Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-04-30T15:33:34.468Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological reconstruction of Miaohephyton bifurcatum, a possible brown alga from the Neoproterozoic Doushantuo Formation, South China

Published online by Cambridge University Press:  14 July 2015

Shuhai Xiao ,
Andrew H. Knoll  and
Xunlai Yuan
Shuhai Xiao
Affiliation:
1Botanical Museum, Harvard University, 26 Oxford Street, Cambrige, Massachusetts 02138,
Andrew H. Knoll
Affiliation:
1Botanical Museum, Harvard University, 26 Oxford Street, Cambrige, Massachusetts 02138,
Xunlai Yuan
Affiliation:
2Nanjing Institute of Geology and Palaeontology, Academia Sinica, Nanjing 210008, People's Republic of China
Get access Rights & Permissions [Opens in a new window]

Abstract

On the basis of morphological and taphonomic study of a large sample population, Miaohephyton bifurcatum Steiner, emend. from the terminal Proterozoic Doushantuo Formation (600-550 Ma), South China, is interpreted as algal fragments shed from their parent thalli for reproductive or environmental reasons. Characters such as regularly dichotomous, multicellular thalli with forked tips, apical and intercalary meristematic growth, abscission structures, and possible conceptacles collectively suggest an affinity with the brown algae, in particular the order Fucales. In conjunction with reports of xanthophyte fossils in older Neoproterozoic rocks, this reinterpretation of Miaohephyton bifurcatum indicates that photosynthetic stramenopiles (chrysophytes, synurophytes, xanthophytes, phaeophytes, and diatoms; or chromophytes sensu stricto) diversified during the Neoproterozoic Era along with the red and green algae. This, in turn, suggests that the secondary endosymbiosis that gave rise to the photosynthetic stramenopiles took place relatively soon after the evolutionary transformation of cyanobacteria to rhodophyte plastids.

Type
Research Article
Information
Journal of Paleontology , Volume 72 , Issue 6 , November 1998 , pp. 1072 - 1086
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allison, C. W., and Hilgert, J. W. 1986. Scale microfossils from the Early Cambrian of northwest Canada. Journal of Paleontology, 60:973–1015.CrossRefGoogle Scholar
Awramik, S. M., McMenamin, D. S., Yin, C., Zhao, Z., Ding, Q., and Zhang, S. 1985. Prokaryotic and eukaryotic microfossils from a Proterozoic/Phanerozoic transition in China. Nature, 315:655–658.CrossRefGoogle Scholar
Ayala, F. J., Rzhetsky, A., and Ayala, F. J. 1998. Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates. Proceedings of the National Academy of Sciences, USA, 95:606–611.CrossRefGoogle ScholarPubMed
Bhattacharya, D., and Medlin, L. K. 1995. The phylogeny of plastids: A review based on comparisons of small-subunit ribosomal RNA coding regions. Journal of Phycology, 31:489–498.CrossRefGoogle Scholar
Bhattacharya, D., Medlin, L. K., Wainright, P. O., Ariztia, E. V., Bibeau, C., Stickel, S. K., and Sogin, M. L. 1992. Algae containing chlorophylls a+c are paraphyletic: molecular evolutionary analysis of the Chromophyta. Evolution, 46:1801–1817.CrossRefGoogle ScholarPubMed
Butterfield, N. J., Knoll, A. H., and Swett, K. 1988. Exceptional preservation of fossils in an upper Proterozoic shale. Nature, 334:424–427.CrossRefGoogle Scholar
Butterfield, N. J., Knoll, A. H., and Swett, K. 1990. A bangiophyte red alga from the Proterozoic of Arctic Canada. Science, 250:104–107.CrossRefGoogle ScholarPubMed
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata, 34:1–84.CrossRefGoogle Scholar
Cavalier-Smith, T. 1982. The origins of plastids. Biological Journal of the Linnean Society, 17:289–306.CrossRefGoogle Scholar
Cavalier-Smith, T. 1989. The Kingdom Chromista. p. 381–407. In Green, J. C., Leadbeater, B. S. C. and Diver, W. L., (eds.), The Chromophyte Algae: Problems and Perspectives. Clarendon Press, Oxford.Google Scholar
Cavalier-Smith, T. 1992. The number of symbiotic origins of organelles. BioSystems, 28:91–106.CrossRefGoogle ScholarPubMed
Cavalier-Smith, T., Allsopp, M. T. E. P., and Chao, E. E. 1994. Chimeric conundra: Are nucleomorphs and chromists monophyletic or polyphyletic?. Proceedings, National Academy of Sciences, USA, 91:11368–11372.Google ScholarPubMed
Cavalier-Smith, T., and Chao, E. E. 1996. 18S rRNA sequence of Heterosigma carterae (Raphidophyceae), and the phylogeny of heterokont algae (Ochrophyta). Phycologia, 35:500–510.CrossRefGoogle Scholar
Chen, M., and Xiao, Z. 1991. Discovery of the macrofossils in the Upper Sinian Doushantuo Formation at Miaohe, eastern Yangtze Gorges. Scientia Geologica Sinica, 1991:317–324 [in Chinese with English abstract].Google Scholar
Chen, M., and Xiao, Z. 1992. Macrofossil biota from upper Doushantuo Formation in eastern Yangtze Gorges, China. Acta Palaeontologica Polonica, 31:513–529 [in Chinese with English abstract].Google Scholar
Chen, M., Xiao, Z., and Yuan, X. 1994. A new assemblage of megafossils—Miaohe biota from Upper Sinian Doushantuo Formation, Yangtze Gorges. Acta Palaeontologica Sinica, 33:391–403 [in Chinese with English abstract].Google Scholar
Clayton, M. N. 1984. Evolution of the Phaeophyta with particular reference to the Fucales. p. 11–46. In Round, F. E. and Chapman, D. J., (eds.), Progress in Phycological Research, volume 3. Bristol Biopress, Bristol.Google Scholar
Daugbjerg, N., and Andersen, R. A. 1997. Phylogenetic analysis of the rbcL sequences from haptophytes and heterokont algae suggest their chloroplasts are unrelated. Molecular Biology and Evolution, 14(12):1242–1251.CrossRefGoogle ScholarPubMed
Ding, L., Li, Y., Hu, X., Xiao, Y., Su, C., and Huang, J. 1996. Sinian Miaohe Biota. Geological Publishing House, Beijing, 221 p. [In Chinese with English abstract.]Google Scholar
Ding, L., Zhang, L., Li, Y., and Dong, J. 1992. The Study of the Late Sinian—Early Cambrian Biotas from the Northern Margin of the Yangtze Platform. Scientific and Technical Documents Publishing House, Beijing, 135 p. [In Chinese with English abstract.]Google Scholar
Douglas, S. E. 1992. Eukaryote-eukaryote endosymbioses: insights from studies of a cryptomonad alga. BioSystems, 28:57–68.CrossRefGoogle ScholarPubMed
Douglas, S. E., Murphy, C. A., Spencer, D. F., and Gray, M. W. 1991. Cryptomonad algae are evolutionary chimeras of two phylogenetically distinct unicellular eukaryotes. Nature, 350:148–151.CrossRefGoogle ScholarPubMed
Douglas, S. E., and Turner, S. 1991. Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. Journal of Molecular Evolution, 33:267–273.CrossRefGoogle ScholarPubMed
Druehl, L. D., and Saunders, G. W. 1992. Molecular explorations in kelp evolution, p. 47–83. In Round, F. E. and Chapman, D. J., (eds.), Progress in Phycological Research. Bristol Biopress, Bristol.Google Scholar
Du, R., and Tian, L. 1985. Algal macrofossils from the Qingbaikou System in the Yanshan Range of North China. Precambrian Research, 29:5–14.Google Scholar
Du, R., and Tian, L. 1986. The Macroalgal Fossils of the Qingbaikou Period in the Yanshan Range. Hebei Science and Technology Press, Shijiazhuang, 114 p. [In Chinese with English abstract.]Google Scholar
Fritsch, F. E. 1965 (reprinted). The Structure and Reproduction of the Algae, Vol. 2. Cambridge University Press, Cambridge, 939 p.Google Scholar
Fry, W. L., and Banks, H. P. 1955. Three new genera of algae from the Upper Devonian of New York. Journal of Paleontology, 29:37–44.Google Scholar
Gibbs, S. P. 1981. The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Annals of the New York Academy of Sciences, 361:193–208.CrossRefGoogle ScholarPubMed
Gingerich, P. D. 1983. Rates of evolution: Effects of time and temporal scaling. Science, 222:159–161.CrossRefGoogle ScholarPubMed
Givulescu, R., and Nicorici, E. 1960. Das Sarmat von Fizes (Rumanien) und seine fossile Flora. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 110:180–185.Google Scholar
Gnilovskaya, M. B. 1990. Vendotaenids—Vendian metaphytes. p. 138–147. In Sokolov, B. S. and Iwanowski, A. B., (eds.), The Vendian System. volume 1, Paleontology. Springer-Verlag, Berlin.Google Scholar
Gray, J., and Boucot, A. J. 1979. The Devonian land plant Protosalvinia. Lethaia, 12:57–63.CrossRefGoogle Scholar
Greenwood, A. D. 1974. The Cryptophyta in relation to phylogeny and photosynthesis. Electron Microscopy, 2:566–567.Google Scholar
Grey, K., and Williams, I. R. 1990. Problematic bedding-plane markings from the Middle Proterozoic Manganese Subgroup, Bangemall Basin, Western Australia. Precambrian Research, 46:307–328.CrossRefGoogle Scholar
Hao, S., and Beck, C. B. 1991. Catenalis digitata, gen. et sp. nov., a plant from the Lower Devonian (Siegenian) of Yunnan, China. Canadian Journal of Botany, 69:873–882.Google Scholar
Hermann, T. N. 1990. Organic World Billion Year Ago. Nauka, Leningrad, 49 p.Google Scholar
Hibberd, D. J., and Norris, R. E. 1984. Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta divisio nova, Chlorarachniophyceae classis nova). Journal of Phycology, 20:310–330.CrossRefGoogle Scholar
Hiller, N., and Gess, R. W. 1996. Marine algal remains from the Upper Devonian of South Africa. Review of Palaeobotany and Palynology, 91:143–149.CrossRefGoogle Scholar
Hofmann, H. J. 1985. The mid-Proterozoic Little Dal macrobiota, Mackenzie Mountains, north-west Canada. Palaeontology, 28:331–354.Google Scholar
Hori, H., and Osawa, S. 1987. Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Molecular Biology and Evolution, 4:445–472.Google ScholarPubMed
Kaufman, A. J., Knoll, A. H., and Awramik, S. M. 1992. Biostratigraphic and chemostratigraphic correlation of Neoproterozoic sedimentary successions: Upper Tindir Group, northwestern Canada, as a test case. Geology, 20:181–185.2.3.CO;2>CrossRefGoogle ScholarPubMed
Knoll, A. H. 1992. The early evolution of eukaryotes: a geological perspective. Science, 256:622–627.CrossRefGoogle ScholarPubMed
Kooistra, W. H. C. F., and Medlin, L. K. 1996. Evolution of the diatoms (Bacillariophyta), IV. A reconstruction of their age from small subunit rRNA coding regions and the fossil record. Molecular Phylogenetics and Evolution, 6:391–407.Google ScholarPubMed
Lambert, I. B., Walter, M. R., Zang, W., Lu, S., and Ma, G. 1987. Paleoenvironment and carbon isotope stratigraphy of Upper Proterozoic carbonates of the Yangtze Platform. Nature, 325:140–142.CrossRefGoogle Scholar
Leary, R. L. 1986. Three new genera of fossil non-calcareous algae from Valmeyeran (Mississippian) Strata of Illinois. American Journal of Botany, 73:369–375.CrossRefGoogle Scholar
Lee, J. S. 1924. Geology of the Gorge district of the Yangtze from Ichang to Tzehui, with special reference to the development of the Gorges. Bulletin Geological Society of China, 3:351–391.CrossRefGoogle Scholar
Leipe, D. D., Wainright, P. O., Gunderson, J. H., Porter, D., Patterson, D. J., Valois, F, Himmerich, S., and Sogin, M. L. 1994. The stramenopiles from a molecular perspective: 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis. Phycologia, 33:369–377.CrossRefGoogle Scholar
Lim, B. -L., Kawai, H., Hori, H., and Osawa, S. 1986. Molecular evolution of 5S ribosomal RNA from red and brown algae. Japanese Journal of Genetics, 61:169–176.Google Scholar
Liu, Z., and Du, R. 1991. Morphology and systematics of Longfengshania. Acta Palaeontologica Sinica, 30:106–114 [in Chinese with English abstract].Google Scholar
Loeblich, A. R. J. 1974. Protistan phylogeny as indicated by the fossil record. Taxon, 23:277–290.CrossRefGoogle Scholar
Maier, U.-G. 1992. The four genomes of the alga Pyrenomonas salina (Cryptophyta). BioSystems, 28:69–73.CrossRefGoogle ScholarPubMed
Martin, W., Somerville, C. C., and Loiseaux-de Goer, S. 1992. Molecular phylogenies of plastid origins and algal evolution. Journal of Molecular Evolution, 35:385–404.CrossRefGoogle Scholar
McFadden, G., and Gilson, P. 1995. Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis. Trends in Ecology and Evolution, 10:12–17.CrossRefGoogle ScholarPubMed
McFadden, G., Gilson, P., Hofmann, C. J. B., Adcock, G. J., and Maier, U.-G. 1994. Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proceedings, National Academy of Sciences, USA, 91:3690–3694.Google ScholarPubMed
Medlin, L. K., Kooistra, W. H. C. F., Potter, D., Saunders, G. W., and Andersen, R. A. 1997. Phylogenetic relationships of the “golden algae” (haptophytes, heterokont chromophytes) and their plastids. Plant Systematics and Evolution (Suppl.), 11:187–219.CrossRefGoogle Scholar
Melkonian, M. 1996. Phylogeny of photosynthetic protists and their plastids. Verhandlungen der Deutschen Zoologischen Gesellschaft, 89:71–96.Google Scholar
Morden, C. W., Delwiche, C. F., Kuhsel, M., and Palmer, J. D. 1992. Gene phylogenies and the endosymbiotic origin of plastids. BioSystems, 28:75–90.CrossRefGoogle ScholarPubMed
Niklas, K. J., and Phillips, T. L. 1976. Morphology of Protosalvinia from the Upper Devonian of Ohio and Kentucky. American Journal of Botany, 63:9–29.CrossRefGoogle Scholar
Ochman, H., and Wilson, A. C. 1987. Evolution in bacteria: Evidence for a universal substitution rate in cellular genomes. Journal of Molecular Evolution, 26:74–86.CrossRefGoogle ScholarPubMed
Parker, B. C., and Dawson, E. Y. 1965. Non-calcareous marine algae from California Miocene deposits. Nova Hedwigia, 10:273–295.Google Scholar
Patterson, D. J. 1989. Stramenopiles: chromophytes from a protistan perspective. p. 357–379. In Green, J. C., Leadbeater, B. S. C. and Diver, W. L., (eds.), The Chromophyte Algae: Problems and Perspectives. Clarendon Press, Oxford.Google Scholar
Perasso, R., Baroin, A., Qu, L. H., Bachellerie, J. P., and Adoutte, A. 1989. Origin of the algae. Nature, 339:142–144.CrossRefGoogle ScholarPubMed
Philippe, H., and Adoutte, A. 1996. How far can we trust the molecular phylogeny of protists? Verhandlungen der Deutschen Zoologischen Gesellschaft, Hauptvorträge, 89:49–62.Google Scholar
Philippe, H., Sorhannus, U., Baroin, A., Perasso, R., Gasse, F., and Adoutte, A. 1994. Comparison of molecular and paleontological data in diatom suggests a major gap in the fossil record. Journal of Evolutionary Biology, 7:247–265.CrossRefGoogle Scholar
Phillips, T. L., Niklas, K. J., and Andrews, H. N. 1972. Morphology and vertical distribution of Protosalvinia (Foerstia) from the New Albany Shale (Upper Devonian). Review of Palaeobotany and Palynology, 14:171–196.CrossRefGoogle Scholar
Potter, D., Saunders, G. W., and Andersen, R. A. 1997. Phylogenetic relationship of the raphidophyceae and xanthophyceae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. American Journal of Botany, 84:966–972.CrossRefGoogle ScholarPubMed
Pritchard, H. N., and Bradt, P. T. 1984. Biology of Nonvascular Plants. Times Mirror/Mosby College Publishing, St. Louis, 550p.Google Scholar
Rajanikanth, A. 1989. A fossil marine brown alga from the Gangapur Formation, Pranthita-Godavari Graben. Current Science, 58:78–80.Google Scholar
Raven, P. H. 1970. A multiple origin for plastids and mitochondria. Science, 169:641–646.CrossRefGoogle ScholarPubMed
Rothpletz, A. 1896. Über die Flysch-Fucoiden und einige andere fossile Algen, sowie über liasische, Diatomeen führende Hornschwamme. Zeitschrift der Deutschen Geologischen Gesellschaft, 48:854–914.Google Scholar
Saunders, G. W., and Druehl, L. D. 1992. Nucleotide sequences of the small-subunit ribosomal RNA genes from selected Laminariales (Phaeophyta): Implications for kelp evolution. Journal of Phycology, 28:544–549.CrossRefGoogle Scholar
Schopf, J. M. 1978. Foerstia and recent interpretations of early, vascular land plant. Lethaia, 11:139–143.CrossRefGoogle Scholar
Sogin, M. L. 1994. The origin of eukaryotes and evolution into major kingdoms. p. 181–192. In Bengtson, S., (ed.), Early Life on Earth. Columbia University Press, New York.Google Scholar
Sorhannus, U. 1994. Relative-rate tests versus paleontological divergence data for diatoms and vertebrates. Acta Palaeontologica Polonica, 38:199–214.Google Scholar
Steiner, M. 1994. Die neoproterozoischen Megaalgen Südchinas. Berliner geowissenschaftliche Abhandlungen (E), 15:1–146.Google Scholar
Stiller, J. W., and Hall, B. D. 1997. The origin of red algae: Implications for plastid evolution. Proceedings, National Academy of Sciences, USA, 94:4520–4525.Google ScholarPubMed
Sun, W. 1986. Late Precambrian pennatulids (sea pens) from the eastern Yangtze Gorge, China: Paracharnia Gen. nov. Precambrian Research, 31:361–375.Google Scholar
Taggart, R. E., and Parker, L. R. 1976. A new fossil alga from the Silurian of Michigan. American Journal of Botany, 63:1390–1392.CrossRefGoogle Scholar
Taylor, W. A., and Taylor, T. N. 1987. Spore wall ultrastructure of Protosalvinia. American Journal of Botany, 74:437–443.CrossRefGoogle Scholar
Walter, M. R., Du, R., and Horodyski, R. J. 1990. Coiled carbonaceous megafossils from the middle Proterozoic of Jixian (Tianjin) and Montana. American Journal of Science, 290-A:133–148.Google Scholar
Walter, M. R., Oehler, J. H., and Oehler, D. Z. 1976. Megascopic algae 1300 million years old from the Belt Supergroup, Montana: A reinterpretation of Walcott's Helminthoidichnites. Journal of Paleontology, 50:872–881.Google Scholar
Wang, Z., Yang, J., and Sun, W. 1996. Carbon isotope record of Sinian seawater in Yangtze Platform. Geological Journal of Universities, 2:112–120 [in Chinese with English abstract].Google Scholar
Whatley, J. M., and Whatley, F. R. 1981. Chloroplast evolution. New Phytologists, 87:233–247.CrossRefGoogle Scholar
Xiao, S., Knoll, A.H., Kaufman, A.J., Yin, L., and Zhang, Y. 1997. Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform. Precambrian Research, 84:197–220.Google Scholar
Yin, L. 1985. Microfossils of the Doushantuo Formation in the Yangtze Gorge district, western Hubei. Palaeontologia Cathayana, 2:229–249.Google Scholar
Yin, L. 1987. Microbiotas of latest Precambrian sequences in China. p. 415–494. In Nanjing Institute of Geology and Palaeontology, (ed.), Stratigraphy and Palaeontology of Systemic Boundaries in China: Precambrian-Cambrian Boundary, Vol. 1. Nanjing University Press, Nanjing.Google Scholar
Yin, L., and Li, Z. 1978. Precambrian microfloras of southwest China with reference to their stratigraphic significance. Memoir Nanjing Institute of Geology and Palaeontology, Academia Sinica, 10:41–108 [in Chinese with English abstract].Google Scholar
Yuan, X., Li, J., and Chen, M. 1995. Development and their fossil records of metaphytes from late Precambrian. Acta Palaeontologica Sinica, 34:90–102 [in Chinese with English abstract].Google Scholar
Yuan, X., Wang, Q., and Zhang, Y. 1993. Late Precambrian Weng'an Biota from Guizhou, southwest China. Acta Micropalaeontologica Sinica, 10:409–420 [in Chinese with English abstract].Google Scholar
Zhang, Y. 1989. Multicellular thallophytes with differentiated tissues from Late Proterozoic phosphate rocks of South China. Lethaia, 22:113–132.Google Scholar
Zhang, Y., and Yuan, X. 1992. New data on multicellular thallophytes and fragments of cellular tissues from Late Proterozoic phosphate rocks, South China. Lethaia, 25:1–18.Google Scholar
Zhang, Y., Yin, L., Xiao, S., and Knoll, A.H. 1998. Permineralized fossils from the Terminal Proterozoic Doushantuo Formation, South China. The Paleontological Society, Memoir, in press.CrossRefGoogle Scholar
Zhang, Z. 1981a. A new Oscillatoriaceae-like filamentous microfossil from the Sinian (late Precambrian) of western Hubei Province, China. Geological Magazine, 118:201–206.Google Scholar
Zhang, Z. 1981b. Precambrian microfossils from the Sinian of south China. Nature, 289:792–793.Google Scholar
Zhang, Z. 1984. Microflora of the late Sinian Doushantuo Formation, Hubei Province, China, p. 129–140. In Anonymous, (ed.), Scientific Papers on Geology for International Exchange,—Prepared for the 27th International Geological Congress, 1984, Moscow, volume 1. Geological Publishing House, Beijing. [In Chinese with English abstract.]Google Scholar
Zhang, Z. 1986. New material of filamentous fossil cyanophytes from the Doushantuo Formation (late Sinian) in the eastern Yangtze Gorge. Acta Geologica Sinica, 1986:30–37 [in Chinese with English abstract].Google Scholar
Zhao, Z., Xing, Y., Ding, Q., Liu, G., Zhao, Y., Zhang, S., Meng, X., Yin, C., Ning, B., and Han, R. 1988. The Sinian System of Hubei. China University of Geosciences Press, Wuhan, 205 p. [In Chinese with English abstract.]Google Scholar
Zhao, Z., Xing, Y., Ding, Q., Ma, G., and Chen, Y. 1985. Biostratigraphy of the Yangtze Gorge Area, (1) Sinian. Geological Publishing House, Beijing, 143 p. [In Chinese with English abstract.]Google Scholar
Zhu, W., and Chen, M. 1984. On the discovery of macrofossil algae from the late Sinian in the eastern Yangtze Gorges, south China. Acta Botanica Sinica, 26:558–560 [in Chinese with English abstract].Google Scholar