A distinct phoronid larva: morphological and molecular evidence
Elena N. Temereva A C and Tatiana V. Neretina B
+ Author Affiliations
- Author Affiliations
A Dept. Invertebrate Zoology, Biological Faculty, Moscow State University, Vorobievy Gory 1, 12, 119992 Moscow, Russia.
B White Sea Biological Station, Biological Faculty, Moscow State University, Moscow, Russia.
C Corresponding author. Email: temereva@mail.ru
Invertebrate Systematics 27(6) 622-633 https://doi.org/10.1071/IS13023
Submitted: 19 May 2013 Accepted: 12 June 2013 Published: 20 December 2013
Abstract
Phoronids can be a major component of benthic and planktonic marine communities. Currently, the phoronid world fauna includes ten recognised species, known from adults; however, at least 32 larval forms have been described or documented. This study examined the morphology and 18S rRNA and 28S rRNA genes of two phoronid larvae abundant in Vostok Bay, Sea of Japan. One type was identified as the larval stage of Phoronopsis harmeri, although some distinctive features of this larva differ from the typical description. The morphological and molecular characteristics of the other larva did not match those of described species. According to our morphological results, this second actinotroch larva belongs to the genus Phoronis, but differs morphologically and molecularly from all the known species in the genus, all of which are represented in GenBank for the markers employed here. Taken together, our data suggest that the second actinotroch larva belongs to an undescribed phoronid species. The adult form of this actinotroch has never been identified, but our data suggest a close relationship with Phoronis pallida. The existence of a putative new phoronid species is also confirmed by presence of competent phoronid larvae, which are found in different aquatic areas, have a unique set of morphological features, and whose belonging is still not established.
Additional keywords: actinotroch, 18S rRNA, 28S rRNA, Phoronida, taxonomy.
References
Álvarez, F., Emig, C. C., Roldán, C., and Viéitez, J. M. (2005). Lophophorata: Phoronida, Brachiopoda. In: ‘Fauna Ibérica, vol. 27’. (Museo de Ciencias Naturales, CSIC: Madrid, Spain.) 273 pp.Andrews, E. A. (1890). On a new American species of the remarkable animal Phoronis. Annals & Magazine of Natural History 5, 445–449.
| On a new American species of the remarkable animal Phoronis.Crossref | GoogleScholarGoogle Scholar |
Brooks, W. K., and Cowles, R. P. (1905). Phoronis architecta: its life history, anatomy and breeding habits. Memoirs of the National Academy of Science 10, 72–113.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=fb309fc886ca0bad32dc0daac67aa1f7CAS | 15034147PubMed |
Emig, C. C. (1971). Taxonomie et systematique des Phoronidiens. Bulletin du Museum d’Histoire naturelle Paris (Zoologie) 8, 69–568.
Emig, C. C. (1972). Phoronidiens récoltés lors de la campagne ‘Biaçores’ du N/O Jean Charcot (3 Octobre–20 Novembre 1971). Tethys (Cornella de Llobregat) 4, 423–428.
Emig, C. C. (1982). The biology of Phoronida. Advances in Marine Biology 19, 2–90.
Emig, C. C. (1984). New data on the phoronids, Lophophorata, collected by Soviet expeditions. Biologiya Morya 4, 65–67.
Emig, C. C. (2013). Phoronida. Available at: http://www.com.univ-mrs.fr/DIMAR/Phoro/ [Accessed 24 July 2013]
Emig, C., and Golikov, A. (1990). On phoronids of the far eastern seas of the USSR and their distribution in the Pacific Ocean. Zoologicheskij Zhurnal 69, 22–30.
Forneris, L. (1959). Phoronidea from Brazil. Boletim do Instituto Océanographico 10, 1–105.
Garlitska, L., Neretina, T., Schepetov, D., Mugue, N., De Troch, M., Baguley, J., and Azovsky, A. (2012). Cryptic diversity of the ‘cosmopolitan’ harpacticoid copepod Nannopus palustris: genetic and morphological evidence. Molecular Ecology 21, 5336–5347.
| Cryptic diversity of the ‘cosmopolitan’ harpacticoid copepod Nannopus palustris: genetic and morphological evidence.Crossref | GoogleScholarGoogle Scholar | 22989315PubMed |
Giribet, G., Carranza, S., Baguñá, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
| First molecular evidence for the existence of a Tardigrada + Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVylur8%3D&md5=4c5b6d64e3e18a8fd7f3f6c62ccc683eCAS | 8583909PubMed |
Herrmann, K. (1979). Larvalentwicklung und Metamorphose von Phoronis psammophila (Phoronida, Tentaculata). Helgoländer Wissenschaftliche Meeresuntersuchungen 32, 550–581.
| Larvalentwicklung und Metamorphose von Phoronis psammophila (Phoronida, Tentaculata).Crossref | GoogleScholarGoogle Scholar |
Ikeda, I. (1901). Observation on the development, structure and metamorphosis of Actinotrocha. Journal of the College of Science, Imperial University, Tokyo 13, 507–591.
Johnson, K. B. (2001). Phoronida. In: ‘An Identification Guide to the Larval Marine Invertebrates of the Pacific Northwest’. (Ed. A. L. Shanks.) pp. 251–257. (Oregon State University Press: Corvallis, OR.)
Johnson, K. B., and Zimmer, R. L. (2002). Phylum Phoronida. In: ‘Atlas of Marine Invertebrate Larvae’. (Eds C. Young, M. Rice and M. Sewell.) pp. 429–439. (Academic Press: San Diego, CA.)
Litvaitis, M. K., Nunn, G., Thomas, W. K., and Kocher, T. D. (1994). A molecular approach for the identification of meiofaunal turbellarians (Platyhelminthes, Turbellaria). Marine Biology 120, 437–442.
| A molecular approach for the identification of meiofaunal turbellarians (Platyhelminthes, Turbellaria).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1OqtLo%3D&md5=14d2a36f9ebd45dcac229b9ce00a572fCAS |
Mamkaev, Yu. V. (1962). About phoronids of far eastern seas. Issledovaniya dal’nevostochnykh morei USSR 8, 219–237.
Marsden, J. (1959). Phoronidea from the Pacific coast of North America. Canadian Journal of Zoology 37, 87–111.
| Phoronidea from the Pacific coast of North America.Crossref | GoogleScholarGoogle Scholar |
Metschnikoff, E. (1871). Ueber Metamorphose einiger Seethiere. III. Ueber Actinotrocha. Zeitschrift fur Wissenschartliche Zoologie 21, 286–313.
Müller, J. (1846). Bericht uber einige Tierformen der Nordsee. Archiv für Anatomie and Physiologie 13, 101–104.
Omelyanenko, V. A., and Kulikova, V. A. (2011). Pelagic larvae of benthic invertebrates of the Vostok Bay, Peter the Great Bay, Sea of Japan: composition, phenology, and population dynamics. Russian Journal of Marine Biology 37, 7–22.
| Pelagic larvae of benthic invertebrates of the Vostok Bay, Peter the Great Bay, Sea of Japan: composition, phenology, and population dynamics.Crossref | GoogleScholarGoogle Scholar |
Posada, D., and Crandall, K. A. (2001). Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580–601.
| Selecting the best-fit model of nucleotide substitution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVOmuw%3D%3D&md5=981075d011b72c670edf6ffc5408c7b8CAS | 12116655PubMed |
Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=c60b5f7b2a55d284223f3a076ea93fe5CAS | 12912839PubMed |
Santagata, S. (2002). Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evolution & Development 4, 28–42.
| Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida).Crossref | GoogleScholarGoogle Scholar |
Santagata, S. (2004). A waterborne behavioral cue for the actinotroch larvae of Phoronis pallida (Phoronida) produced by Upogebia pugettensis (Decapoda: Thalassinidea). The Biological Bulletin 207, 103–115.
| A waterborne behavioral cue for the actinotroch larvae of Phoronis pallida (Phoronida) produced by Upogebia pugettensis (Decapoda: Thalassinidea).Crossref | GoogleScholarGoogle Scholar | 15501852PubMed |
Santagata, S., and Cohen, B. (2009). Phoronid phylogenetics (Brachiopoda; Phoronata): evidence from morphological cladistics, small and large subunit rDNA sequences, and mitochondrial cox1. Zoological Journal of the Linnean Society 157, 34–50.
| Phoronid phylogenetics (Brachiopoda; Phoronata): evidence from morphological cladistics, small and large subunit rDNA sequences, and mitochondrial cox1.Crossref | GoogleScholarGoogle Scholar |
Santagata, S., and Zimmer, R. L. (2002). Comparison of the neuromuscular system among actinotroch larvae: systematic and evolutionary implications. Evolution & Development 4, 43–54.
| Comparison of the neuromuscular system among actinotroch larvae: systematic and evolutionary implications.Crossref | GoogleScholarGoogle Scholar |
Selys-Longchamps, M. (1907). Phoronis. Fauna und Flora des Golfes von Neapel. Monograph 30, 280 .
Silén, L. (1954). Developmental biology of Phoronidea of the Gullmar Fiord area (west coast of Sweden). Acta Zoologica (Stockholm, Sweden) 35, 215–257.
| Developmental biology of Phoronidea of the Gullmar Fiord area (west coast of Sweden).Crossref | GoogleScholarGoogle Scholar |
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=fd9be04d282e64e6ed94338c1130bc17CAS | 21546353PubMed |
Temereva, E. N. (2005). Phylum Phoronids. In: ‘Biota of the Russian basin of the Sea of Japan. Vol. 3. Brachiopoda and Phoronida’. (Ed. A.V. Adrianov.) pp. 50–136. (Dalnauka: Vladivostok, Russia.)
Temereva, E. N. (2009). New data on distribution, morphology and taxonomy of phoronid larvae (Phoronida, Lophophorata). Invertebrate Zoology 6, 47–64.
Temereva, E. N., and Malakhov, V. V. (2004). Key to the phoronid larvae (Phoronida, Lophophorata) from the Sea of Japan. Zoologicheskij Zhurnal 83, 1115–1126.
Temereva, E. N., Malakhov, V. V., and Chernyshev, A. V. (2006). Giant actinotroch, a larva of Phoronida from the South China Sea: the giant larva phenomenon. Doklady Biological Sciences 410, 1–4.
Temereva, E. N., and Malakhov, V. V. (2007). Embryogenesis and larval development of phoronid Phoronopsis harmeri Pixell, 1912: dual origin of the coelomic mesoderm. Invertebrate Reproduction & Development 50, 57–66.
| Embryogenesis and larval development of phoronid Phoronopsis harmeri Pixell, 1912: dual origin of the coelomic mesoderm.Crossref | GoogleScholarGoogle Scholar |
Temereva, E. N., and Neretina, T. V. (2012). World fauna of phoronid larvae: the existence of unknown phoronid species. Abstracts of Xth International Larval Biology Symposium. July 30–August 3. Berkeley, CA, USA. 66–67.
Vyshkvartzev, D. I., Lebedev, E. B., and Kalashnikov, V. Z. (1990). Consequences of the typhoon ‘Vera’: casting of invertebrates on a sandy spit in Possjet Bay of the Sea of Japan. Russian Journal of Marine Biology 5, 78–80.
Waddell, P. J., and Steel, M. A. (1997). General-time reversible distances with unequal rates across sites: mixing G and inverse Gaussian distribution with invariant sites. Molecular Phylogenetics and Evolution 8, 398–414.
| General-time reversible distances with unequal rates across sites: mixing G and inverse Gaussian distribution with invariant sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVensA%3D%3D&md5=667cc37fdb59d12b26d920d9b9986d09CAS | 9417897PubMed |
Whiting, M. F., Carpenter, J. M., Wheeler, Q. D., and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.
| 1:STN:280:DC%2BD383js1yqtQ%3D%3D&md5=a9245cf9f037d3c680ee93e07e809a2dCAS | 11975347PubMed |
Wilson, E. B. (1881). The origin and significance of the metamorphosis of Actinitrocha. Quarterly Journal of Microscopical Science 21, 202–218.
Zimmer, R. L. (1964). Reproductive biology and development of Phoronida. Dissertation, University of California.
Zimmer, R. L. (1978). The comparative structure of the preoral hood coelom in Phoronida and the fate of this cavity during and metamorphosis. In: ‘Settlement and Metamorphosis of Marine Invertebrate Larvae’. (Eds F. S. Chia and M. E. Rice.) pp. 23–40. (Elsevier: New York.)
Zimmer, R. L. (1991). Phoronida. In: ‘Reproduction of Marine Invertebrates. Vol. 4. Echinoderms and Lophophorates’. (Eds A. C. Giese, J. S. Pearse and V. B. Pearse.) pp. 1–45. (Boxwood Press: Pacific Grove, CA.)
