Taxonomic analysis of the genital plates and associated structures in Ophiuroidea (Echinodermata)
Abstract
Recently, new insights have been gained from the ophiuroid skeleton that were instrumental in the inference of a new phylogeny. The so far least studied ossicles are the adradial and abradial genital plates and the radial shields, which articulate with each other and support the genital slit and disc. In addition, the inner sides of the oral shields and madreporites have never been examined in detail. The present study utilized SEM, micro-CT and digital photography to document and examine these structures in 57 species from 28 of the currently accepted 34 families of Ophiuroidea. Early ontogeny and fossils were also considered. Previously, mainly the articular structures had been analysed, but the overall shape of the genital plates was here found to hold important phylogenetic signals. A long-neglected ossicle was re-discovered and studied in detail for the first time, here named the oral genital plate. It was recognized in all Ophintegrida, but was found to be absent in all Euryophiurida. The oral genital plate articulates with the oral shield and supports the proximal part of the genital slit wall. Abradial and oral genital plates were found to be absent in species that lack genital slits, but the adradial genital plate was always present. Numerous new morphological characters with potential phylogenetic signals were identified, described and figured in detail. A pre-existing character matrix was extended and revised with these new data, as well as with recently revised data on oral papillae, and a Bayesian phylogenetic analysis was performed. This phylogeny largely agrees with the current molecular hypothesis, but some branches were not supported.
References
Brazeau M.D. 2011. Problematic character coding methods in morphology and their effects. Biological Journal of the Linnean Society 104: 489–498. https://doi.org/10.1111/j.1095-8312.2011.01755.x
Byrne M. 1994. Ophiuroidea. In: Harrison F.W. & Chia F.-S. (eds) Echinodermata. Microscopic Anatomy of Invertebrates: 247–343. Wiley-Liss, New York.
Christensen A.B. & Colacino J.M. 2000. Respiration in the burrowing brittlestar, Hemipholis elongata Say (Echinodermata, Ophiuroidea): a study of the effects of environmental variables on oxygen uptake. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 127: 201–213. https://doi.org/10.1016/S1095-6433(00)00254-3
Christodoulou M., O’Hara T.D., Hugall A.F. & Arbizu P.M. 2019. Dark ophiuroid biodiversity in a prospective abyssal mine field. Current Biology 29 (22): 3909–3912.e3. https://doi.org/10.1016/j.cub.2019.09.012
Clark E.G., Hutchinson J.R., Darroch S.A.F., Mongiardino Koch N., Brady T.R., Smith S.A. & Briggs D.E.G. 2018. Integrating morphology and in vivo skeletal mobility with digital models to infer function in brittle star arms. Journal of Anatomy 233: 696–714. https://doi.org/10.1111/joa.12887
David B. & Laurin B. 1996. Morphometrics and cladistics: measuring phylogeny in the sea urchin Echinocardium. Evolution 50: 348–359. https://doi.org/10.1111/j.1558-5646.1996.tb04498.x
Dubois P. 2014. The skeleton of postmetamorphic echinoderms in a changing world. The Biological Bulletin 226: 223–236. https://doi.org/10.1086/BBLv226n3p223
Ezhova O.V., Malakhov V.V. & Martynov A.V. 2016. Madreporites of Ophiuroidea: are they phylogenetically informative? Zoomorphology 135: 333–350.n https://doi.org/10.1007/s00435-016-0315-x
Goharimanesh M., Stöhr S., Mirshamsi O., Ghassemzadeh F. & Adriaens D. 2021. Interactive identification key to all brittle star families (Echinodermata; Ophiuroidea) leads to revised morphological descriptions. European Journal of Taxonomy 766: 1–63. https://doi.org/10.5852/ejt.2021.766.1483
Goharimanesh M., Ghassemzadeh F., De Kegel B., Van Hoorebeke L., Stöhr S., Mirshamsi O. & Adriaens D. 2022. The evolutionary relationship between arm vertebrae shape and ecological lifestyle in brittle stars (Echinodermata: Ophiuroidea). Journal of Anatomy 240: 1034–1047. https://doi.org/10.1111/joa.13617
Gondim A.I., Dias T.L.P., Christoffersen M.L. & Stöhr S. 2015. Redescription of Hemieuryale pustulata von Martens, 1867 (Echinodermata, Ophiuroidea) based on Brazilian specimens, with notes on systematics and habitat association. Zootaxa 3925 (3): 341–360. https://doi.org/10.11646/zootaxa.3925.3.2
Gondim de Farias A.I. 2016. Sistemática da família Hemieuryalidae Verrill, 1899 (Echinodermata, Ophiuroidea, Ophiurida). PhD thesis. Universidade Federal da Paraíba, João Pessoa, Paraiba.
Hainey M.A.H. & Emlet R.B. 2020. Gorgonocephalus eucnemis (Echinodermata: Ophiuroidea) and bursal ventilation. The Biological Bulletin 238 (3): 193–205. https://doi.org/10.1086/709575
Hendler G. 1978. Development of Amphioplus abditus (Verrill) (Echinodermata: Ophiuroidea). II. Description and discussion of ophiuroid skeletal ontogeny and homologies. Biological Bulletin 154: 79–95. https://doi.org/10.2307/1540776
Hendler G. 2018. Armed to the teeth: a new paradigm for the buccal skeleton of brittle stars (Echinodermata: Ophiuroidea). Contributions in Science 526: 189–311. https://doi.org/10.5962/p.324539
Hoggett A.K. 1991. The genus Macrophiothrix (Ophiuroidea: Ophiotrichidae) in Australian waters. Invertebrate Taxonomy 4: 1077–1146. https://doi.org/10.1071/it9901077
Huelsenbeck J.P. & Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
King B. 2019. Which morphological characters are influential in a Bayesian phylogenetic analysis? Examples from the earliest osteichthyans. Biology Letters 15: e20190288. https://doi.org/10.1098/rsbl.2019.0288
Kokorin A.I., Mirantsev G.V. & Rozhnov S.V. 2014. General features of echinoderm skeleton formation. Paleontological Journal 48: 1532–1539. https://doi.org/10.1134/S0031030114140056
Landschoff J. & Griffiths C. 2015. Three-dimensional visualisation of brooding behaviour in two distantly related brittle stars from South African waters. African Journal of Marine Science 37: 533–541. https://doi.org/10.2989/1814232X.2015.1095801
LeClair E.E. 1996. Arm joint articulations in the ophiuran brittlestars (Echinodermata: Ophiuroidea): a morphometric analysis of ontogenetic, serial, and interspecific variation. Journal of Zoology 240: 245–275. https://doi.org/10.1111/j.1469-7998.1996.tb05283.x
Lewis P.O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913–925. https://doi.org/10.1080/106351501753462876
Limaye A. 2012. Drishti: a volume exploration and presentation tool. Proceedings of SPIE, Developments in X-Ray Tomography VIII, 85060X: 1–9. Society of Photo-Optical Instrumentation Engineers, San Diego, CA. https://doi.org/10.1117/12.935640
Ludwig H. 1888. Ophiopteron elegans, eine neue, wahrscheinlich schwimmende Ophiuridenform. Zeitschrift für wissenschaftliche Zoologie 47: 459–464.
Lyman T. 1869. Preliminary report on the Ophiuridae and Astrophytidae dredged in deep water between Cuba and Florida Reef. Bulletin of the Museum of Comparative Zoology 1: 309–354.
Lyman T. 1874. Ophiuridae and Astrophytidae, new and old. Bulletin of the Museum of Comparative Zoology 3: 221–272.
Lyman T. 1882. Report on the Ophiuroidea. In: Thomson C.W. & Murray J. (eds) Report of the Scientific Results of the Voyage of H.M.S. Challenger 1873–76. Zoology V: 1–386.
Martynov A.V. 2010. Reassessment of the classification of the Ophiuroidea (Echinodermata), based on morphological characters. I. General character evaluation and delineation of the families Ophiomyxidae and Ophiacanthidae. Zootaxa 2697 (1): 1–154. https://doi.org/10.11646/zootaxa.2697.1.1
Matsumoto H. 1915. A new classification of the Ophiuroidea: with descriptions of new genera and species. Proceedings of the Academy of Natural Sciences 67: 43–92.
Matsumoto H. 1917. A monograph of Japanese Ophiuroidea, arranged according to a new classification. Journal of the College of Science, Imperial University, Tokyo 38: 1–408.
Murakami S. 1963. The dental and oral plates of Ophiuroidea. Transactions of the Royal Society of New Zealand, Zoology 4: 1–48.
O’Hara T.D., Hugall A.F., Thuy B., Stöhr S. & Martynov A.V. 2017. Restructuring higher taxonomy using broad-scale phylogenomics: the living Ophiuroidea. Molecular Phylogenetics and Evolution 107: 415–430. https://doi.org/10.1016/j.ympev.2016.12.006
O’Hara T.D., Stöhr S., Hugall A.F., Thuy B. & Martynov A. 2018. Morphological diagnoses of higher taxa in Ophiuroidea (Echinodermata) in support of a new classification. European Journal of Taxonomy 416: 1–35. https://doi.org/10.5852/ejt.2018.416
O’Hara T.D., Thuy B. & Hugall A.F. 2021. Relict from the Jurassic: new family of brittle-stars from a New Caledonian seamount. Proceedings of the Royal Society B: Biological Sciences 288: e20210684. https://doi.org/10.1098/rspb.2021.0684
Okanishi M., Fujita T., Maekawa Y. & Sasaki T. 2017. Non-destructive morphological observations of the fleshy brittle star, Asteronyx loveni using micro-computed tomography (Echinodermata, Ophiuroidea, Euryalida). ZooKeys 663: 1–19. https://doi.org/10.3897/zookeys.663.11413
Pineda-Enriquez T. 2013. Filogenia del género Ophiolepis Müller & Troschel, 1840 (Ophiuroidea: Ophiolepididae) inferida por caracteres morfológicos. MSc Thesis. Universidad Nacional Autónoma de México.
Polly P.D., Lawing A.M., Fabre A.-C. & Goswami A. 2013. Phylogenetic Principal Components Analysis and geometric morphometrics. Hystrix, the Italian Journal of Mammalogy 24: 33–41. https://doi.org/10.4404/hystrix-24.1-6383
Ronquist F., Huelsenbeck J.P., Teslenko M., Zhang C. & Nylander J.A.A. 2020. MrBayes version 3.2 Manual: Tutorials and Model Summaries. Available from https://nbisweden.github.io/MrBayes/manual.html [accessed 19 Apr. 2024].
Schoener A. 1967. Post-larval development of five deep-sea ophiuroids. Deep-Sea Research 14: 645–660.
Schoener A. 1969. Atlantic ophiuroids: some post-larval forms. Deep-Sea Research 16: 127–140.
Sereno P.C. 2007. Logical basis for morphological characters in phylogenetics. Cladistics 23: 565–587. https://doi.org/10.1111/j.1096-0031.2007.00161.x
Simões T.R., Vernygora O.V., de Medeiros B.A.S. & Wright A.M. 2023. Handling logical character dependency in phylogenetic inference: extensive performance testing of assumptions and solutions using simulated and empirical data. Systematic Biology 2 (3): 662–680. https://doi.org/10.1093/sysbio/syad006
Smith A.B., Paterson G.L.J. & Lafay B. 1995. Ophiuroid phylogeny and higher taxonomy: morphological, molecular and palaeontological perspectives. Zoological Journal of the Linnean Society 114: 213–243. https://doi.org/10.1111/j.1096-3642.1995.tb00117c.x
Stöhr S. 2005. Who’s who among baby brittle stars (Echinodermata: Ophiuroidea): postmetamorphic development of some North Atlantic forms. Zoological Journal of the Linnean Society 143: 543–576. https://doi.org/10.1111/j.1096-3642.2005.00155.x
Stöhr S. 2011. New records and new species of Ophiuroidea (Echinodermata) from Lifou, Loyalty Islands, New Caledonia. Zootaxa 3089 (1): 1–50. https://doi.org/10.11646/zootaxa.3089.1.1
Stöhr S. & Martynov A. 2016. Paedomorphosis as an evolutionary driving force: insights from deep-sea brittle stars. PLoS One 11: e0164562. https://doi.org/10.1371/journal.pone.0164562
Stöhr S. & O’Hara T.D. 2021. Deep-sea Ophiuroidea (Echinodermata) from the Danish Galathea II Expedition, 1950–52, with taxonomic revisions. Zootaxa 4963 (3): 505–529. https://doi.org/10.11646/zootaxa.4963.3.6
Stöhr S., O’Hara T.D. & Thuy B. 2012a. Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS One 7: 1–14. https://doi.org/10.1371/journal.pone.0031940
Stöhr S., Sautya S. & Ingole B. 2012b. Brittle stars (Echinodermata: Ophiuroidea) from seamounts in the Andaman Sea (Indian Ocean): first account, with descriptions of new species. Journal of the Marine Biological Association of the United Kingdom 92 (5): 1195–1208. https://doi.org/10.1017/S0025315412000240
Stöhr S., Boissin E. & Hoareau T.B. 2013. Taxonomic revision and phylogeny of the Ophiocoma brevipes group (Echinodermata, Ophiuroidea), with description of a new subgenus (Breviturma) and a new species. European Journal of Taxonomy 68: 1–26. https://doi.org/10.5852/ejt.2013.68
Stöhr S., Clark E.G., Thuy B. & Darroch S.A.F. 2019. Comparison of 2D SEM imaging with 3D micro-tomographic imaging for phylogenetic inference in brittle stars (Echinodermata: Ophiuroidea). Zoosymposia 15: 146–158. https://doi.org/10.11646/zoosymposia.15.1.17
Stöhr S., Weber A.A.-T., Boissin E. & Chenuil A. 2020. Resolving the Ophioderma longicauda (Echinodermata: Ophiuroidea) cryptic species complex: five sisters, three of them new. European Journal of Taxonomy 600: 1–37. https://doi.org/10.5852/ejt.2020.600
Stöhr S., O’Hara T.D. & Thuy B. 2022. World Ophiuroidea Database. World Ophiuroidea Database. https://doi.org/10.14284/358
Stürtz B. 1890. Neuer Beitrag zur Kenntnis paläozoischer Seesterne. Palaeontographica 36: 203–250.
Sumida P.Y.G., Tyler P.A., Gage J.D. & Nørrevang A. 1998. Postlarval development in shallow and deep-sea ophiuroids (Echinodermata: Ophiuroidea) of the NE Atlantic Ocean. Zoological Journal of the Linnean Society 124: 267–300. https://doi.org/10.1111/j.1096-3642.1998.tb00577.x
Thuy B. & Stöhr S. 2011. Lateral arm plate morphology in brittle stars (Echinodermata: Ophiuroidea): new perspectives for ophiuroid micropalaeontology and classification. Zootaxa 3013 (1): 1–47. https://doi.org/10.11646/zootaxa.3013.1.1
Thuy B. & Stöhr S. 2016. A new morphological phylogeny of the Ophiuroidea (Echinodermata) accords with molecular evidence and renders microfossils accessible for cladistics. PLoS One 11: e0156140. https://doi.org/10.1371/journal.pone.0156140
Thuy B. & Stöhr S. 2018. Unravelling the origin of the basket stars and their allies (Echinodermata, Ophiuroidea, Euryalida). Scientific Reports 8: e8493. https://doi.org/10.1038/s41598-018-26877-5
Thuy B., Numberger-Thuy L.D. & Pineda-Enríquez T. 2021. New fossils of Jurassic ophiurid brittle stars (Ophiuroidea; Ophiurida) provide evidence for early clade evolution in the deep sea. Royal Society Open Science 8: e210643. https://doi.org/10.1098/rsos.210643
Thuy B., Eriksson M.E., Kutscher M., Lindgren J., Numberger-Thuy L.D. & Wright D.F. 2022. Miniaturization during a Silurian environmental crisis generated the modern brittle star body plan. Communications Biology 5: 1–9. https://doi.org/10.1038/s42003-021-02971-9
Thuy B., Knox L., Numberger-Thuy L.D., Smith N.S. & Sumrall C.D. 2023. Ancient deep ocean as a harbor of biotic innovation revealed by Carboniferous ophiuroid microfossils. Geology 51 (2): 157–161. https://doi.org/10.1130/G50596.1
Ubaghs G. 1941. Description de quelques ophiures de Famennien de la Belgique. Bulletin du Musée royal des Sciences naturelles de Belgique 17: 1–31.
Ung V., Dubus G., Zaragueta-Bagils R. & Vignes-Lebbe R. 2010. Xper2: introducing e-taxonomy. Bioinformatics 26: 703–704. https://doi.org/10.1093/bioinformatics/btp715
Vadon C. 1988. Paedomorphosis and phylogenetic relationships in Ophiuridae. In: Burke R.D., Mladenov P.V., Lambert P. & Parsley R.L. (eds) Sixth International Echinoderm Conference: 323. Balkema, Melbourne.
Ware J.L. & Barden P. 2016. Incorporating fossils into hypotheses of insect phylogeny. Current Opinion in Insect Science 18: 69–76. https://doi.org/10.1016/j.cois.2016.10.003
Wilkie I.C. & Brogger M.I. 2018. The peristomial plates of ophiuroids (Echinodermata: Ophiuroidea) highlight an incongruence between morphology and proposed phylogenies. PLoS One 13: e0202046. https://doi.org/10.1371/journal.pone.0202046
Wright A.M. & Hillis D.M. 2014. Bayesian analysis using a simple likelihood model outperforms parsimony for estimation of phylogeny from discrete morphological data. PLoS One 9: e109210. https://doi.org/10.1371/journal.pone.0109210
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