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Using a combined approach to explain the morphological and ecological diversity in Phanogenia gracilis Hartlaub, 1893 (Echinodermata: Crinoidea) sensu lato: two species or intraspecific variation?

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Abstract

Phanogenia gracilis sensu lato is a shallow-water crinoid distributed throughout the Indo-western Pacific. The taxonomy of P. gracilis s.l. is clouded by the presence of two distinct morphotypes, each differing in morphology and ecology. The goal was to determine the taxonomic status of P. gracilis s.l. using partial gene sequences of two mitochondrial DNA genes, cytochrome oxidase c subunit I and NADH dehydrogenase subunit II, in conjunction with morphological and ecological data. The molecular phylogenies revealed three lineages separated by 5.0–6.6% corrected genetic distance, which is consistent with the genetic distances among other echinoderm species. Neither morphotype was monophyletic, nor was any examined morphological character exclusive to any one lineage. Discriminant function analysis (DFA) of the morphological and ecological data yielded significant results when grouping P. gracilis by morphotype and by clades recovered in the phylogenetic analyses, but grouping by sample locality was rejected. Although DFA results of grouping by clade were significant, jackknife support was weak, while only correctly grouping specimens by their respective clades 65% of the time. The results suggest the possibility of cryptic species, but additional molecular and morphological data are needed to confirm this. This study demonstrates the need to reevaluate the taxonomy of crinoid species and their respective diagnostic characters.

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References

  • Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap? 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. doi:https://doi.org/10.1093/molbev/msg028

    Article  CAS  Google Scholar 

  • Bradbury RH, Reichelt RE, Meyer DL, Birtles RA (1987) Patterns in the distribution of the crinoid community at Davies Reef on the central Great Barrier Reef. Coral Reefs 5:189–196. doi:https://doi.org/10.1007/BF00300962

    Article  Google Scholar 

  • Chen JC, Chang KH, Chen CP (1988) Shallow water crinoids of Kenting National Park, Taiwan. Bull Inst Zool Acad Sin 27(2):73–90

    Google Scholar 

  • Clark AH (1921) A monograph of the existing crinoids. Bull US Natl Mus 82:1–795 (57 plates)

    Google Scholar 

  • Clark AH (1931) A monograph of the existing crinoids. Bull US Natl Mus 82:1–816 (82 plates)

    Google Scholar 

  • Clark HL (1946) The echinoderm fauna of Australia. Publication No. 566. Carnegie Institute of Washington, Washington, DC

    Google Scholar 

  • Clark AM, Rowe FWE (1971) Shallow-water Indo-west Pacific echinoderms. British Museum: Natural History, London

    Google Scholar 

  • DeSalle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philos Trans R Soc Lond B Biol Sci 360:1905–1916. doi:https://doi.org/10.1098/rstb.2005.1722

    Article  CAS  Google Scholar 

  • Fabricius KE (1994) Spatial patterns in shallow-water crinoid communities on the Central Great Barrier Reef. Aust J Mar Freshw Res 45:1225–1236. doi:https://doi.org/10.1071/MF9941225

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:https://doi.org/10.2307/2408678

    Article  Google Scholar 

  • Gislén T (1940) A collection of crinoids from the South Sea Islands. Kungl Svenska Vetenskap Handlingar 18:1–16 (3 plates)

    Google Scholar 

  • Hart MW, Keever CC, Dartnall AJ, Byrne M (2006) Morphological and genetic variation indicate cryptic species within Lamarck’s little sea star, Parvulastra (= Patiriella) exigua. Biol Bull 210:158–167. doi:https://doi.org/10.2307/4134604

    Article  CAS  Google Scholar 

  • Hartlaub C (1891) Beitrag zur Kenntniss der Comatuliden-Fauna des Indischen Archipels. Nova Acta der Kaiserlische Leopoldinisch-Carolinisch Deutschen Akademie der Naturforsche 58:5–120 (5 plates)

    Google Scholar 

  • Hartlaub C (1893) Beitrag zur Kenntnis der Comatulidenfauna des Indischen Archipels. Nova Acta Kaiserl Leopoldina-Carolinea Deutschen Akad Naturforsch 58:1–120 (5 plates)

    Google Scholar 

  • Helgen LE, Rouse GW (2006) Species delimitation and distribution in Aporometra (Crinoidea: Echinodermata): endemic Australian featherstars. Invertebr Syst 20:395–414. doi:https://doi.org/10.1071/IS05050

    Article  CAS  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192. doi:https://doi.org/10.2307/2992540

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny, version 3.0. Bioinformatics 17:754–755. doi:https://doi.org/10.1093/bioinformatics/17.8.754

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688. doi:https://doi.org/10.1080/10635150290102366

    Article  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245. doi:https://doi.org/10.1093/bioinformatics/17.12.1244

    Article  CAS  Google Scholar 

  • Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in Tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975. doi:https://doi.org/10.1554/0014-3820(2001)055[0955:PSASIT]2.0.CO;2

    Article  CAS  Google Scholar 

  • Luning J (1992) Phenotypic plasticity of Daphnia pulex in the presence of invertebrate predators: morphological and life history responses. Oecologia 92:383–390. doi:https://doi.org/10.1007/BF00317464

    Article  Google Scholar 

  • Marchinko KB (2003) Dramatic phenotypic plasticity in barnacle legs (Balanus glandula Darwin): magnitude, age dependence, and speed of response. Evolution 57:1281–1290

    Article  Google Scholar 

  • Messing CG (1975) The systematics and distribution of the Crinoidea Comatulida (exclusive of Macrophreatina) collected by the R/V GERDA in the Straits of Florida and adjacent waters. M.S. thesis, University of Miami, 285 p

  • Messing CG (1994) Comatulid crinoids (Echinodermata) of Madang, Papua New Guinea, and environs: diversity and ecology. In: David B, Guille A, Feral JP, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 237–243

    Google Scholar 

  • Messing CG (1997) Living Comatulids. In: Waters J, Maples C (eds) Geobiology of Echinoderms. Paleontological Society Paper No. 3. Paleontological Society, Baltimore, pp 3–30

    Google Scholar 

  • Messing CG (1998a) An initial re-assessment of the distribution and diversity of the East Indian shallow-water crinoid fauna. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, pp 187–192

    Google Scholar 

  • Messing CG (1998b) Revision of the recent Indo-West Pacific comatulid genus Comaster Agassiz. Part 1. The type species of Comaster and Phanogenia Lovén (Echinodermata: Crinoidea: Comasteridae). Invertebr Taxon 12:191–209. doi:https://doi.org/10.1071/IT97004

    Article  Google Scholar 

  • Messing CG (2001) A key to the genera of Comasteridae (Echinodermata: Crinoidea) with the description of a new genus. Bull Biol Soc Wash 10:277–300

    Google Scholar 

  • Messing CG (2003) Unique morphology in the living bathyl feather star, Atelecrinus (Echinodermata: Crinoidea). Invertebr Biol 122:280–292

    Article  Google Scholar 

  • Messing CG (2007) The crinoid fauna (Echinodermata: Crinoidea) of Palau. Pac Sci 61(1):91–111. doi:https://doi.org/10.1353/psc.2007.0010

    Article  Google Scholar 

  • Meyer DL (1973) Feeding behavior and ecology of shallow-water unstalked crinoids (Echinodermata) in the Caribbean Sea. Mar Biol (Berl) 22:105–129. doi:https://doi.org/10.1007/BF00391776

    Article  Google Scholar 

  • Meyer DL, Macurda DB (1980) Ecology and distribution of shallow-water crinoids of Palau and Guam. Micronesica 16:59–99

    Google Scholar 

  • Mittelbach GG, Osenberg CW, Wainwright PC (1999) Variation in feeding morphology between pumpkinseed populations: phenotypic plasticity or evolution. Evol Ecol Res 1:111–128

    Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) A tool for editing and annotating multiple sequence alignments. Distributed by the authors

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi:https://doi.org/10.1080/10635150490522304

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:https://doi.org/10.1093/bioinformatics/14.9.817

    Article  CAS  Google Scholar 

  • Puorto G, Da Graca SM, Theakston RDG, Thorpe RS, Warrell DA (2001) Combining mitochondrial DNA sequences and morphological data to infer species boundaries: phylogeography of lancehead pitvipers in the Brazilian Atlantic forest, and the status of Bothrops pradoi (Squamata: Serpentes: Viperidae). J Evol Biol 14:527–538. doi:https://doi.org/10.1046/j.1420-9101.2001.00313.x

    Article  CAS  Google Scholar 

  • Rowe FWE, Hoggett AK, Birtles RA, Vail LL (1986) Revision of some comasterid genera from Australia (Echinodermata: Crinoidea), with descriptions of two new genera and nine new species. Zool J Linn Soc 86:197–277. doi:https://doi.org/10.1111/j.1096-3642.1986.tb01812.x

    Article  Google Scholar 

  • Sites JW Jr, Crandall KA (1997) Testing species boundaries in biodiversity studies. Conserv Biol 11:1289–1297

    Article  Google Scholar 

  • Stoletzki N, Schierwater B (2005) Genetic and color morph differentiation in the Caribbean sea anemone Condylactis gigantean. Mar Biol (Berl) 147:747–754. doi:https://doi.org/10.1007/s00227-005-1620-y

    Article  Google Scholar 

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony, (*and other methods), version 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:https://doi.org/10.1093/nar/25.24.4876

    Article  CAS  Google Scholar 

  • Trussell GC (2000) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54:151–166

    Article  CAS  Google Scholar 

  • Wiens JJ (2004) The role of morphological data in phylogeny reconstruction. Syst Biol 53:653–661. doi:https://doi.org/10.1080/10635150490472959

    Article  Google Scholar 

  • Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54:844–851. doi:https://doi.org/10.1080/10635150500354878

    Article  Google Scholar 

  • Wilson NG, Hunter RL, Lockhart SJ, Halanych KM (2007) Multiple lineages and absence of panmixia in the “circumpolar” crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica. Mar Biol (Berl) 152:895–904. doi:https://doi.org/10.1007/s00227-007-0742-9

    Article  Google Scholar 

  • Zmarzly DL (1985) The shallow-water crinoid fauna of Kwajalein Atoll, Marshall Islands: ecological observations, interatoll comparisons, and zoogeographic affinities. Pac Sci 39:340–358

    Google Scholar 

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Acknowledgments

We would like to thank the South Australian Museum, and Patrick and Lori Colin and Laura Martin of the Coral Reef Research Foundation, Koror, Palau, for the loan of specimens. We would also like to thank Andrea Scouras of Simon Fraser University for advice toward primer design and access to unpublished data, Vince Richards for the help with project design and data analysis, and the three anonymous reviewers for their constructive comments. This research was supported by a Nova Southeastern University President’s Faculty Research and Development Grant (2004–2005; Charles G. Messing and Mahmood S. Shivji) and an Australian Biological Resources Study Participatory Program Research Grant (Greg W. Rouse and Charles G. Messing).

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Correspondence to Christopher L. Owen.

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Communicated by U. Sommer.

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Owen, C.L., Messing, C.G., Rouse, G.W. et al. Using a combined approach to explain the morphological and ecological diversity in Phanogenia gracilis Hartlaub, 1893 (Echinodermata: Crinoidea) sensu lato: two species or intraspecific variation?. Mar Biol 156, 1517–1529 (2009). https://doi.org/10.1007/s00227-009-1173-6

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