Testing Species Assignments in Extant Terebratulide Brachiopods: A Three-dimensional Geometric Morphometric Analysis of Long-Looped Brachidia


Autoři: Natalia López Carranza aff001;  Sandra J. Carlson aff001
Působiště autorů: Department of Earth and Planetary Sciences, University of California, Davis, CA, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225528

Souhrn

Species of terebratulide brachiopods have been largely characterized qualitatively on the basis of morphology. Furthermore, species-level morphological variability has rarely been analyzed within a quantitative framework. The objective of our research is to quantify morphological variation to test the validity of extant named species of terebratulide brachiopods, focusing on the lophophore-supporting structures—the “long loops.” Long loops are the most distinctive and complex morphological feature in terebratellidine brachiopods and are considered to be phylogenetically and taxonomically informative. We studied eight species with problematic species identities in three genera distributed in the North Pacific: Laqueus, Terebratalia, and Dallinella. Given how geometrically complex long loops are, we generated 3D models from computed tomography (CT) scans of specimens of these eight species and analyzed them using 3D geometric morphometrics. Our goal was to determine ranges of variation and to test whether species are clearly distinguishable from one another in morphospace and statistically. Previous studies have suggested that some species might be overly split and are indistinguishable. Our results show that these extant species of terebratellidines can be reliably distinguished on the basis of quantitative loop morphometrics. Using 3D geometric morphometric methods, we demonstrate the utility of CT beyond purely descriptive imaging purposes in testing the morphometric validity of named species. It is crucial to treat species described and named from qualitative morphology as working hypotheses to be tested; many macroevolutionary studies depend upon the accurate assessment of species in order to identify and seek to explain macroevolutionary patterns. Our results provide quantitative documentation of the distinction of these species and thus engender greater confidence in their use to characterize macroevolutionary patterns among extant terebratellidine brachiopods. These methods, however, require further testing in extinct terebratellidines, which only rarely preserve the delicate long loop in three dimensions. In addition, molecular analyses of extant terebratellidines will test the species delimitations supported by the morphometric analyses presented in this study. [Species determination; morphological variability; 3D geometric morphometrics; terebratulide brachiopods; long loops.]

Klíčová slova:

Computed axial tomography – Fossils – Morphometry – Phylogenetics – principal component analysis – Taxonomy – Brachiopods – Fossil record


Zdroje

1. MacKinnon DI, Lee DE. Loop Morphology and Terminology in Terebratulida. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 5: Rhynchonelliformea (part). Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 2006.

2. Laumer CE, Fernández R, Lemer S, Combosch D, Kocot KM, Riesgo A, et al. Revisiting metazoan phylogeny with genomic sampling of all phyla. Proceedings of the Royal Society B. 2019 Jul 10;286(1906):20190831. doi: 10.1098/rspb.2019.0831 31288696

3. Logan A. Geographic Distribution of Extant Articulated Brachiopods. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 6: Supplement. Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 2007.

4. Emig CC, Bitner MA, Alvarez F. Brachiopoda database [Internet]. 2018. Available from: http://paleopolis.es/brachiopoda_database on 04-04-2019.

5. Carlson SJ. The evolution of Brachiopoda. Annual Review of Earth and Planetary Sciences. 2016;44:409–38.

6. Rowell AJ. The monophyletic origin of the Brachiopoda. Lethaia. 1982;15(4):299–307.

7. Carlson SJ, Fitzgerald PC. Sampling taxa, estimating phylogeny and inferring macroevolution: an example from Devonian terebratulide brachiopods. Earth and Environmental Science Transactions of the Royal Society of Edinburgh. 2007;98(3–4):311–25.

8. Sperling EA, Pisani D, Peterson KJ. Molecular paleobiological insights into the origin of the Brachiopoda. Evolution & development. 2011;13(3):290–303.

9. Lee DE, MacKinnon DI, Smirnova TN, Baker PG, Yu-Gan J, Dong-Li S. Terebratulida. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 5: Rhynchonelliformea (part). Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 2006.

10. Rudwick MJ. Living and fossil brachiopods. London: Hutchinson Univ. Libr.; 1970.

11. Emig CC. Le lophophore—structure significative des Lophophorates (Brachiopodes, Bryozoaires, Phoronidiens). Zoologica Scripta. 1976 Dec;5(1‐4):133–7.

12. Reed CG, Cloney RA. Brachiopod tentacles: ultrastructure and functional significance of the connective tissue and myoepithelial cells in Terebratalia. Cell and tissue research. 1977 Nov 1;185(1):17–42. doi: 10.1007/bf00226666 563291

13. Gilmour TH. Food-collecting and waste-rejecting mechanisms in Glottidia pyramidata and the persistence of lingulacean inarticulate brachiopods in the fossil record. Canadian Journal of Zoology. 1981 Aug 1;59(8):1539–47.

14. Williams A, James MA, Emig CC, Mackay S, Rhodes MC. Anatomy. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 1: introduction. Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 1997.

15. Temereva EN, Kuzmina TV. The first data on the innervation of the lophophore in the rhynchonelliform brachiopod Hemithiris psittacea: what is the ground pattern of the lophophore in lophophorates? BMC Evolutionary Biology. 2017 Dec;17(1):172. doi: 10.1186/s12862-017-1029-5 28760135

16. Lee DE, MacKinnon DI. Introduction. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 5: Rhynchonelliformea (part). Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 2006.

17. Buckman SS. Homoeomorphy among Jurassic Brachiopoda. Proceedings of the Cotteswold Naturalists’ Field Club. 1901;13(4):231–90.

18. Cloud PE. Homeomorphy, and a remarkable illustration. American Journal of Science. 1941;239(12):899–904.

19. Stehli FG. Paleozoic Terebratulida. In: Moore RC, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 1965.

20. Cooper GA. Homeomorphy in Recent deep-sea brachiopods. Smithsonian Contributions to Paleobiology. 1972; 11:1–25.

21. Cooper GA. Terebratulacea (Brachiopoda), Triassic to Recent: A Study of the Brachidia (Loops). Smithsonian Contributions to Paleobiology. 1983;50:1–445.

22. Waagen WH. Salt Range Fossils. I. Productus- Limestone Fossils. Geological Survey of India, Memoirs, Palaeontologia Indica (series 13). 1883;4(2):391–546.

23. Muir-Wood HM. A history of the classification of the phylum Brachiopoda. London: British Museum; 1955.

24. Stehli FG. Evolution of the loop and lophophore in terebratuloid brachiopods. Evolution. 1956; 10(2):187–200.

25. MacKinnon DI, Lee DE, Baker PG, Smirnova TN, Dagys AS, Dong-li S. Terebratellidina. In: Kaesler RL, editor. Treatise on Invertebrate Paleontology. Part H. Brachiopoda Revised, Vol. 5: Rhynchonelliformea (part). Part H, Brachiopoda. New York & Lawrence: Geological Society of America & University of Kansas Press; 2006.

26. Rudwick MJ. Filter-feeding mechanisms in some brachiopods from New Zealand. Zoological Journal of the Linnean Society. 1962;44(300):592–615.

27. Dall WH. A revision of the Terebratulidae and Lingulidae, with remarks on and descriptions of some recent forms. American Journal of Conchology. 1870;6(2):88–168.

28. Dall WH. Annotated list of the Recent Brachiopoda in the collection of the United States National Museum, with descriptions of thirty-three new forms. United States National Museum, Proceedings. 1920;57(2314):261–377.

29. MacKinnon D, Long S. Terebratula californiana Kuster, 1844, and reappraisal of west coast north American brachiopod species referred to the genus Laqueus Dall, 1870. Bulletin-Natural History Museum Geology Series. 2000;56(2):85–90.

30. Davidson T. A Monograph of recent Brachiopoda, Part 2. Linnean Society of London, Transactions series 2, Zoology. 1887;4(2):74–182.

31. Pennington JT, Tamburri MN, Barry JP. Development, temperature tolerance, and settlement preference of embryos and larvae of the articulate brachiopod Laqueus californianus. The Biological Bulletin. 1999;196(3):245–56. doi: 10.2307/1542949 28296489

32. Oldroyd IS. The marine shells of the West Coast of North America: Stanford University Press; 1924.

33. Tunnicliffe V, Wilson K. Brachiopod populations: distribution in fjords of British Columbia (Canada) and tolerance of low. Marine Ecology-Progress Series. 1988;47:117–28.

34. Hatai KM. On some Cenozoic Brachiopoda from the North American region. American Midland Naturalist. 1938;19(3):706–22.

35. Hertlein LG, Grant US. The Cenozoic Brachiopoda of western North America: University of California Press; 1944.

36. Sowerby GB. Descriptions of thirteen new species of brachiopods. Proceedings of the Zoological Society of London; 1846;14:91–95.

37. Hatai KM. A list of the Brachiopoda dredged by the Hukui-maru from Wakasa Bay, Hukui Prefecture, Japan. The Venus. 1936;6(3):146–54.

38. Zezina O. Check-list of Holocene brachiopods annotated with geographical ranges of species. Paleontological Journal. 2010;44(9):1176–99.

39. Dunker WBRH. Index molluscorum maris Japonici: T. Fischer, editor; 1882.

40. Yabe H, Hatai K. The Recent brachiopod fauna of Japan. Proceedings of the Imperial Academy. 1934;10(10):661–4.

41. Saito M, Kojima S, Endo K. Mitochondrial COI sequences of brachiopods: genetic code shared with protostomes and limits of utility for phylogenetic reconstruction. Molecular Phylogenetics and Evolution. 2000 Jun 1;15(3):331–44. doi: 10.1006/mpev.2000.0773 10860643

42. Saito M, Endo K. Molecular phylogeny and morphological evolution of laqueoid brachiopods. Paleontological Research. 2001 Jun 29;5(2):87–100.

43. World Register of Marine Species (WoRMS). Laqueus Dall, 1870 [Internet]. Available at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=235265

44. Beecher CE. Revision of the families of loop-bearing Brachiopoda. The development of Terebratalia obsoleta Dall. Connecticut Academy of Arts and Sciences, Transactions. 1893;9(2):376–99, 3 pl.

45. Du Bois HM. Variation induced in brachiopods by environmental conditions. Publications of the Puget Sound Marine Station. 1916;1:177–183.

46. Paine RT. Growth and size distribution of the brachiopod Terebratalia transversa Sowerby. Pacific Science. 1969;XXIII:337–343.

47. Schumann D. Hydrodynamic influences in brachiopod shell morphology of Terebratalia transversa (Sowerby) from the San Juan Islands, USA. Brachiopods through Time Proceedings of the 2nd International Brachiopod Congress; 1991.

48. Krause RA Jr. An assessment of morphological fidelity in the sub-fossil record of a terebratulide brachiopod. Palaios. 2004;19(5):460–76.

49. Hochberg FG. Brachiopoda. In: Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel. Santa Barbara Museum of Natural History. 1997;14:1–74.

50. Light SF. The Light and Smith manual: Intertidal Invertebrates from Central California to Oregon: University of California Press; 2007.

51. Hatai KM. The Cenozoic Brachiopoda of Japan. Science reports of the Tohoku Imperial University 2nd series, Geology. 1940;20:1–A24.

52. Dall WH. A new genus of brachiopods. American Naturalist. 1871; 5:1–55.

53. Thomson JA. Brachiopod morphology: types of folding in the Terebratulacea. Geological Magazine. 1915;2(608):71–6.

54. Adams A, Reeve L. Mollusca. Part 1. In: Adams A, editors. The Zoology of the Voyage of the H.M.S. Samarang. Reeve and Benham; 1850. p. 1–87.

55. Slice DE. Geometric morphometrics. Annual Review of Anthropology. 2007;36:261–81.

56. Zelditch ML, Swiderski DL, Sheets HD. Geometric morphometrics for biologists: a primer: Academic Press; 2012.

57. Bookstein FL. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge, United Kingdom: Cambridge University Press; 1991.

58. Haney RA, Mitchell CE, Kim K. Geometric morphometric analysis of patterns of shape change in the Ordovician brachiopod Sowerbyella. Palaios. 2001;16(2):115–25.

59. Tort A, Laurin B. Intra-and interspecific variation in internal structures of the genus Stenosarina (Brachiopoda, Terebratulida) using landmarks. Journal of Paleontology. 2001;75(2):261–73.

60. Ruggiero ET, Raia P, Buono G. Geometric morphometrics species discrimination within the genus Terebratula from the Late Cenozoic of Italy. Fossil and Strata. 2008;54:209–17.

61. Bose R, Schneider CL, Leighton LR, Polly PD. Influence of atrypid morphological shape on Devonian episkeletobiont assemblages from the lower Genshaw formation of the Traverse Group of Michigan: a geometric morphometric approach. Palaeogeography, Palaeoclimatology, Palaeoecology. 2011;310(3–4):427–41.

62. Bose R. A new morphometric model in distinguishing two closely related extinct brachiopod species. Historical Biology. 2012;24(6):655–64.

63. Topper TP, Strotz LC, Skovsted CB, Holmer LE. Do brachiopods show substrate‐related phenotypic variation? A case study from the Burgess Shale. Palaeontology. 2017;60(2):269–79.

64. Lee S, Jung J, Shi G. A three‐dimensional geometric morphometric study of the development of sulcus versus shell outline in Permian neospiriferine brachiopods. Lethaia. 2018;51(1):1–14.

65. Motchurova-Dekova N, Harper DA. Synchrotron radiation X-ray tomographic microscopy (SRXTM) of brachiopod shell interiors for taxonomy: preliminary report. Geoloski anali Balkanskoga poluostrva. 2010;(71):109–17.

66. Pakhnevich A. Study of fossil and recent brachiopods, using a skyscan 1172 X-ray microtomograph. Paleontological Journal. 2010;44(9):1217–30.

67. Błażejowski B, Binkowski M, Bitner MA, Gieszcz P. X-ray microtomography (XMT) of fossil brachiopod shell interiors for taxonomy. Acta Palaeontologica Polonica. 2011;56(2):439–41.

68. Gaspard D. X-ray computed tomography: A promising tool to investigate the brachiopod shell interior. Effects on 3D modelling and taxonomy. Comptes Rendus Palevol. 2013;12(3):149–58.

69. Seidel R, Lüter C. Overcoming the fragility–X-ray computed micro-tomography elucidates brachiopod endoskeletons. Frontiers in Zoology. 2014;11(1):65. doi: 10.1186/s12983-014-0065-x 25642279

70. Schreiber HA, Roopnarine PD, Carlson SJ. Three-dimensional morphological variability of Recent rhynchonellide brachiopod crura. Paleobiology. 2014;40(4):640–58.

71. Lee S, Shi GR, Park T-YS, Oh JR, Mii HS, Lee M. Virtual palaeontology: the effects of mineral composition and texture of fossil shell and hosting rock on the quality of X-ray microtomography (XMT) outcomes using Palaeozoic brachiopods. Palaeontologia Electronica. 2017;20(2):1–25.

72. Pakhnevich A, Kurkin A, Lavrov A, Tarasenko K, Kovalenko E, Kaloyan A, et al. Synchrotron and neutron tomography of paleontological objects on the facilities of the Kurchatov Institute. Journal of Imaging. 2018;4(8):103.

73. Hendricks JR, Saupe EE, Myers CE, Hermsen EJ, Allmon WD. The generification of the fossil record. Paleobiology. 2014;40(4):511–28.

74. Watanabe A. How many landmarks are enough to characterize shape and size variation? PloS one. 2018;13(6):e0198341. doi: 10.1371/journal.pone.0198341 29864151

75. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2015.

76. Adams DC, Otárola‐Castillo E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution. 2013;4(4):393–9.

77. Schlager S. Morpho and Rvcg–Shape Analysis in R: R-Packages for geometric morphometrics, shape analysis and surface manipulations. In. Zheng G, Li S, Székely G, editors. Statistical shape and deformation analysis. Academic Press; 2017;p. 217–56.

78. Klingenberg CP, Monteiro LR. Distances and directions in multidimensional shape spaces: implications for morphometric applications. Systematic Biology. 2005;54(4):678–88. doi: 10.1080/10635150590947258 16126663

79. Muir-Wood HM. On the internal structure of some Mesozoic Brachiopoda. Philosophical Transactions of the Royal Society of London Series B, Containing Papers of a Biological Character. 1934;223(494–508):511–67.

80. Bitner MA, Motchurova-Dekova N. Brachiopods from the Sanadinovo Formation (lower Cenomanian) in northern Bulgaria. Cretaceous Research. 2005;26(4):525–39.

81. Raduloviç V, Raduloviç B, Rabrenoviç D. Upper Barremian representatives of Dzirulina Nutsubidze, 1945 (Terebratellidina, Brachiopoda) from eastern Serbia. Geologica Carpathica. 2006;57(4):269.

82. Smirnova T. Ontophylogenetic studies of the brachiopods of the Order Terebratulida. Paleontological Journal. 2008;42(8):805.

83. Cunningham JA, Rahman IA, Lautenschlager S, Rayfield EJ, Donoghue PC. A virtual world of paleontology. Trends in ecology & evolution. 2014;29(6):347–57.


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