To be or not to be? What molecules say about Runcina brenkoae Thompson, 1980 (Gastropoda: Heterobranchia: Runcinida)

Authors

  • Ana Karla Araujo Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEIMAR), Universidad de Cádiz https://orcid.org/0000-0001-5305-6700
  • Marta Pola Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid https://orcid.org/0000-0003-0518-346X
  • Manuel Antonio E. Malaquias Section of Taxonomy and Evolution, Department of Natural History, University Museum of Bergen https://orcid.org/0000-0002-9668-945X
  • Juan Lucas Cervera Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEIMAR), Universidad de Cádiz - Instituto Universitario de Investigación Marina (INMAR), Campus de Excelencia Internacional del Mar (CEIMAR), Universidad de Cádiz https://orcid.org/0000-0002-8337-2867

DOI:

https://doi.org/10.3989/scimar.04907.07A

Keywords:

Runcinida, DNA barcoding, species delimitation, integrative taxonomy, biodiversity, phylogeny

Abstract


Runcinids are poorly known minute marine slugs inhabiting intertidal and shallow subtidal rocky shores. Among the European species, Runcina brenkoae, described from the Adriatic Sea in the Mediterranean, has been described to display chromatic variability, placing in question the true identity and geographic distribution of the species. In this paper we investigate the taxonomic status of R. brenkoae based on specimens from the central and western Mediterranean Sea and the southern Iberian coastline of Portugal and Spain, following an integrative approach combining multi-locus molecular phylogenetics based on the mitochondrial markers cytochrome c oxidase subunit I and 16S rRNA and the nuclear gene histone H3, together with the study of morpho-anatomical characters investigated by scanning electron microscopy. To aid in species delimitation, the Automatic Barcode Gap Discovery and Bayesian Poisson tree process methods were employed. Our results indicate the existence of a complex of three species previously identified as R. brenkoae, namely two new species here described (R. marcosi n. sp. and R. lusitanica n. sp.) and R. brenkoae proper.

Downloads

Download data is not yet available.

References

Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723. https://doi.org/10.1109/TAC.1974.1100705

Alfaro M.E., Zoller S., Lutzoni F. 2003. Bayes or bootstraps? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol. Biol. Evol. 20: 255-266. https://doi.org/10.1093/molbev/msg028 PMid:12598693

Austin J., Gosliner T., Malaquias M.A.E. 2018. Systematic revision, diversity patterns, and trophic ecology of the tropical Indo-West Pacific sea slug genus Phanerophthalmus A. Adams, 1850 (Cephalaspidea, Haminoeidae). Invertebr. Syst. 32: 1336-1387. https://doi.org/10.1071/IS17086

Ballesteros M., Madrenas E., Pontes M. 2016. Actualización del catálogo de los moluscos opistobranquios (Gastropoda: Heterobranchia) de las costas catalanas. Spira 6: 1-28.

Burn R. 1963. Australian Runcinacea (Mollusca, Gastropoda). Aust. Zool. 13: 9-22.

Burn R., Thompson T.E. 1998. Order Cephalaspidea. In: Beesley P.L, Ross G.J.B., Wells A. (eds), Mollusca: The Southern Synthesis. Fauna of Australia. Vol. 5. Part B, CSIRO Publishing, Melbourne, pp. 565-1234.

Cervera J.L., García-Gómez J.L., García F.J. 1991. The genus Runcina Forbes and Haley, 1851 (Opisthobranchia: Cephalaspidea) in the Strait of Gibraltar, with the description of a new species from the bay of Algeciras. J. Moll. Stud. 57: 199-208. https://doi.org/10.1093/mollus/57.Supplement_Part_4.199

Cervera J.L., Calado G., Gavaia C., et al. 2004. An annotated and updated checklist of the opisthobranchs (Mollusca: Gastropoda) from Spain and Portugal (including islands and archipelagos). Bol. Inst. Esp. Oceanogr. 20: 1-122.

Chernyshev A.V. 2006. New data on mollusks of the family Runcinidae (Gastropoda: Opisthobranchia) from Russian Far Eastern seas. Bull. Russian 10: 122-125.

Colgan D., McLauchlan A., Wilson G.D.F., et al. 1998. Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust. J. Zool. 46: 419-437. https://doi.org/10.1071/ZO98048

Darriba D., Taboada G.L., Doallo R., et al. 2012. jModelTest2: more models, new heuristics and parallel computing. Nat. Methods 9: 696-704. https://doi.org/10.1038/nmeth.2109 PMid:22847109 PMCid:PMC4594756

Drummond A.J., Ashton B., Cheung M., et al. 2009. GENEIOUS v4.6. Available from: http://www.geneious.com/

Folmer R.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.

Ghiselin T. 1963. On the functional and comparative anatomy of Runcina setoensis Baba, an opisthobranch gastropod. Publ. Seto Mar. Biol. Lab. 11: 389-398. https://doi.org/10.5134/175336

Gosliner T.M. 1991. Four new species and a new genus of opisthobranch gastropods from the Pacific coast of North America. The Veliger 34: 272-290.

Guindon S., Gascuel O. 2003. A simple, fast, and accurate method to estimate large phylogenies by maximum-liklihood. Syst. Biol. 52: 696-704. https://doi.org/10.1080/10635150390235520 PMid:14530136

Hillis D.M., Bull J.J. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42: 182-192. https://doi.org/10.1093/sysbio/42.2.182

Jörger K.M., Stöger I., Kano Y., et al. 2010. On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evol. Biol. 10: 323. https://doi.org/10.1186/1471-2148-10-323 PMid:20973994 PMCid:PMC3087543

Katoh K., Asimenos G., Toh H. 2009. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537: 39-64. https://doi.org/10.1007/978-1-59745-251-9_3 PMid:19378139

Korshunova T.A., Picton B., Furfaro G., et al. 2019. Multilevel fine-scale diversity challenges the 'cryptic species' concept. Sci. Rep. 9: 6732. https://doi.org/10.1038/s41598-019-42297-5 PMid:31043629 PMCid:PMC6494890

Kress A. 1977. Runcina ferruginea n. sp. (Opisthobranchia: Cephalaspidea), a new runcinid from Great Britain. J. Mar. Biol. Assoc. UK 57: 201-211. https://doi.org/10.1017/S0025315400021342

Krug P.J., Berriman J.S., Valdés Á. 2018. Phylogenetic systematics of the shelled sea slug genus Oxynoe Rafinesque, 1814 (Heterobranchia: Sacoglossa), with integrative descriptions of seven new species. Invertebr. Syst. 32: 950-1003. https://doi.org/10.1071/IS17080

Kumar S., Stecher G., Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. https://doi.org/10.1093/molbev/msw054 PMid:27004904

Layton K.K.S., Gosliner T.M., Wilson N.G. 2018. Flexible colour patterns obscure identification and mimicry in Indo-Pacific Chromodoris nudibranchs (Gastropoda: Chromodorididae). Mol. Phylog. Evol. 124: 27-36. https://doi.org/10.1016/j.ympev.2018.02.008 PMid:29476907

Maddison W.P., Maddison D.R. 2018. Mesquite: a modular system for evolutionary analysis. http://www.mesquiteproject.org

Malaquias M.A.E., Mackenzie-Dodds J., Bouchet P., et al. 2009. A molecular phylogeny of the Cephalaspidea sensu lato (Gastropoda: Euthyneura): Architectibranchia redefined and Runcinacea reinstated. Zool. Scr. 38: 23-41. https://doi.org/10.1111/j.1463-6409.2008.00354.x

Moro L., Ortea J. 2015. Nuevos taxones de babosas marinas de las islas Canarias y de Cabo Verde (Mollusca: Heterobranchia). Vieraea 43: 21-86.

Odhner N.H. 1968. Sous-Classe des Opisthobranches. In: Franc A., Grassé P.P. (ed.) Traité de Zoologie 5: 608-893, Masson, Paris.

Ortea J., Moro L., Bacallado J.J. 2015. Babosas Marinas Canarias. Turquesa Ed., Tenerife, 144 pp.

Oskars T.R., Bouchet P., Malaquias, M.A.E. 2015. A new phylogeny of the Cephalaspidea (Gastropoda: Heterobranchia) based on expanded taxon sampling and gene markers. Mol. Phylog. Evol. 89: 130-150. https://doi.org/10.1016/j.ympev.2015.04.011 PMid:25916189

Padula V., Araújo A.K., Matthews-Cascon H., et al. 2014. Is the Mediterranean nudibranch Cratena peregrina (Gmelin, 1791) present on the Brazilian coast? Integrative species delimination and description of Cratena minor n. sp. J. Moll. Stud. 80: 575-584. https://doi.org/10.1093/mollus/eyu052

Palumbi S.R., Martin A., Roman S., et al. 1991. The Simple Fools' Guide to PCR. Dept. Zoology & Kewalo Laboratory, Univ. Hawaii, 46 pp. https://palumbilab.stanford.edu/SimpleFoolsMaster.pdf

Puillandre N., Lambert A., Brouillet S., et al. 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 PMid:21883587

Rambaut A., Drummond A.J., Xie D., et al. 2018. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst. Biol. 67: 901-904. https://doi.org/10.1093/sysbio/syy032 PMid:29718447 PMCid:PMC6101584

Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. https://doi.org/10.1093/bioinformatics/btg180 PMid:12912839

Schmekel L. 1985. Aspects of evolution within the opisthobranchs. In Trueman E.R., Clarke M.R. (eds) The Mollusca, Evolution, 10. Academic Press, Orlando: New York. pp. 221-267. https://doi.org/10.1016/B978-0-12-751410-9.50013-7

Schmekel L., Capellato D. 2001. Contributions to the Runcinidae. I. Six new species of the genus Runcina (Opisthobranchia Cephalaspidea) in the Mediterranean. Vie Milieu 51: 141-160.

Schmekel L., Capellato D. 2002. Contributions to the Runcinidae. II. Three new species and comparative studies on five stablished species of Runcina (Opisthobranchia Cephalaspidea) in the Mediterranean. Vie Milieu 52: 85-102.

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic anaslysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. https://doi.org/10.1093/bioinformatics/btu033 PMid:24451623 PMCid:PMC3998144

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 PMid:17654362

Thompson T.E. 1976. Biology of Opisthobranch Molluscs. Vol I. The Ray Society, London, 207 pp.

Thompson T.E. 1980. New species of the bullomorph genus Runcina from the northern Adriatic Sea. J. Moll. Stud. 46: 154-157.

Thompson T.E., Brodie G. 1988. Eastern Mediterranean Opisthobranchia: Runcinidae (Runcinacea), with a review of Runcinid classification and a description of a new species from Fiji. J. Moll. Stud. 54: 339-346. https://doi.org/10.1093/mollus/54.3.339

Vayssière A. 1883. Recherches anatomiques sur les genres Pelta (Runcina) et Tylodina. Ann. Sci. Nat. Zool. 15: 1-46.

Wägele H., Klussmann-Kolb A., Verbeek E., et al. 2014. Flashback and foreshadowing - a review of the taxon Opisthobranchia. Org. Divers. Evol. 14: 133-149. https://doi.org/10.1007/s13127-013-0151-5

Zhang J., Kapli P., Pavlidis P., et al. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869-2876. https://doi.org/10.1093/bioinformatics/btt499 PMid:23990417 PMCid:PMC3810850

Published

2019-09-30

How to Cite

1.
Araujo AK, Pola M, Malaquias MAE, Cervera JL. To be or not to be? What molecules say about Runcina brenkoae Thompson, 1980 (Gastropoda: Heterobranchia: Runcinida). Sci. mar. [Internet]. 2019Sep.30 [cited 2024Apr.25];83(3):223-35. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1816

Issue

Section

Articles