Advertisement

Marine Biology

, Volume 156, Issue 8, pp 1517–1529 | Cite as

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?

  • Christopher L. Owen
  • Charles G. Messing
  • Greg W. Rouse
  • Mahmood S. Shivji
Original Paper

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.

Keywords

Bayesian Inference Discriminant Function Analysis NADH Dehydrogenase Subunit Articular Facet Discriminant Function Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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 We would also like to thank Andrea Scouras of Simon Fraser University for advice toward primer design and access to unpublished data, Vince Richards for the help with project design and data analysis, and the three anonymous reviewers for their constructive comments.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).

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. Chen JC, Chang KH, Chen CP (1988) Shallow water crinoids of Kenting National Park, Taiwan. Bull Inst Zool Acad Sin 27(2):73–90Google Scholar
  4. Clark AH (1921) A monograph of the existing crinoids. Bull US Natl Mus 82:1–795 (57 plates)Google Scholar
  5. Clark AH (1931) A monograph of the existing crinoids. Bull US Natl Mus 82:1–816 (82 plates)Google Scholar
  6. Clark HL (1946) The echinoderm fauna of Australia. Publication No. 566. Carnegie Institute of Washington, Washington, DCGoogle Scholar
  7. Clark AM, Rowe FWE (1971) Shallow-water Indo-west Pacific echinoderms. British Museum: Natural History, LondonGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi: https://doi.org/10.2307/2408678 CrossRefGoogle Scholar
  11. Gislén T (1940) A collection of crinoids from the South Sea Islands. Kungl Svenska Vetenskap Handlingar 18:1–16 (3 plates)Google Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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
  14. 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
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. Marchinko KB (2003) Dramatic phenotypic plasticity in barnacle legs (Balanus glandula Darwin): magnitude, age dependence, and speed of response. Evolution 57:1281–1290CrossRefGoogle Scholar
  23. 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 pGoogle Scholar
  24. 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 237–243Google Scholar
  25. Messing CG (1997) Living Comatulids. In: Waters J, Maples C (eds) Geobiology of Echinoderms. Paleontological Society Paper No. 3. Paleontological Society, Baltimore, pp 3–30Google Scholar
  26. 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 187–192Google Scholar
  27. 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 CrossRefGoogle Scholar
  28. Messing CG (2001) A key to the genera of Comasteridae (Echinodermata: Crinoidea) with the description of a new genus. Bull Biol Soc Wash 10:277–300Google Scholar
  29. Messing CG (2003) Unique morphology in the living bathyl feather star, Atelecrinus (Echinodermata: Crinoidea). Invertebr Biol 122:280–292CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. Meyer DL, Macurda DB (1980) Ecology and distribution of shallow-water crinoids of Palau and Guam. Micronesica 16:59–99Google Scholar
  33. Mittelbach GG, Osenberg CW, Wainwright PC (1999) Variation in feeding morphology between pumpkinseed populations: phenotypic plasticity or evolution. Evol Ecol Res 1:111–128Google Scholar
  34. Nicholas KB, Nicholas HB Jr (1997) A tool for editing and annotating multiple sequence alignments. Distributed by the authorsGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. Sites JW Jr, Crandall KA (1997) Testing species boundaries in biodiversity studies. Conserv Biol 11:1289–1297CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. Swofford DL (2002) PAUP* phylogenetic analysis using parsimony, (*and other methods), version 4.0b10. Sinauer, SunderlandGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. Trussell GC (2000) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54:151–166CrossRefGoogle Scholar
  44. Wiens JJ (2004) The role of morphological data in phylogeny reconstruction. Syst Biol 53:653–661. doi: https://doi.org/10.1080/10635150490472959 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. Zmarzly DL (1985) The shallow-water crinoid fauna of Kwajalein Atoll, Marshall Islands: ecological observations, interatoll comparisons, and zoogeographic affinities. Pac Sci 39:340–358Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Christopher L. Owen
    • 1
    • 2
  • Charles G. Messing
    • 1
  • Greg W. Rouse
    • 3
  • Mahmood S. Shivji
    • 1
  1. 1.National Coral Reef InstituteNova Southeastern University Oceanographic CenterDania BeachUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA
  3. 3.Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA

Personalised recommendations