Development; Evo devo; Evolution; Visual system

Indexed keywords

ARTHROPOD; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EYE DEVELOPMENT; MORPHOGENESIS; NONHUMAN; PHYLOGENY; PLESIOMORPHY; REVIEW; SEPARATION TECHNIQUE; VISUAL SYSTEM;

ARTHROPODA; CHILOPODA; CRUSTACEA; DIPLOPODA; HEXAPODA; INSECTA; MYRIAPODA; SCUTIGEROMORPHA; TRILOBITA; UNIRAMIA; XIPHOSURA;

EID: 33845296144     PISSN: 14678039     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.asd.2006.08.009     Document Type: Review

References (104)

1. Anderson H. Postembryonic development of the visual system of the locust, Schistocerca gregaria. Patterns of growth and developmental interactions in the retina and optic lobe. Journal of Embryology and Experimental Morphology 45 (1978) 55-83
2. Andersson G. Post-embryogenic development of Lithobius forficatus (L.), (Chilopoda: Lithobiidae). Entomologica Scandinavica 7 (1976) 161-168
3. Bitsch C., and Bitsch J. Phylogenetic relationships of basal hexapods among the mandibulate arthropods: a cladistic analysis based on comparative morphological characters. Zoologica Scripta 33 (2004) 511-550
4. Bitsch C., and Bitsch J. Evolution of eye structure and arthropod phylogeny. In: Koenemann S. (Ed). Crustaceans & Arthropod relationships (2005), CRC Press, Taylor & Francis Book Inc., New York 185-214
5. Blower J.G. Millipedes. Synopses of the British Fauna (New Series) No 35 (1985), EJ Brill/W Backhuis, Leyden 242 pp
6. Bonini N.M., and Choi K.W. Early decisions in Drosophila eye morphogenesis. Current Opinion in Genetics and Development 5 (1995) 507-515
7. Campos-Ortega J.A. On compound eye development in Drosophila melanogaster. In: Hunt R.K. (Ed). Current Topics in Developmental Biology 15 (1980), Academic Press, New York 347-371
8. Clarkson E.N.K. The evolution of the eye in trilobites. Fossils Strata 4 (1975) 7-31
9. Clarkson E.N.K. The visual system of trilobites. Palaeontology 16 (1979) 827-840
10. Clarkson E.N.K., and Zhang X.-G. Ontogeny of the carboniferous trilobite Paladin eichwaldi shunnerensis (King 1914). Transaction of the Royal Society of Edinburgh: Earth Sciences 82 (1991) 277-295
11. Clarkson E., Levi-Setti R., and Horváth G. The eyes of trilobites; the oldest preserved visual system. Arthoped Structure and Development 35 4 (2006) 247-259
12. Cook C.E., Smith M.L., Telford M.J., Bastianello A., and Akam M. Hox genes and the phylogeny of the arthropods. Current Biology 11 (2001) 759-763
13. Cutforth T., and Gaul U. The genetics of visual system development in Drosophila: specification, connectivity and asymmetry. Current Opinion in Neurobiology 7 (1997) 48-54
14. Dohle W. 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. Annals de la Société Entomologique de France (NS) 37 (2001) 85-103
15. Dong X., Zavitz K.H., Thomas B.J., Lin M., Campbell S., and Zipursky S.L. Control of G1 in the developing Drosophila eye: rca1 regulates cyclin A. Genes and Development 11 (1997) 94-105
16. Dove H., and Stollewerk A. Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development 130 (2003) 2161-2171
17. Edgecombe G.D. Morphological data, extant Myriapoda, and the myriapod stem-group. Contributions to Zoology 73 (2004) 207-252
18. Edgecombe G.D., and Giribet G. Adding mitochondrial sequence data (16S rRNA and cytochrome c oxidase subunit I) to the phylogeny of centipedes (Myriapoda, Chilopoda): an analysis of morphology and four molecular loci. Journal of Zoological Systematics and Evolutionary Research 42 (2004) 89-134
19. Egelhaaf A., Altenfeld H., and Hoffmann H.-U. Evidence for the priming role of the central retinula cell in ommatidium differentiation of Ephestia kuehniella. Roux's Archives of Developmental Biology 197 (1988) 184-189
20. Elofsson R. The development of the compound eyes of Penaeus duorarum (Crustacea: Decapoda) with remarks on the nervous system. Zeitschrift für Zellforschung 97 (1969) 323-350
21. Elofsson R., and Dahl E. The optic neuropils and chiasmata of Crustacea. Zeitschrift für Zellforschung 107 (1970) 343-360
22. Enghoff H., Dohle W., and Blower J.G. Anamorphosis in millipedes (Diplopoda) - the present state of knowledge with some developmental and phylogenetic considerations. Zoological Journal of the Linnean Society 109 (1993) 103-234
23. Fahrenbach W.H. The visual system of the horseshoe crab Limulus polyphemus. International Reviews of Cytology 41 (1975) 285-349
24. Freeman M. Cell determination strategies in the Drosophila eye. Development 124 (1997) 261-270
25. French, K.A., 1980. The development of photoreception in Limulus polyphemus: morphology, electrophysiology, and behavior. PhD thesis, Boston University Graduate School, pp. 1-168.
26. Fordyce D., and Cronin T.W. Trilobite vision: a comparison of schizochroal and holochroal eyes with compound eyes of modern arthropods. Paleobiology 19 (1993) 288-303
27. Friedrich M. Evolution of insect eye development: first insights from fruit fly, grasshopper and flour beetle. Integrative and Comparative Biology 43 (2003) 505-521
28. Friedrich M. Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila melanogaster. Arthropod Structure and Development 35 4 (2006) 357-378
29. Friedrich, M. Insect interordinal relationships: evidence from the visual system. Entomologische Abhandlungen Dresden, in press.
30. Friedrich, M. 2006b. Continuity versus split and reconstitution: exploring the molecular developmental corollaries of insect eye primordium evolution. Developmental Biology, doi:10.1016/j.ydbio.2006.08.027.
31. Friedrich M., and Benzer S. Divergent decapentaplegic expression patterns in the compound eye development and the evolution of insect metamorphosis. Journal of Experimental Zoology 288 (2000) 39-55
32. Friedrich M., and Tautz D. Arthropod rDNA phylogeny revisited: a consistency analysis using Monte Carlo Simulation. Annals de la Société Entomologique de France (NS) 37 (2001) 21-40
33. Friedrich M., Rambold T., and Melzer R.R. The early stages of ommatidial development in the flour beetle Tribolium castaneum (Coleoptera; Tenebrionidae). Development Genes and Evolution 206 (1996) 136-146
34. Green P., Hartenstein A.Y., and Hartenstein V. The embryonic development of the Drosophila visual system. Cell and Tissue Research 273 (1993) 583-598
35. Hafner G.S., and Tokarski T.R. Morphogenesis and pattern formation in the retina of the crayfish Procambarus clarkii. Cell and Tissue Research 293 (1998) 535-550
36. Hafner G.S., and Tokarski T.R. Retinal development in the lobster Homarus americanus: comparison with compound eyes of insects and other crustaceans. Cell Tissue Research 305 (2001) 147-158
37. Hafner G.S., Tokarski T.R., and Hammond-Soltis G. Development of the crayfish retina: a light- and electron-microscopic study. Journal of Morphology 173 (1982) 101-118
38. Hafner G.S., Martin R.L., and Tokarski T.R. Photopigment gene expression and rhabdome formation in the crayfish (Procambarus clarkii). Cell and Tissue Research 311 (2003) 99-105
39. Harzsch S. Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea and Hexapoda?. Arthropod Structure and Development 32 (2003) 17-38
40. Harzsch S. Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny. Integrative and Comparative Biology 46 (2006) 162-194
41. Harzsch S., and Dawirs R.R. Maturation of the compound eyes and eyestalk ganglia during larval development of the brachyuran crustaceans Hyas araneus L. (Decapoda, Majidae) and Carcinus maenas L. (Decapoda, Portunidae). Zoology 99 (1995/96) 189-204
42. Harzsch S., and Walossek D. Neurogenesis in the developing visual system of the branchiopod crustacean Triops longicaudatus (LeConte, 1846): corresponding patterns of compound-eye formation in Crustacea and Insecta?. Development Genes and Evolution 211 (2001) 37-43
43. Harzsch S., Benton J., Dawirs R.R., and Beltz B. A new look at embryonic development of the visual system in decapod crustaceans: neuropil formation, neurogenesis and apoptotic cell death. Journal of Neurobiology 39 (1999) 294-306
44. Harzsch S., Müller C.H.G., and Wolf H. From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister-group relationship of Chelicerata and "Myriapoda" but favour the Mandibulata concept. Development Genes and Evolution 215 (2005) 53-68
45. Harzsch S., Wildt M., Battelle B., and Waloszek D. Immunohistochemical localization of neurotransmitters in the nervous system of larval Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura): evidence for a conserved architecture of the protocerebrum in Euarthropoda. Arthropod Structure and Development 34 (2005) 327-342
46. Harzsch, S., Melzer, R.R., Müller, C.H.G., 2006a. Mechanisms of eye development and evolution of the arthropod visual system: the lateral eyes of Myriapoda are not modified insect ommatidia. Organisms, Diversity and Evolution, in press.
47. Harzsch, S., Vilpoux, K., Blackburn, D.C., Platchetzki, D., Brown, N.L., Melzer, R., Kempler, K.E., Battelle, B., 2006b. Evolution of arthropod visual systems: development of the eyes and central visual pathways in the horseshoe crab Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura). Developmental Dynamics 235, 2641-2655.
48. Heberlein U., and Moses K. Mechanisms of Drosophila retinal morphogenesis: the virtues of being progressive. Cell 81 (1995) 987-990
49. Hwang U.W., Friedrich M., Tautz D., Park C.J., and Kim W. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413 (2001) 154-157
50. Kadner D., and Stollewerk A. Neurogenesis in the chilopod Lithobius forficatus suggests more similarities to chelicerates than to insects. Development Genes and Evolution 214 (2004) 367-379
51. Klass K.D., and Kristensen N.P. The ground plan and affinities of hexapods: recent progress and open problems. In: Deuve T. (Ed). Origin of the Hexapoda. Annals de la Société Entomologique de France (NS) 37 (2001) 265-581
52. Mallatt J.M., Garey J.R., and Shultz J.W. Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Molecular Phylogenetics and Evolution 31 (2004) 178-191
53. Malzacher P. Die Embryogenese des Gehirns paurometaboler Insekten. Untersuchungen an Carausius morosus und Periplaneta americana. Zeitschrift für Morphologie der Tiere 62 (1968) 103-161
54. Marler J.J., Barlow R.B., Eisele L., and Kass L. Photoreceptors add at the anterior edge of Limulus lateral eyes. Biological Bulletin 165 (1983) 541
55. Mayer G. Structure and development of onychophoran eyes - what is the ancestral visual organ in arthropods?. Arthropod Structure and Development 35 4 (2006) 231-245
56. Meadors S., McGuiness C., Dodge F.A., and Barlow R.B. Growth, visual field and resolution in the juvenile Limulus lateral eye. Biological Bulletin 201 (2001) 272-274
57. Meinertzhagen I.A. Development of the compound eye and optic lobes of insects. In: Young D. (Ed). Developmental Neurobiology of Arthropods (1973), Cambridge University Press, London 51-104
58. Meinertzhagen I.A., and Hanson T.E. The development of the optic lobe. In: Bate M., and Martinez-Arias A. (Eds). The Development of Drosophila melanogaster (1993), Cold Spring Harbor Laboratory Press, Cold Spring-Harbor 1363-1491
59. Melzer R.R., Diersch R., Nicastro D., and Smola U. Compound eye evolution: highly conserved retinula and cone cell patterns indicate a common origin of the insect and crustacean ommatidium. Naturwissenschaften 84 (1997) 542-544
60. Melzer R., Michalke C., and Smola U. Walking on insect paths: early ommatidial development in the compound eye of the ancestral crustacean Triops cancriformis. Naturwissenschaften 87 (2000) 308-311
61. Mittmann B. Early neurogenesis in the horseshoe crab and its implication for arthropod relationships. Biological Bulletin 203 (2002) 221-222
62. Mittmann B., and Scholtz G. Development of the nervous system in the "head" of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Development Genes and Evolution 213 (2003) 9-17
63. Moses K. Drosophila Eye Development (2002), Springer Verlag Berlin, Heidelberg, New York 1-277
64. Mouze M. Croissance et metamorphose de l'appareil visuel des Aeschnidae (Odonata). International Journal of Insect Morphology and Embryology 1 (1972) 181-200
65. Müller C.H.G., and Meyer-Rochow V.B. Fine structural description of the lateral ocellus of Craterostigmus tasmanianus Pocock, 1902 (Chilopoda: Craterostigmophora) and phylogenetic considerations. Journal of Morphology 267 (2006) 850-865
66. Müller C.H.G., and Meyer-Rochow V.B. Fine structural organization of the lateral ocelli in two species of Scolopendra (Chilopoda: Pleurostigmophora): an evolutionary evaluation. Zoomorphology 125 (2006) 13-26
67. Müller, C.H.G., Rosenberg, J., 2006. Homology of lateral ocelli in the Pleurostigmophora? New evidence from the retinal structure of some lithobiomorph species (Chilopoda: Lithobiidae). Journal of Morphology, 267, 850-865.
68. Müller C.H.G., Rosenberg J., Richter S., and Meyer-Rochow V.B. The compound eye of Scutigera coleoptrata (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural re-investigation that adds support to the Mandibulata-concept. Zoomorphology 122 (2003) 191-209
69. Oakley T.H. On homology of arthropod compound eyes. Integrative and Comparative Biology 43 (2003) 522-530
70. Paulus H.F. Eye structure and the monophyly of the Arthropoda. In: Gupta A.P. (Ed). Arthropod Phylogeny (1979), van Nostrand Reinhold Co, New York 299-383
71. Paulus H.F. Evolutionswege zum Larvalauge der Insekten - ein Modell für die Entstehung und die Ableitung der ozellulären Lateralaugen der Myriapoda von Fazettenaugen. Zoologische Jahrbücher Systematik 113 (1986) 353-371
72. Paulus H.F. Phylogeny of the Myriapoda - Crustacea - Insecta: a new attempt using photoreceptor structure. Journal of Zoological Systematics and Evolutionary Research 38 (2000) 189-208
73. Peitsalmi M., and Pajunen V.I. Mapping the ocular field in Proteroiulus fuscus (Am Stein) (Diplopoda, Blaniulidae). Annals Zoologica Fennici 28 (1991) 31-39
74. Peitsalmi M., and Pajunen V.I. Eye growth Choneiulus palmatus (Nemec) and Nopoiulus kochii (Gervais) (Diplopoda, Blaniulidae). Annals Zoologica Fennici 29 (1992) 39-46
75. Peterson K.J., and Eernisse D.J. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evolution and Development 3 (2001) 170-205
76. Pisani D., Poling L.L., Lyons-Weiler M., and Hedges S.B. The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biology 2 (2004) 1
77. Ready D.F., Hanson T.E., and Benzer S. Development of the Drosophila retina, a neurocrystalline lattice. Developmental Biology 53 (1976) 217-240
78. Regier J.C., and Shultz J.W. Elongation factor-2: a useful gene for arthropod phylogenetics. Molecular Phylogenetics and Evolution 20 (2001) 136-148
79. Richter S. The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Organisms. Diversity and Evolution 2 (2002) 217-237
80. Sahli F. Présence en Sarre et contribution à l'étude du développement post-embryonnaire de Cylindroiulus (Aneuloboiulus) silvarum Meinert, 1868 (Myriapoda, Diplopoda, Iulidae). Annales Universitatis Saraviensis. Series Scientias 4 (1955) 151-164
81. Saudray Y. Développement post-embryonnaire d'un Iulide indigène Cylindoiulus (Aneuloboiulus) silvarum Meinert. Archives de la Zoologie Experimetalle 89 (1952) 1-14
82. Schram F.R., and Koenemann S. Are crustaceans monophyletic?. In: Cracraft J., and Donoghue M.J. (Eds). Assembling the Tree of Life (2004), Oxford University Press, New York 319-329
83. Shultz J.W., and Regier J.C. Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean + hexapod clade. Proceedings of the Royal Society London B 267 (2000) 1011-1019
84. Smith K., Ridings C., Dodge F.A., and Barlow R.B. Development of the lateral eye of juvenile Limulus. Biological Bulletin 203 (2002) 222-223
85. Spies T. Structure and phylogenetic interpretation of diplopod eyes (Diplopoda). Zoomorphology 98 (1981) 241-260
86. Stollewerk A. Recruitment of cell groups through Delta/Notch signalling during spider neurogenesis. Development 129 (2002) 5339-5348
87. Stollewerk A., and Chipman A.D. Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships. Integrative and Comparative Biology 46 (2006) 195-206
88. Stollewerk A., and Simpson P. Evolution of early development of the nervous system: a comparison between arthropods. Bioessays 27 (2005) 874-883
89. Stollewerk A., Weller M., and Tautz D. Neurogenesis in the spider Cupiennius salei. Development 128 (2001) 2673-2688
90. Stollewerk A., Tautz D., and Weller M. Neurogenesis in the spider: new insights from comparative analysis of morphological processes and gene expression patterns. Arthropod Structure and Development 32 (2003) 5-16
91. Strausfeld N.J. Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behavior and Evolution 52 (1998) 186-206
92. Strausfeld N.J. The evolution of crustacean and insect optic lobes and the origin of chiasmata. Arthropod Structure and Development 34 (2005) 235-256
93. Thomas A.T. Developmental palaeobiology of trilobite eyes and its evolutionary significance. Earth-Sciences Reviews 71 (2005) 77-93
94. Tomlinson A. The cellular dynamics of pattern formation in the eye of Drosophila. Journal of Embryology and Experimental Morphology 89 (1985) 313-331
95. Vachon M. Contribution à l'étude du développement post-embryonnaire de Pachybolus lingulatus Voges (Myriapodes, Diplopodes, Spirobolides). Les étapes de la croissance. Annales dos Sciences Naturelles Zoologie 2 (1947) 109-121
96. Waterman T.H. Relative growth and the compound eye in Xiphosura. Journal of Morphology 95 (1954) 125-158
97. Weiner W.W., and Chamberlain S.C. The visual field of American horseshoe crabs: two different eye shapes in Limulus polyphemus. Visual Neuroscience 11 (1994) 333-346
98. Whitington P.M. The development of the crustacean nervous system. In: Scholtz G. (Ed). "Evolutionary Developmental Biology of Crustacea" Crustacean issues vol. 15 (2004), Publishers A.A. Balkema, Lisse, Netherlands 135-167
99. Whitington P.M., Meier T., and King P. Segmentation, nevrogenesis and formation of early axonal pathways in the centipede, Ethmostigmus rubripes (Brandt). Roux's Archives of Developmental Biology 199 (1991) 349-363
100. Wildt M., and Harzsch S. A new look at an old visual system: structure and development of the compound eyes and optic ganglia of the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca). Journal of Neurobiology 52 (2002) 117-132
101. Wolff T., and Ready D.F. The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave. Development 113 (1991) 841-850
102. Wolff T., and Ready D.F. Pattern formation in the Drosophila retina. In: Bate M., and Martinez-Arias A. (Eds). The Development of Drosophila melanogaster (1993), Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1277-1325
103. Wolff T., Martin K.A., Rubin G.M., and Zipursky S.L. The development of the Drosophila visual system. In: Cowan W.M., Jessell T.M., and Zipursky S.L. (Eds). Molecular and Cellular Approaches to Neural Development (1997), Oxford University Press 474-508
104. Zhang X.-G., and Clarkson E.N.K. The eyes of lower Cambrian eodiscid trilobites. Palaeontology 33 (1990) 911-933