Living with a giant parchment tube worm: a description of a new nudibranch species (Gastropoda: Heterobranchia) associated with the annelid Chaetopterus
- 163 Downloads
Abstract
Small fionid nudibranch specimens collected within a Chaetopterus sp. tube worm are described here as a new species Tenellia chaetopterana sp. nov. This case is the first example of symbiotic association between a mollusk and an annelid host amongst cladobranch sea slugs. The external morphology of this species suggests it is adapted for living inside the worm’s tube: flattened body, laterally directed cerata and rhinophores, and wide foot. Molecular data, including partial sequences of mitochondrial COI and 16S and nuclear H3 genes, indicates that this species is distinct from other members of the genus Tenellia as well as other fionids. The species is close to the coral-feeding fionids of the genus Tenellia (formerly in genus Phestilla) in several morphological characters such as general radula morphology, absence of cnidosacs, and flattened body shape, as well as by molecular data. Tenellia chaetopterana sp. nov. has unique biology, implicating possible diversity previously overlooked by nudibranch faunistic studies.
Keywords
Nudibranchia Fionidae Symbiotic associations Endoecism Integrative systematics Molecular phylogenyNotes
Acknowledgments
We are deeply grateful to Prof. Temir Britayev and Prof. Daniel Martin for their intense efforts in organization of Chaetopterus symbiotic communities studies and for valuable help in the fieldwork. Elena Mekhova helped in collecting and procssing of the living Chaetopterus specimens. Ángel Valdés, Maria Stanovova, and two anonymous reviewers are owed special thanks for constructive criticism that improved the manuscript. We also want to thank the staff of the Electron Microscopy Cabinet of Severtsov Institute of Ecology and Evolution of RAS, staff of the Cooperative Laboratory of Electron Microscopy of Moscow State University, and the staff of the Cooperative Far Eastern Center of Electron Microscopy for providing SEM facilities. Molecular study was conducted using equipment of the Core Centrum of Institute of Developmental Biology RAS. Field explorations were supported by Russian Science Foundation grant no. 14-14-01179 and funding provided by the Vietnam-Russia Tropical Center to YD. Morphological and molecular studies were supported by Russian Science Foundation grant no. 14-50-00034 to IE.
Supplementary material
References
- Anker A, Murina GV, Lira C et al (2005) Macrofauna associated with Echiuran burrows: a review with new observations of the innkeeper worm, Ochetostoma erythrogrammon Leuckart and Rüppel, in Venezuela. Zool Stud 44:157–190. https://doi.org/10.1007/s12630-011-9640-1 Google Scholar
- Behrens DW (1998) Cuthona rolleri Behrens and Gosliner, 1988. http://slugsite.tierranet.com/nudwk/nudwk130.htm. Accessed 14 Feb 2017
- Behrens DW, Gosliner TM (1988) A new species of tergipedid nudibranch from Morro Bay, California. Veliger 31:262–266Google Scholar
- Bouchet P (2010) Fionidae. MolluscaBase. World Register of Marine Species. http://marinespecies.org/aphia.php?p=taxdetails&id=23039. Accessed 11 May 2017
- Britayev TA, Mekhova E, Deart Y, Martin D (2017) Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae). PeerJ 5:e2930. https://doi.org/10.7717/peerj.2930 CrossRefPubMedPubMedCentralGoogle Scholar
- Brown GH (1980) The British species of the aeolidacean family Tergipedidae (Gastropoda: Opisthobranchia) with a discussion of the genera. Zool J Linnean Soc 69:225–255CrossRefGoogle Scholar
- Burghardt I, Schrödl M, Wägele H (2008) Three new solar-powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidioidea) from the tropical indo-Pacific, with analysis of their photosynthetic activity and notes on biology. J Molluscan Stud 74:277–292CrossRefGoogle Scholar
- Calado G, Urgorri V (2002) A new species of Calma Alder & Hancock, 1855 (Gastropoda: Nudibranchia) with a review of the genus. J Molluscan Stud 68:311–317CrossRefGoogle Scholar
- Cámara S, Carmona L, Cella K et al (2014) Tergipes tergipes (Förskal, 1775) (Gastropoda: Nudibranchia) is an amphiatlantic species. J Molluscan Stud 80:642–646. https://doi.org/10.1093/mollus/eyu015 CrossRefGoogle Scholar
- Carmona L, Pola M, Gosliner TM, Cervera JL (2013) A tale that morphology fails to tell: a molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS One 8:e63000. https://doi.org/10.1371/journal.pone.0063000 CrossRefPubMedPubMedCentralGoogle Scholar
- Cella K, Carmona L, Ekimova I et al (2016) A radical solution: the phylogeny of the Nudibranch family Fionidae. PLoS One 11:1–32. https://doi.org/10.1371/journal.pone.0167800 CrossRefGoogle Scholar
- Chichvarkhin AY, Ekimova I, Egorova E, Chichvarkhina OV (2016) Species identity of a nudibranch mollusk of the genus Cuthona associated with hermit crabs in the sea of Japan. Biol Morya 42:449–457 [in Russian]Google Scholar
- Colgan DJ, McLauchlan A, Wilson GDF et al (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust J Zool 46:419. https://doi.org/10.1071/ZO98048 CrossRefGoogle Scholar
- Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
- Faucci A, Toonen RJ, Hadfield MG (2007) Host shift and speciation in a coral-feeding nudibranch. Proc R Soc B 274:111–119. https://doi.org/10.1098/rspb.2006.3685 CrossRefPubMedGoogle Scholar
- Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299. https://doi.org/10.1371/journal.pone.0013102 PubMedGoogle Scholar
- Gosliner TM (1979) The systematics of the Aeolidacea (Nudibranchia: Mollusca) of the Hawaiian islands, with descriptions of two new species. Pac Sci 33:37–77Google Scholar
- Gosliner TM (1981) A new species of tergipedid nudibranch from the coast of California. J Molluscan Stud 47:200–205Google Scholar
- Gosliner TM, Valdés A, Beherens DW (2015) Nudibranch and sea slug identification: indo-Pacific. New World Press, JacksonvilleGoogle Scholar
- Hadfield MG (1977) Chemical interactions in larval settling of a marine gastropod. In: Faulkner DJ, Fenical WH (eds) Marine natural products chemistry. Plenum Publishing Company, New York, pp 403–413CrossRefGoogle Scholar
- Harris LG (1975) Studies on the life history of two coral-eating nudibranchs of the genus Phestilla. Biol Bull 149:539–550CrossRefGoogle Scholar
- Henry SM (1966) Symbiosis. I. Associations of microorganisms, plants and marine organisms. Academic Press, New YorkGoogle Scholar
- Huelsenbeck JP, Bull JJ, Cunningham CW (1996) Combining data in phylogenetic analysis. Trends Ecol Evol 11:152–158. https://doi.org/10.1016/0169-5347(96)10006-9 CrossRefPubMedGoogle Scholar
- Jörger KM, Norenburg JL, Wilson NG, Schrödl M (2012) Barcoding against a paradox? Combined species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evol Biol 12:245. https://doi.org/10.1186/1471-2148-12-245
- Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
- Lambert WJ (1991) Coexistence of hydroid eating nudibranchs: do feeding biology and habitat use matter? Biol Bull 181:248–260CrossRefGoogle Scholar
- Lê HLV, Lecointre G, Perasso R (1993) A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Mol Phylogenet Evol 2:31–51CrossRefPubMedGoogle Scholar
- Marcus E, Marcus E (1970) Opisthobranchs from Curaçao and faunistically related regions. Stud Fauna Curacao 33:1–129Google Scholar
- Martin D, Britayev TA (1998) Symbiotic polychaetes: review of known species. Oceanogr Mar Biol Ann Rev 36:217–340Google Scholar
- Martynov AV, Sanamyan NP, Korshunova TA (2015) New data on the opisthobranch molluscs (Gastropoda: Opisthobranchia) of waters if commander islands and far-eastern seas of Russia. In: Bugaev VF, Tokranov AM, Chernyagina OA (eds) Conservation of biodiversity of Kamchatka and coastal waters. Proceedings of XV international scientific conference. Kamchatpress, Petropavlovsk-Kamchatsky, pp 55–69 [In Russian]Google Scholar
- Miller MC (1977) Aeolid nudibranchs (Gastropoda: Opisthobranchia) of the family Tergipedidae from New Zealand waters. Zool J Linnean Soc 60:197–222CrossRefGoogle Scholar
- Miller SE, Hadfield MG (1986) Ontogeny of phototaxis and metamorphic competence in larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). J Exp Mar Biol Ecol 97(1):95–112CrossRefGoogle Scholar
- Morton B (1989) Partnerships in the Sea - Hong Kong`s Marine Symbioses. Hong Kong University Press, Hong Kong. 140 pGoogle Scholar
- Palumbi SR, Kessing B, Martin A (1991) The simple fool’s guide to PCR, 2nd ed. Department of zoology, University of Hawaii, Honolulu, pp 12Google Scholar
- Pola M, Gosliner TM (2010) The first molecular phylogeny of cladobranchian opisthobranchs (Mollusca, Gastropoda, Nudibranchia). Mol Phylogenet Evol 56:931–941. https://doi.org/10.1016/j.ympev.2010.05.003 CrossRefPubMedGoogle Scholar
- Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x CrossRefPubMedGoogle Scholar
- Puslednik L, Serb JM (2008) Molecular phylogenetics of the Pectinidae (Mollusca: Bivalvia) and effect of increased taxon sampling and outgroup selection on tree topology. Mol Phylogenet Evol 48:1178–1188. https://doi.org/10.1016/j.ympev.2008.05.006 CrossRefPubMedGoogle Scholar
- Ritson-Williams R, Shjegstad S, Paul V (2003) Host specificity of four corallivorous Phestilla nudibranchs (Gastropoda: Opisthobranchia). Mar Ecol Prog Ser 255:207–218CrossRefGoogle Scholar
- Roginskaya IS (1970) Tenellia adspersa, a nudibranch new to the Azov Sea, with notes on its taxonomy and ecology. Malacol Rev 3:167–174Google Scholar
- Roginskaya IS (1987) Order Nudibranchia Blainville, 1814. In: Starobogatov YI, Naumov AD (eds) Molluscs of the White Sea. Keys to the Fauna of USSR. Nauka, Leningrad, pp 155–201 [in Russian]Google Scholar
- Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804. https://doi.org/10.1038/nature02053 CrossRefPubMedGoogle Scholar
- Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
- Rudman WB (1979) The ecology and anatomy of a new species of aeolid opisthobranch mollusc; a predator of the scleractinian coral Porites. Zool J Linnean Soc 4:339–350CrossRefGoogle Scholar
- Rudman WB (1981) Further studies on the anatomy and ecology of opisthobranch molluscs feeding on the scleractinian coral Porites. Zool J Linnean Soc 71:373–412CrossRefGoogle Scholar
- Sukumaran J, Holder MT (2010) DendroPy: a python library for phylogenetic computing. Bioinformatics 26:1569–1571. https://doi.org/10.1093/bioinformatics/btq228 CrossRefPubMedGoogle Scholar
- Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164 CrossRefPubMedGoogle Scholar
- Wägele M, Johnsen G (2001) Observations on the histology and photosynthetic performance of “solar-powered” opisthobranchs (Mollusca, Gastropoda, Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Org Div Evol 1:193–210CrossRefGoogle Scholar
- Wagner D, Kahng SE, Toonen RJ (2009) Observations on the life history and feeding ecology of a specialized nudibranch predator (Phyllodesmium poindimiei), with implications for biocontrol of an invasive octocoral (Carijoa riisei) in Hawaii. J Exp Mar Biol Ecol 372:64–74CrossRefGoogle Scholar
- Williams JD, McDermott JJ (2004) Hermit crab biocoenoses: a worldwide review of diversity and natural history of hermit crab associates. J Exp Mar Biol Ecol 305:1–128. https://doi.org/10.1016/j.jembe.2004.02.020 CrossRefGoogle Scholar
- Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas, AustinGoogle Scholar