Benthoplanidae, a new family of benthic ctenophores (Platyctenida), based on morphological and genetic data

Nicholas Bezio , Gustav Paulay , Allen Collins

Journal of Systematics and Evolution ›› 2026, Vol. 64 ›› Issue (2) : 387 -400.

PDF (6944KB)
Journal of Systematics and Evolution ›› 2026, Vol. 64 ›› Issue (2) :387 -400. DOI: 10.1111/jse.70023
Research Article
Benthoplanidae, a new family of benthic ctenophores (Platyctenida), based on morphological and genetic data
Author information +
History +
PDF (6944KB)

Abstract

We present a phylogenetic analysis of benthic ctenophores of the order Platyctenida, sampling all but one genus. Using complete mitochondrial genomes and nuclear ribosomal data and a reassessment of anatomy, our integrated analysis uncovers an unexpectedly close relationship between two unusual members of the Coeloplanidae: Coeloplana (Benthoplana) meteoris and Vallicula multiformis. These two species form a well-supported clade, deriving at or near the base of the tree of Platyctenida, distantly related to other Coeloplana, rendering Coeloplana and Coeloplanidae non-monophyletic. A unique mitochondrial gene order and a tentacle bulb with four extensions are newly identified synapomorphies of this lineage. We elevate the subgenus Benthoplana to the generic level, erect the new family Benthoplanidae for Benthoplana and Vallicula, and provide diagnoses for these taxa and their accepted species. We also show that planktonic Ctenoplana (Diploctena) neritica is the early life stage of Benthoplana meteoris, and suggest that the remaining Ctenoplanidae likely represent early life history stages of Coeloplanidae and perhaps other platyctenes. While both the nuclear ribosomal (18S and 28S) and mitochondrial protein-coding genes suggest a deep phylogenetic divergence between Benthoplanidae and Coeloplanidae, we detect conflicting phylogenetic signal between these markers, suggesting nuclear-mitochondrial discordance, leaving the placement of Tjalfiellidae and Lyroctenidae uncertain.

Keywords

Benthoplana / Coeloplanidae / Ctenophora / Ctenoplanidae / mitochondrial genome / ribosomal RNA / systematics

Cite this article

Download citation ▾
Nicholas Bezio, Gustav Paulay, Allen Collins. Benthoplanidae, a new family of benthic ctenophores (Platyctenida), based on morphological and genetic data. Journal of Systematics and Evolution, 2026, 64 (2) : 387-400 DOI:10.1111/jse.70023

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Allio R, Scornavacca C, Nabholz B, Clamens A-L, Sperling FA, Condamine FL. 2020. Whole genome shotgun phylogenomics resolves the pattern and timing of swallowtail butterfly evolution. Systematic Biology 69(1): 38–60.

[2]

Arafat H, Alamaru A, Gissi C, Huchon D. 2018. Extensive mitochondrial gene rearrangements in Ctenophora: Insights from benthic Platyctenida. BMC Evolutionary Biology 18: 1–11.

[3]

Arnold P. 1993. First record of ctenophore Coeloplana (Benthoplana) meteoris (Thiel, 1968) from Australia. Memoirs of the Queensland Museum 33(1): 16.

[4]

Bayha KM, Chang MH, Mariani CL, Richardson JL, Edwards DL, DeBoer TS, Moseley C, Aksoy E, Decker MB, Gaffney PM, Harbison GR, McDonald JH, Caccone A. 2015. Worldwide phylogeography of the invasive ctenophore Mnemiopsis leidyi (Ctenophora) based on nuclear and mitochondrial DNA data. Biological Invasions 17(3): 827–850.

[5]

Bezio N, Collins AG. 2024. Redescription of the deep-sea benthic ctenophore genus Tjalfiella from the North Atlantic (Class Tentaculata, Order Platyctenida, Family Tjalfiellidae). Zootaxa 5486(2): 241–266.

[6]

Burkhardt P, Colgren J, Medhus A, Digel L, Naumann B, Soto-Angel JJ, Nordmann EV, Sachkova MY, Kittelmann M. 2023. Syncytial nerve net in a ctenophore adds insights on the evolution of nervous systems. Science 380(6642): 293–297.

[7]

Chen S, Zhou Y, Chen Y, Gu J. 2018. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17): i884–i890.

[8]

Christianson LM, Johnson SB, Schultz DT, Haddock SHD. 2022. Hidden diversity of Ctenophora revealed by new mitochondrial COI primers and sequences. Molecular Ecology Resources 22(1): 283–294.

[9]

Dawydoff C. 1950. La nouvelle forme de Ctenophores planarises sessiles provenant de la Mer de Chine Meridionale (Savangia atentaculata nov. gen. nov. spec.). Comptes Rendus Hebdomadaires des Seances de l'Academie des Science 231(17): 814–816.

[10]

Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452(7188): 745–749.

[11]

Fricke HW, Plante R. 1971. Contribution à l'étude des Cténophores Platycténides de Madagascar: Ctenoplana (Diploctena n.s. gen.) neritica n.sp. et Coeloplana (Benthoplana n.s. gen.) meteoris (Thiel 1968). Cahiers de Biologie Marine 12: 57–75.

[12]

Fujiwara Y, Kawato M, Yamamoto T, Yamanaka T, Sato-Okoshi W, Noda C, Tsuchida S, Komai T, Cubelio SS, Sasaki T, Jacobsen K, Kubokawa K, Fujikura K, Maruyama T, Furushima Y, Okoshi K, Miyake H, Miyazaki M, Nogi Y, Yatabe A, Okutani T. 2007. Three-year investigations into sperm whale-fall ecosystems in Japan. Marine Ecology 28(1): 219–232.

[13]

Gasmi S, Nève G, Pech N, Tekaya S, Gilles A, Perez Y. 2014. Evolutionary history of Chaetognatha inferred from molecular and morphological data: A case study for body plan simplification. Frontiers in Zoology 11(1): 1–25.

[14]

Gershwin L, Zeidler W, Davie PJF. 2010. Ctenophora of Australia. Memoirs of the Queensland Museum 54: 1–45.

[15]

Giraldes BW. 2019. The first record of the Indo-Pacific benthic ctenophore Coeloplana (Benthoplana) meteoris (Ctenophora: Coeloplanidae) in the Arabian-Persian Gulf. Journal of Asia-Pacific Biodiversity 12(3): 467–469.

[16]

Glynn PW, Bayer FM, Renegar DA. 2014. Coeloplana waltoni, a new species of minute benthic ctenophore (Ctenophora: Platyctenida) from south Florida. Proceedings of the Biological Society of Washington 127(2): 423–436.

[17]

Glynn PW, Coffman B, Primov K, Renegar DA, Gross J, Blackwelder P, Martinez N, Dominguez J, Vanderwoude J, Riegl BM. 2019. Benthic ctenophore (Order Platyctenida) reproduction, recruitment, and seasonality in south Florida. Invertebrate Biology 138(3): e12256.

[18]

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology 59(3): 307–321.

[19]

Haddock SHD. 2004. A golden age of gelata: Past and future research on planktonic ctenophores and cnidarians. Hydrobiologia 530: 549–556.

[20]

Harbison G, Madin L. 1982. Ctenophora. In: Parker SP ed. Synopsis and classification of living organisms. New York: McGraw-Hill. 707–715.

[21]

Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42(2): 182–192.

[22]

Hoban ML, Whitney J, Collins AG, Meyer C, Murphy KR, Reft AJ, Bemis KE. 2022. Skimming for barcodes: Rapid production of mitochondrial genome and nuclear ribosomal repeat reference markers through shallow shotgun sequencing. PeerJ 10: e13790.

[23]

Johnson SB, Winnikoff JR, Schultz DT, Christianson LM, Patry WL, Mills CE, Haddock SHD. 2022. Speciation of pelagic zooplankton: Invisible boundaries can drive isolation of oceanic ctenophores. Frontiers in Genetics 13: 970314.

[24]

Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780.

[25]

Komai T. 1922. Studies on two aberrant ctenophores, Coeloplana and Gastrodes. Kyoto: Niodo Publishers.

[26]

Komai T. 1941. A new remarkable sessile ctenophore. Proceedings of the Imperial Academy 17(6): 216–220.

[27]

Kowalevsky A. 1880. Coeloplana metschnikowii. Zoologischer Anzeiger 3(51): 140.

[28]

Kramp PL. 1942. Ctenophora. The Godthaab Expedition 1928. Meddeleser om Grönland 80(9): 1–19.

[29]

Lefort V, Longueville JE, Gascuel O. 2017. SMS: Smart model selection in PhyML. Molecular Biology and Evolution 34(9): 2422–2424.

[30]

Lindsay DJ, Miyake H. 2007. A novel benthopelagic ctenophore from 7,217 m depth in the Ryukyu Trench, Japan, with notes on the taxonomy of deepsea cydippids. Plankton and Benthos Research 2(2): 98–102.

[31]

Mack JM, Klinth M, Martinsson S, Lu R, Stormer H, Hanington P, Proctor HC, Erséus C, Bely A. 2023. Cryptic carnivores: Intercontinental sampling reveals extensive novel diversity in a genus of freshwater annelids. Molecular Phylogenetics and Evolution 182: 107748.

[32]

Marcus EDBR. 1956. Vallicula multiformis Rankin, 1956, from Brazil. Boletim do Instituto Oceanográfico 7: 87–91.

[33]

Martinsson S, Klinth M, Erséus C. 2018. A new Scandinavian Chamaedrilus species (Clitellata: Enchytraeidae), with additional notes on others. Zootaxa 4521(3): 417–429.

[34]

Matsumoto GI, Gowlett-Holmes KL. 1996. Coeloplana scaberiae sp. nov., a new benthic ctenophore (Ctenophora: Platyctenida: Coeloplanidae) from South Australia. Records of the South Australian Museum 29(1): 33–40.

[35]

Mills CE. 2017. Phylum Ctenophora: List of all valid species names [online]. Available from https://Faculty.Washington.Edu/Cemills/Ctenolist.Html [accessed 13 February 2025].

[36]

Miyake H, Wada S, Adachi A, Ohtsuka S, Ikeda S, Yonetani M, Pagliawan HB, Metillo E, Okoshi K. 2019. Benthic platyctenid ctenophore, Vallicula multiformis Rankin, 1956, found in an aquarium on Palawan Island, the Philippines. Plankton and Benthos Research 14(1): 14–21.

[37]

Mohri K, Watanabe H. 2024. Neuromuscular organization of the benthic ctenophore, Vallicula multiformis. Zoological Letters 10(1): 3.

[38]

Moroz LL, Collins R, Paulay G. 2024. Ctenophora: Illustrated guide and taxonomy. In: Moroz LL ed. Ctenophores: Methods and protocols. Clifton, NJ: Humana Press. 27–102.

[39]

Mortensen T. 1910. Tjalfiella tristoma n. g., n. sp. A sessile ctenophore from Greenland. Videnskabelige Meddelelser fra denNaturhistoriske Forening i Kjøbenhavn 17: 249–253.

[40]

Mortensen T. 1912. Papers from Dr. Th. Mortensen's Pacific expedition—The Danish Ingolf-Expedition: Ctenophora, Vol. 5. Part 2. Copenhagen: H. Hagerup. 59 pp., 15 text figs., 10 pls.

[41]

Prasade A, Apte D, Kale P, Oliveira OM. 2015. Vallicula multiformis Rankin, 1956 (Ctenophora, Platyctenida): First record from the Indian Ocean. Check List 11(1): 1544.

[42]

Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. 2020. Using SPAdes DE Novo Assembler. Current Protocols in Bioinformatics 70(1): e102.

[43]

Puente-Tapia FA, Ortigosa D, Vital XG, Palomino-Alvarez LA. 2023. First record of a benthic ctenophore in the Mexican Atlantic: Vallicula multiformis (Platyctenida, Coeloplanidae). Journal of the Marine Biological Association of the United Kingdom 103: e47.

[44]

Puillandre N, Brouillet S, Achaz G 2021. ASAP: Assemble species by automatic partitioning. Molecular Ecology Resources 21(2): 609-620.

[45]

Rankin JJ. 1956. The structure and biology of Vallicula multiformis, gen. et sp. nov., a platyctenid ctenophore. The Journal of the Linnean Society 43(289): 55–71.

[46]

Robilliard GA, Dayton PK. 1972. A new species of platyctenean ctenophore, Lyrocteis flavopallidus sp. nov., from McMurdo Sound, Antarctica. Canadian Journal of Zoology 50(1): 47–52.

[47]

Schultz DT, Haddock SHD, Bredeson JV, Green RE, Simakov O, Rokhsar DS. 2023. Ancient gene linkages support ctenophores as sister to other animals. Nature 618(7963): 110–117.

[48]

Simion P, Bekkouche N, Jager M, Quéinnec E, Manuel M. 2015. Exploring the potential of small RNA subunit and ITS sequences for resolving phylogenetic relationships within the phylum Ctenophora. Zoology 118(2): 102–114.

[49]

Thiel H. 1968. Coeloplana meteoris nov. spec. (Ctenophora: Platyctenea): Bescheibung und systematische Stellung mit einem Vergleich der Gastrovascularsysteme in deiser Ordung. Meteor Forschungsergebnisse 3: 1–13, 18 text-figs.

[50]

Townsend JP, Tassia MG, Damian-Serrano A, Whelan NV, Halanych KM, Sweeney AM. 2020. A mesopelagic ctenophore representing a new family, with notes on family-level taxonomy in Ctenophora: Vampyroctena delmarvensis gen. nov. sp. nov. (Vampyroctenidae, fam. nov.). Marine Biodiversity 50(3): 34.

[51]

Venkatraman K, Raghunathan C, Raghuraman R, Sreeraj CR. 2012. Marine Biodiversity. Kolkata: Zoological Survey of India.

[52]

Whelan NV, Kocot KM, Moroz TP, Mukherjee K, Williams P, Paulay G, Moroz LL, Halanych KM. 2017. Ctenophore relationships and their placement as the sister group to all other animals. Nature Ecology & Evolution 1(11): 1737–1746.

[53]

Wirtz P. 1998. Twelve invertebrate and eight fish species new to the marine fauna of Madeira, and a discussion of the zoogeography of the area. Helgoländer Meeresuntersuchungen 52: 197–207.

RIGHTS & PERMISSIONS

2025 The Author(s). Journal of Systematics and Evolution published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences. This article has been contributed to by U.S.Government employees and their work is in the public domain in the USA.

PDF (6944KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/