Four new Solenogastres (Mollusca, Aplacophora) from the South China Sea and paraphyly of Proneomeniidae Simroth, 1893
M. Carmen Cobo
A * , Emily L. McLaughlin A and Kevin M. Kocot A B
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA.
B Alabama Museum of Natural History, The University of Alabama, Tuscaloosa, AL, USA.
Invertebrate Systematics 37(6) 301-333 https://doi.org/10.1071/IS22062
Submitted: 22 November 2022 Accepted: 14 April 2023 Published: 29 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Solenogastres and Caudofoveata (Aplacophora) remain some of the least known molluscs, despite ubiquity in the marine environment and importance in understanding molluscan evolution. The use of new morphological techniques and development of DNA barcode libraries have helped make specimen identification easier. However, for solenogasters, using histology for identification and adequate description of species remains necessary in most cases. This, together with the facts that knowledge about solenogaster species distributions is biased and that most species were described from one or very few individuals, explains why many open questions about the actual distribution, intra- and interspecific variability, etc., remain. We performed an integrative taxonomic study of eight specimens of solenogasters from the South China Sea (West Pacific Ocean) thatresulted in the identification of four new species of Proneomeniidae. Species identification and description following the established diagnostic characters were straightforward. However, phylogenetic analysis of molecular data obtained from these specimens and other members of Proneomeniidae indicate that the family is polyphyletic. We recovered representatives of two other families, Epimeniidae (Epimenia) and Strophomeniidae (Anamenia), nested within Proneomeniidae with strong support. Ancestral character state reconstruction indicates that characters commonly used in solenogaster taxonomy, such as the radula and foregut glands, may be more evolutionarily labile in this group than previously known. Therefore our work fills knowledge gaps regarding the diversity and distribution of members of this family but raises important questions about solenogaster taxonomy and systematics that should be further assessed with additional markers and broader taxon sampling.
ZooBank: urn:lsid:zoobank.org:pub:BCADACD6-9AD0-442A-AD64-031BA8D88599
Keywords: barcoding, biodiversity, mitochondrial DNA, Mollusca, morphology, south-west Pacific, systematics, taxonomy.
References
Bergmeier, FS, Haszprunar, G, Tod, C, and Jörger, KM (2016). Lost in a taxonomic Bermuda Triangle: comparative 3D-microanatomy of cryptic mesopsammic Solenogastres (Mollusca). Organisms, Diversity & Evolution 16, 613–639.| Lost in a taxonomic Bermuda Triangle: comparative 3D-microanatomy of cryptic mesopsammic Solenogastres (Mollusca).Crossref | GoogleScholarGoogle Scholar |
Bergmeier, FS, Brandt, A, Schwabe, E, and Jörger, KM (2017). Abyssal Solenogastres (Mollusca, Aplacophora) from the Northwest Pacific: scratching the surface of deep-sea diversity using integrative taxonomy. Frontiers in Marine Science 4, 410.
| Abyssal Solenogastres (Mollusca, Aplacophora) from the Northwest Pacific: scratching the surface of deep-sea diversity using integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Bergmeier, FS, Haszprunar, G, Brandt, A, Saito, H, Kano, Y, and Jörger, KM (2019). Of basins, plains, and trenches: systematics and distribution of Solenogastres (Mollusca, Aplacophora) in the Northwest Pacific. Progress in Oceanography 178, 102187.
| Of basins, plains, and trenches: systematics and distribution of Solenogastres (Mollusca, Aplacophora) in the Northwest Pacific.Crossref | GoogleScholarGoogle Scholar |
Bergmeier, FS, Ostermair, L, and Jörger, KM (2021). Specialized predation by deep-sea Solenogastres revealed by sequencing of gut contents. Current Biology 31, R836–R837.
| Specialized predation by deep-sea Solenogastres revealed by sequencing of gut contents.Crossref | GoogleScholarGoogle Scholar |
Cobo, MC, and Kocot, KM (2020). Micromenia amphiatlantica sp. nov.: first solenogaster (Mollusca, Aplacophora) with an amphi-Atlantic distribution and insight into abyssal solenogaster diversity. Deep-Sea Research – I. Oceanographic Research Papers 157, 103189.
| Micromenia amphiatlantica sp. nov.: first solenogaster (Mollusca, Aplacophora) with an amphi-Atlantic distribution and insight into abyssal solenogaster diversity.Crossref | GoogleScholarGoogle Scholar |
Cobo, MC, and Kocot, KM (2021). On the diversity of abyssal Dondersiidae (Mollusca: Aplacophora) with the description of a new genus, six new species, and a review of the family. Zootaxa 4933, 63–97.
| On the diversity of abyssal Dondersiidae (Mollusca: Aplacophora) with the description of a new genus, six new species, and a review of the family.Crossref | GoogleScholarGoogle Scholar |
De Oliveira, AL, Wollesen, T, Kristof, A, Scherholz, M, Redl, E, Todt, C, Bleidorn, C, and Wanninger, A (2016). Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks. BMC Genomics 17, 905.
| Comparative transcriptomics enlarges the toolkit of known developmental genes in mollusks.Crossref | GoogleScholarGoogle Scholar |
Folmer, O, Black, M, Hoeh, W, Lutz, R, and Vrijenhoek, R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
García-Álvarez, O, and Salvini-Plawen, L (2007). Species and diagnosis of the families and genera of Solenogastres (Mollusca). Iberus 25, 73–143.
García-Álvarez, O, and Urgorri, V (2003). Solenogastres molluscs from the BENTART Collection (South Shetland Islands, Antarctica), with a description of a new species. Iberus 21, 43–56.
García-Álvarez, O, Urgorri, V, and von Salvini-Plawen, L (2000). Two new species of Dorymenia (Mollusca: Solenogastres: Proneomeniidae) from the South Shetland Islands (Antarctica). Journal of the Marine Biological Association of the United Kingdom 80, 835–842.
| Two new species of Dorymenia (Mollusca: Solenogastres: Proneomeniidae) from the South Shetland Islands (Antarctica).Crossref | GoogleScholarGoogle Scholar |
García-Álvarez, O, Zamarro, M, and Urgorri, V (2009). Proneomeniidae (Solenogastres, Cavibelonia) from the Bentart-2006 Expedition, with description of a new species. Iberus 27, 67–78.
García-Álvarez O, Salvini -Plawen L, Urgorri V (2014) Solenogastres. In ‘Fauna Iberica. Vol. 38. Mollusca Solenogastres, Caudofoveata, Monoplacophora’. (Eds García-Álvarez O, Salvini-Plawen L, Urgorri, V, Souza Troncoso J) pp. 11–26 (Museo Nacional de Ciencias Naturales. CSIC: Madrid, Spain) [In Spanish]
Gil-Mansilla, E, García-Álvarez, O, and Urgorri, V (2008). New Acanthomeniidae (Solenogastres, Cavibelonia) from the abyssal Angola Basin. Zootaxa 1866, 175–186.
Gil-Mansilla, E, García-Álvarez, O, and Urgorri, V (2008b). Metodología para la recolección, conservación y estudio de los moluscos Solenogastros. [Methodology for the collection, conservation and study of Solenogastres molluscs.] Reseñas Malacológicas XIII, 1–31.
Gil-Mansilla, E, García-Álvarez, O, and Urgorri, V (2009). A new genus and two new species of Simrothiellidae (Solenogastres: Cavibelonia) from the Abyssal Angola Basin. Journal of the Marine Biological Association of the United Kingdom 89, 1507–1515.
| A new genus and two new species of Simrothiellidae (Solenogastres: Cavibelonia) from the Abyssal Angola Basin.Crossref | GoogleScholarGoogle Scholar |
Handl, CH (2002). Imeroherpia laubieri, a new solenogaster from the Bay of Biscay. Journal of Molluscan Studies 68, 329–335.
| Imeroherpia laubieri, a new solenogaster from the Bay of Biscay.Crossref | GoogleScholarGoogle Scholar |
Handl, CH, and Todt, C (2005). Foregut glands of Solenogastres (mollusca): anatomy and revised terminology. Journal of Morphology 265, 28–42.
| Foregut glands of Solenogastres (mollusca): anatomy and revised terminology.Crossref | GoogleScholarGoogle Scholar |
Haszprunar, G (1987). The fine morphology of the osphradial sense organs of the Mollusca. IV. Caudofoveata and Solenogastres. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 315, 63–73.
| The fine morphology of the osphradial sense organs of the Mollusca. IV. Caudofoveata and Solenogastres.Crossref | GoogleScholarGoogle Scholar |
Heath, H (1905). The morphology of a solenogastre. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere Abteilung für Anatomie und Ontogenie der Tiere 21, 701–734.
Heath, H (1911). Reports on the scientific results of the expedition to the Tropical Pacific, in charge of Alexander Agassiz, by the US Fish Commission Steamer Albatross, from August 1899 to June 1900, Commander Jefferson F. Moser. XVI. ‘The Solenogastres.’. Memoirs of the Museum of Comparative Zoology at Harvard College, 45, 1–182.
Heath, H (1918). Solenogastres from the eastern coast of North America. Memoirs of the Museum of Comparative Zoology at Harvard College 45, 187–360.
Hubrecht, A (1880). Proneomenia sluiteri g. et sp. n. g. & sp. nn. Zoologischer Anzeiger 3, 589–590.
Katoh, K, and Standley, DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |
Kocot, KM, and Todt, C (2014). Three new meiofaunal solenogaster species (Mollusca: Aplacophora) from the north-east Pacific. Journal of Natural History 48, 3007–3031.
| Three new meiofaunal solenogaster species (Mollusca: Aplacophora) from the north-east Pacific.Crossref | GoogleScholarGoogle Scholar |
Kocot, KM, Cannon, JT, Todt, C, Citarella, MR, Kohn, AB, Meyer, A, Santos, SR, Schander, C, Moroz, LL, Lieb, B, and Halanych, KM (2011). Phylogenomics reveals deep molluscan relationships. Nature 477, 452–456.
| Phylogenomics reveals deep molluscan relationships.Crossref | GoogleScholarGoogle Scholar |
Kocot, KM, Todt, C, Mikkelsen, NT, and Halanych, KM (2019). Phylogenomics of Aplacophora (Mollusca, Aculifera) and a solenogaster without a foot. Proceedings of the Royal Society of London – B. Biological Sciences 286, 20190115.
| Phylogenomics of Aplacophora (Mollusca, Aculifera) and a solenogaster without a foot.Crossref | GoogleScholarGoogle Scholar |
Kocot, KM, Todt, C, Mikkelsen, NT, and Halanych, KM (2022). Correction to: ‘Phylogenomics of Aplacophora (Mollusca, Aculifera) and a solenogaster without a foot’ (2019) by Kocot et al. Proceedings of the Royal Society of London – B. Biological Sciences 289, 20190115.
| Correction to: ‘Phylogenomics of Aplacophora (Mollusca, Aculifera) and a solenogaster without a foot’ (2019) by Kocot et al.Crossref | GoogleScholarGoogle Scholar |
Koren, J, and Danielssen, DC (1877). Beskrivelse over nye arter, henhørende til slaegten Solenopus, samt nogle oplysninger om dens organisation. [Description of new species, belonging to the genus Solenopus, as well as some information on its organisation.] Journal of Natural History 3, 321–328.
Kowalevsky, A, and Marion, A (1887). Contributions à l’histoire des Solénogastres ou Aplacophores. [Contributions to the history of the Solenogastres or Aplacophores.] Annales du Musée d’Histoire Naturelle de Marseille, Zoologie 3, 1–77.
Lewis, PO (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
| A likelihood approach to estimating phylogeny from discrete morphological character data.Crossref | GoogleScholarGoogle Scholar |
McCutcheon, MG, Kocot, KM, and Cobo, MC (2022). Uncovering the biodiversity of Solenogastres (Mollusca, Aplacophora) with three new species of Proneomeniidae Simroth, 1893 and new data for Dorymenia quincarinata (Ponder, 1970). Molluscan Research 42, 271–286.
| Uncovering the biodiversity of Solenogastres (Mollusca, Aplacophora) with three new species of Proneomeniidae Simroth, 1893 and new data for Dorymenia quincarinata (Ponder, 1970).Crossref | GoogleScholarGoogle Scholar |
Martínez-Sanjuán, J, Kocot, K, García-Álvarez, Ó, Candás, M, and Díaz-Agras, G (2022). Computed microtomography (Micro-CT) in the anatomical study and identification of Solenogastres (Mollusca). Frontiers in Marine Science 8, 760194.
| Computed microtomography (Micro-CT) in the anatomical study and identification of Solenogastres (Mollusca).Crossref | GoogleScholarGoogle Scholar |
Mikkelsen , NT, Kocot , KM, and Halanych , KM (2018). Mitogenomics reveals phylogenetic relationships of caudofoveate aplacophoran molluscs. Molecular Phylogenetics and Evolution 127, 429–436.
| Mitogenomics reveals phylogenetic relationships of caudofoveate aplacophoran molluscs.Crossref | GoogleScholarGoogle Scholar |
Mikkelsen, NT, Todt, C, Kocot, KM, Halanych, KM, and Willassen, E (2019). Molecular phylogeny of Caudofoveata (Mollusca) challenges traditional views. Molecular Phylogenetics and Evolution 132, 138–150.
| Molecular phylogeny of Caudofoveata (Mollusca) challenges traditional views.Crossref | GoogleScholarGoogle Scholar |
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A, and Lanfear, R (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.
| IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era.Crossref | GoogleScholarGoogle Scholar |
Mora, C, Tittensor, DP, Adl, S, Simpson, AGB, and Worm, B (2011). How many species are there on Earth and in the ocean? PLoS Biology 9, e1001127.
| How many species are there on Earth and in the ocean?Crossref | GoogleScholarGoogle Scholar |
Nierstrasz, H (1902). The Solenogastres of the Siboga-Expedition. Siboga-Expeditie 47, 1–46.
Ocean Biodiversity Information System (2022) Observation data collected by Marine Biological Museum, Chinese Academy of Sciences (SCS-Part II). (OBIS, Intergovernmental Oceanographic Commission of UNESCO) Available at www.obis.org/dataset/e68c1476-8ef3-4836-9306-c929e05a58f2
Okusu, A, Schwabe, E, Eernisse, DJ, and Giribet, G (2003). Towards a phylogeny of chitons (Mollusca, Polyplacophora) based on combined analysis of five molecular loci. Organisms Diversity & Evolution 3, 281–302.
| Towards a phylogeny of chitons (Mollusca, Polyplacophora) based on combined analysis of five molecular loci.Crossref | GoogleScholarGoogle Scholar |
Ostermair, L, Brandt, A, Haszprunar, G, Jörger, KM, and Bergmeier, FS (2018). First insights into the solenogaster diversity of the Sea of Okhotsk with the description of a new species of Kruppomenia (Simrothiellidae, Cavibelonia). Deep-Sea Research – II. Topical Studies in Oceanography 154, 214–229.
| First insights into the solenogaster diversity of the Sea of Okhotsk with the description of a new species of Kruppomenia (Simrothiellidae, Cavibelonia).Crossref | GoogleScholarGoogle Scholar |
Pedrouzo, L, Cobo, MC, García-Álvarez, Ó, Rueda, JL, Gofas, S, and Urgorri, V (2014). Solenogastres (Mollusca) from expeditions off the South Iberian Peninsula, with the description of a new species. Journal of Natural History 48, 2985–3006.
| Solenogastres (Mollusca) from expeditions off the South Iberian Peninsula, with the description of a new species.Crossref | GoogleScholarGoogle Scholar |
Pedrouzo, L, García-Álvarez, Ó, Urgorri, V, and Pérez-Señarís, M (2019). New data and 3D reconstruction of four species of Pruvotinidae (Mollusca: Solenogastres) from the NW Iberian peninsula. Marine Biodiversity 49, 277–287.
| New data and 3D reconstruction of four species of Pruvotinidae (Mollusca: Solenogastres) from the NW Iberian peninsula.Crossref | GoogleScholarGoogle Scholar |
Pedrouzo, L, García-Álvarez, Ó, and Urgorri, V (2022). New species of Pruvotininae (Solenogastres, Cavivelonia) from bathyal bottoms off the NW Iberian Peninsula, with a taxonomical discussion about the family Provotinidae. Iberus 40, 317–354.
Pelseneer, P (1901). Les Néoméniens de l’Expédition Antarctique Belge et la distribution géographique des Aplacophora. [The Neomenians of the Belgian Antarctic Expedition and the geographical distribution of Aplacophora.] Bulletin de la Classe des sciences 9–10, 528–534.
Ponder, WF (1970). A new aplacophoran from New Zealand. Journal of the Malacological Society of Australia 2, 47–54.
| A new aplacophoran from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Puillandre, N, Brouillet, S, and Achaz, G (2021). ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609–620.
| ASAP: assemble species by automatic partitioning.Crossref | GoogleScholarGoogle Scholar |
Revell, LJ (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.
| phytools: an R package for phylogenetic comparative biology (and other things).Crossref | GoogleScholarGoogle Scholar |
Saito, H, and Salvini-Plawen, L (2010). A new species of Anamenia (Mollusca: Solenogastres: Cavibelonia) from southern Japan. Venus 69, 1–15.
Salvini-Plawen, L (1978). Antarktische und Subantarktische Solenogastres – eine monographie: (1898–1974). [Antarctic and Subantarctic Solenogastres – a monograph: (1898–1974).] Zoologica 128, 1–315.
Salvini-Plawen L (1985) Early evolution and the primitive groups. In ‘The Mollusca. Vol. 10. Evolution’. (Eds ER Trueman, MR Clarke) pp. 59–150. (Academy Press: Orlando, FL, USA)
Salvini-Plawen, L (1997). Systematic revision of the Epimeniidae (Mollusca: Solenogastres). Journal of Molluscan Studies 63, 131–155.
| Systematic revision of the Epimeniidae (Mollusca: Solenogastres).Crossref | GoogleScholarGoogle Scholar |
Salvini-Plawen, L (2003). On the phylogenetic significance of the aplacophoran Mollusca. Iberus 21, 67–97.
Salvini-Plawen, L, and Steiner, G (2014). The Testaria concept (Polyplacophora + Conchifera) updated. Journal of Natural History 48, 2751–2772.
| The Testaria concept (Polyplacophora + Conchifera) updated.Crossref | GoogleScholarGoogle Scholar |
Scheltema, AH (1988). Ancestors and descendants – relationships of the Aplacophora and Polyplacophora. American Malacological Bulletin 6, 57–68.
Scheltema AH (1992) The Aplacophora: history, taxonomy, phylogeny, biogeography, and ecology. PhD thesis, Woods Hole Oceanographic Institution, MA, USA.
Scheltema, AH, and Ivanov, DL (2000). Prochaetodermatidae of the eastern Atlantic Ocean and Mediterranean Sea (Mollusca: Aplacophora). Journal of Molluscan Studies 66, 313–362.
| Prochaetodermatidae of the eastern Atlantic Ocean and Mediterranean Sea (Mollusca: Aplacophora).Crossref | GoogleScholarGoogle Scholar |
Scheltema, AH, and Jebb, M (1994). Natural history of a solenogaster mollusc from Papua New Guinea, Epimenia australis (Thiele) (Aplacophora: Neomeniomorpha). Journal of Natural History 28, 1297–1318.
| Natural history of a solenogaster mollusc from Papua New Guinea, Epimenia australis (Thiele) (Aplacophora: Neomeniomorpha).Crossref | GoogleScholarGoogle Scholar |
Scheltema, AH, and Schander, C (2000). Discrimination and phylogeny of solenogaster species through the morphology of hard parts (Mollusca, Aplacophora, Neomeniomorpha). The Biological Bulletin 198, 121–151.
| Discrimination and phylogeny of solenogaster species through the morphology of hard parts (Mollusca, Aplacophora, Neomeniomorpha).Crossref | GoogleScholarGoogle Scholar |
Scheltema, AH, Kerth, K, and Kuzirian, AM (2003). Original molluscan radula: comparisons among Aplacophora, Polyplacophora, Gastropoda, and the Cambrian fossil Wiwaxia corrugata. Journal of Morphology 257, 219–245.
| Original molluscan radula: comparisons among Aplacophora, Polyplacophora, Gastropoda, and the Cambrian fossil Wiwaxia corrugata.Crossref | GoogleScholarGoogle Scholar |
Scheltema, AH, Schander, C, and Kocot, KM (2012). Hard and soft anatomy in two genera of Dondersiidae (Mollusca, Aplacophora, Solenogastres). The Biological Bulletin 222, 233–269.
| Hard and soft anatomy in two genera of Dondersiidae (Mollusca, Aplacophora, Solenogastres).Crossref | GoogleScholarGoogle Scholar |
Smith, SA, Wilson, NG, Goetz, FE, Feehery, C, Andrade, SCS, Rouse, GW, Giribet, G, and Dunn, CW (2011). Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 480, 364–367.
| Resolving the evolutionary relationships of molluscs with phylogenomic tools.Crossref | GoogleScholarGoogle Scholar |
Thiele, J (1903). Proneomenia valdiviae n. sp. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899 3, 167–174.
| Proneomenia valdiviae n. sp.Crossref | GoogleScholarGoogle Scholar |
Todt, C (2013). Aplacophoran mollusks—still obscure and difficult? American Malacological Bulletin 31, 181–187.
| Aplacophoran mollusks—still obscure and difficult?Crossref | GoogleScholarGoogle Scholar |
Todt, C, and Kocot, KM (2014). New records for the solenogaster Proneomenia sluiteri (Mollusca) from Icelandic waters and description of Proneomenia custodiens sp. n. Polish Polar Research 35, 291–310.
| New records for the solenogaster Proneomenia sluiteri (Mollusca) from Icelandic waters and description of Proneomenia custodiens sp. n.Crossref | GoogleScholarGoogle Scholar |
Vinther, J, Sperling, EA, Briggs, DEG, and Peterson, KJ (2012). A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors. Proceedings of the Royal Society of London – B. Biological Sciences 279, 1259–1268.
| A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors.Crossref | GoogleScholarGoogle Scholar |
Wirén, A (1892). Studien über die Solenogastren. II. Chaetoderma productum, Neomenia, Proneomenia acuminata. [Studies on the Solenogastra. II. Chaetoderma productum, Neomenia, Proneomenia acuminata.] Kungliga Svenska Vetenskaps-Akademiens Handlingar 25, 1–99.
Wolter, K (1992). Ultrastructure of the radula apparatus in some species of aplacophoran molluscs. Journal of Molluscan Studies 58, 245–256.
| Ultrastructure of the radula apparatus in some species of aplacophoran molluscs.Crossref | GoogleScholarGoogle Scholar |
Zamarro, M, García-Álvarez, O, and Urgorri, V (2019). Biodiversity of the genus Hemimenia (Mollusca, Solenogastres, Neomeniamorpha) in Galician waters (NW Spain) with the description of three new species. Iberus 37, 177–207.
