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Molecular paleobiology of early-branching animals: integrating DNA and fossils elucidates the evolutionary history of hexactinellid sponges

Published online by Cambridge University Press:  08 April 2016

Martin Dohrmann
Affiliation:
Department für Geo- und Umweltwissenschaften, Ludwig-Maximilians-Universität München, Richard-Wagner-Straβe 10, 80333 Munich, Germany
Sergio Vargas
Affiliation:
Department für Geo- und Umweltwissenschaften, Ludwig-Maximilians-Universität München, Richard-Wagner-Straβe 10, 80333 Munich, Germany
Dorte Janussen
Affiliation:
Forschungsinstitut Senckenberg, Sektion Marine Evertebraten I, Senckenberganlage 25, 60325 Frankfurt am Main, Germany
Allen G. Collins
Affiliation:
NMFS, National Systematics Laboratory, National Museum of Natural History, MRC-153, Smithsonian Institution, Post Office Box 37012, Washington, D.C. 20013-7012, U.S.A.
Gert Wörheide*
Affiliation:
Department für Geo- und Umweltwissenschaften and GeoBioCenterLMU, Ludwig-Maximilians-Universität München, and Bayerische Staatsammlung für Paläontologie und Geologie, Richard-Wagner-Straβe 10, 80333 Munich, Germany.
*
*E-mail: [email protected]. Corresponding author

Abstract

Reconciliation of paleontological and molecular phylogenetic evidence holds great promise for a better understanding of the temporal succession of cladogenesis and character evolution, especially for taxa with a fragmentary fossil record and uncertain classification. In zoology, studies of this kind have largely been restricted to Bilateria. Hexactinellids (glass sponges) readily lend themselves to test such an approach for early-branching (non-bilaterian) animals: they have a long and rich fossil record, but for certain taxa paleontological evidence is still scarce or ambiguous. Furthermore, there is a lack of consensus for taxonomic interpretations, and discrepancies exist between neontological and paleontological classification systems. Using conservative fossil calibration constraints and the largest molecular phylogenetic data set assembled for this group, we infer divergence times of crown-group Hexactinellida in a Bayesian relaxed molecular clock framework. With some notable exceptions, our results are largely congruent with interpretations of the hexactinellid fossil record, but also indicate long periods of undocumented evolution for several groups. This study illustrates the potential of an integrated molecular/paleobiological approach to reconstructing the evolution of challenging groups of organisms.

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Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Bengtson, S. 1986. Siliceous microfossils from the Upper Cambrian of Queensland. Alcheringa 10:195216.Google Scholar
Botting, J. P. 2004. An exceptional Caradoc sponge fauna from the Llanfawr Quarries, Central Wales and phylogenetic implications. Journal of Systematic Palaeontology 2:3163.Google Scholar
Brasier, M. D., Green, O., and Shields, G. 1997. Ediacaran sponge spicule clusters from southwestern Mongolia and the origins of the Cambrian fauna. Geology 25:303306.Google Scholar
Brochu, C. A., Sumrall, C. D., and Theodor, J. M. 2004. When clocks (and communities) collide: estimating divergence time from molecules and the fossil record. Journal of Paleontology 78:16.2.0.CO;2>CrossRefGoogle Scholar
Brückner, A. 2006. Taxonomy and paleoecology of lyssacinosan Hexactinellida from the Upper Cretaceous (Coniacian) of Bornholm, Denmark, in comparison with other Postpaleozoic representatives. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 564:1103.Google Scholar
Brückner, A., and Janussen, D. 2005. The first entirely preserved fossil sponge species of the genus Rossella (Hexactinellida) from the Upper Cretaceous of Bornholm, Denmark. Journal of Paleontology 79:2128.Google Scholar
Brunton, F. R., and Dixon, O. A. 1994. Siliceous sponge-microbe biotic associations and their recurrence through the Phanerozoic as reef mound constructors. Palaios 9:370387.Google Scholar
Cárdenas, P., Pérez, T., and Boury-Esnault, N. 2012. Sponge systematics facing new challenges. Advances in Marine Biology 61:79209.Google Scholar
Carrera, M. G., and Botting, J. P. 2008. Evolutionary history of Cambrian spiculate sponges: implications for the Cambrian evolutionary fauna. Palaios 23:124138.Google Scholar
Cartwright, P., and Collins, A. G. 2007. Fossils and phylogenies: integrating multiple lines of evidence to investigate the origin of early major metazoan lineages. Integrative and Comparative Biology 47:744751.Google Scholar
Dohrmann, M., Janussen, D., Reitner, J., Collins, A. G., and Wörheide, G. 2008. Phylogeny and evolution of glass sponges (Porifera, Hexactinellida). Systematic Biology 57:388405.Google Scholar
Dohrmann, M., Collins, A. G., and Wörheide, G. 2009. New insights into the phylogeny of glass sponges (Porifera, Hexactinellida): monophyly of Lyssacinosida and Euplectellinae, and the phylogenetic position of Euretidae. Molecular Phylogenetics and Evolution 52:257262.Google Scholar
Dohrmann, M., Göcke, C., Janussen, D., Reitner, J., Lüter, C., and Wörheide, G. 2011. Systematics and spicule evolution in dictyonal sponges (Hexactinellida: Sceptrulophora) with description of two new species. Zoological Journal of the Linnean Society 163:10031025.Google Scholar
Dohrmann, M., Haen, K. M., Lavrov, D. V., and Wörheide, G. 2012a. Molecular phylogeny of glass sponges (Porifera, Hexactinellida): increased taxon sampling and inclusion of the mitochondrial protein-coding gene, cytochrome oxidase subunit I. Hydrobiologia 687:1120.Google Scholar
Dohrmann, M., Göcke, C., Reed, J., and Janussen, D. 2012b. Integrative taxonomy justifies a new genus, Nodastrella gen. nov., for North Atlantic “Rossella” species (Porifera: Hexactinellida: Rossellidae). Zootaxa 3383:113.Google Scholar
Dong, X., and Knoll, A. H. 1996. Middle and Late Cambrian sponge spicules from Hunan, China. Journal of Paleontology 70:173184.Google Scholar
Donofrio, D. A. 1991. Radiolaria and Porifera (spicula) from the Upper Triassic of Aghdarband (NE-Iran). Abhandlungen der Geologischen Bundes-Anstalt 38:205222.Google Scholar
Donoghue, P. C. J., and Benton, M. J. 2007. Rocks and clocks: calibrating the Tree of Life using fossils and molecules. Trends in Ecology and Evolution 22:424431.Google Scholar
du Dresnay, R., Termier, G., and Termier, H. 1978. Les hexactinellides (lyssakides et dictyonine) du Lias Marocain. Géobios 11:269295.Google Scholar
Erpenbeck, D., and Wörheide, G. 2007. On the molecular phylogeny of sponges (Porifera). Zootaxa 1668:107126.Google Scholar
Erwin, D. H. 2011. Evolutionary uniformitarianism. Developmental Biology 357:2734.Google Scholar
Finks, R. M. 1960. Late Paleozoic sponge faunas of the Texas region. The siliceous sponges. Bulletin of the American Museum of Natural History 120:1160.Google Scholar
Gehling, J. G., and Rigby, J. K. 1996. Long expected sponges from the Neoproterozoic Ediacara fauna of South Australia. Journal of Paleontology 70:185195.Google Scholar
Gradstein, F. M., Ogg, J. G., and Smith, A. G. 2004. A geologic time scale 2004. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Hooper, J. N. A., and van Soest, R. W. M. 2002. Systema Porifera: a guide to the classification of sponges. Plenum, New York.Google Scholar
Huelsenbeck, J. P., and Suchard, M. A. 2007. A nonparametric method for accommodating and testing across-site rate variation. Systematic Biology 56:975987.Google Scholar
Huerta-Cepas, J., Dopazo, J., and Gabaldón, T. 2010. ETE: a python environment for tree exploration. BMC Bioinformatics 11:24.Google Scholar
Kling, S. A., and Reif, W.-E. 1969. The Paleozoic history of amphidisc and hemidisc sponges: new evidence from the Carboniferous of Uruguay. Journal of Paleontology 43:14291434.Google Scholar
Kozur, H. W., Mostler, H., and Repetski, J. E. 1996. “Modern” siliceous sponges from the lowermost Ordovician (early Ibexian–early Tremadocian) Windfall Formation of the Antelope Range, Eureka County, Nevada, U.S.A. Geologisch-Paläontologische Mitteilungen Innsbruck 21:201221.Google Scholar
Krainer, K., and Mostler, H. 1991. Neue Hexactinellide Poriferen aus der südalpinen Mitteltrias der Karawanken (Kärnten, Österreich). Geologisch-Paläontologische Mitteilungen Innsbruck 18:131150.Google Scholar
Krautter, M. 2002. Fossil Hexactinellida: an overview. Pp. 12111223in Hooper and van Soest 2002.Google Scholar
Krautter, M., Conway, K. W., Barrie, J. V., and Neuweiler, M. 2001. Discovery of a “living dinosaur”: globally unique modern hexactinellid sponge reefs off British Columbia, Canada. Facies 44:265282.Google Scholar
Lartillot, N., and Philippe, H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Molecular Biology and Evolution 21:10951109.Google Scholar
Lartillot, N., Lepage, T., and Blanquart, S. 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:22862288.Google Scholar
Leinfelder, R. R., Krautter, M., Laternser, R., Nose, M., Schmid, D. U., Schweigert, G., Werner, W., Keupp, H., Brugger, H., Herrmann, R., Rehfeld-Kiefer, U., Schroeder, J. H., Reinhold, C., Koch, R., Zeiss, A., Schweizer, V., Christmann, H., Menges, G., and Luterbacher, H. 1994. The origin of Jurassic reefs: current research developments and results. Facies 31:156.Google Scholar
Lepage, T., Bryant, D., Philippe, H., and Lartillot, N. 2007. A general comparison of relaxed molecular clock models. Molecular Biology and Evolution 24:26692680.CrossRefGoogle ScholarPubMed
Leys, S. P., Mackie, G. O., and Reiswig, H. M. 2007. The biology of glass sponges. Advances in Marine Biology 52:1145.Google Scholar
Magallón, S. A. 2004. Dating lineages: molecular and paleontological approaches to the temporal framework of clades. International Journal of Plant Sciences 165:S7S21.Google Scholar
Maldonado, M., Carmona, M. C., Uriz, M. J., and Cruzado, A. 1999. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401:785788.Google Scholar
Mehl, D. 1992. Die Entwicklung der Hexactinellida seit dem Mesozoikum. Paläobiologie, Phylogenie und Evolutionsökologie. Berliner Geowissenschaftliche Abhandlungen E 2:1164.Google Scholar
Mehl, D. 1996. Phylogenie und Evolutionsökologie der Hexactinellida (Porifera) im Paläozoikum. Geologisch-Paläontologische Mitteilungen Innsbruck Sonderband 4:155.Google Scholar
Mehl, D., and Fürsich, F. T. 1997. Middle Jurassic Porifera from Kachchh, western India. Paläontologische Zeitschrift 71:1933.Google Scholar
Mehl, D., and Hauschke, N. 1995. Hyalonema cretacea n. sp., first bodily preserved Amphidiscophora (Porifera, Hexactinellida) from the Mesozoic. Geologie und Paläontologie in Westfalen 38:8997.Google Scholar
Mehl, D., and Mostler, H. 1993. Neue Spicula aus dem Karbon und Perm: Konsequenzen für die Evolutionsökologie der Hexactinellida (Porifera), Strategien ihrer Gerüstbildung im Spätpaläozoikum und frühen Mesozoikum. Geologisch-Paläontologische Mitteilungen Innsbruck 19:128.Google Scholar
Mehl-Janussen, D. 1999. Die frühe Evolution der Porifera. Phylogenie und Evolutionsökologie der Poriferen im Paläozoikum mit Schwerpunkt der desmentragenden Demospongiae (“Lithistide”). Münchner Geowissenschaftliche, Abhandlungen A 37:172.Google Scholar
Mostler, H. 1986. Beitrag zur stratigraphischen Verbreitung und phylogenetischen Stellung der Amphidiscophora und Hexasterophora (Hexactinellida, Porifera). Mitteilungen der Österreichischen Geologischen Gesellschaft 78:319359.Google Scholar
Mostler, H. 1989. Mikroskleren hexactinellider Schwämme aus dem Lias der Nördlichen Kalkalpen. Jahrbuch der Geologischen Bundes-Anstalt 132:687700.Google Scholar
Mostler, H. 1990. Hexactinellide Poriferen aus pelagischen Kieselkalken (Unterer Lias, Nördliche Kalkalpen). Geologisch-Paläontologische Mitteilungen Innsbruck 17:143178.Google Scholar
Peterson, K. J., Summons, R. E., and Donoghue, P. C. J. 2007. Molecular palaeobiology. Palaeontology 50:775809.Google Scholar
Peterson, K. J., Cotton, J. A., Gehling, J. G., and Pisani, D. 2008. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philosophical Transactions of the Royal Society of London B 363:14351443.Google Scholar
Pisera, A. 1999. Postpaleozoic history of the siliceous sponges with rigid skeletons. Memoirs of the Queensland Museum 44:463472.Google Scholar
Pisera, A. 2006. Palaeontology of sponges—a review. Canadian Journal of Zoology 84:242261.Google Scholar
Pisera, A., and Bodzioch, A. 1991. Middle Triassic lyssacinosan sponges from Upper Silesia (southern Poland), and the history of hexactinosan and lychniscosan sponges. Acta Geologica Polonica 41:193207.Google Scholar
Reiswig, H. M. 2002a. Order Lychniscosida Schrammen, 1903. P. 1377in Hooper and van Soest 2002.Google Scholar
Reiswig, H. M. 2002b. Family Tretodictyidae Schulze, 1886. Pp. 13411354in Hooper and van Soest 2002.Google Scholar
Reiswig, H. M. 2006. Classification and phylogeny of Hexactinellida (Porifera). Canadian Journal of Zoology 84:195204.Google Scholar
Reiswig, H. M., and Kelly, M. 2011. The marine fauna of New Zealand: hexasterophoran glass sponges of New Zealand (Porifera: Hexactinellida: Hexasterophora): Orders Hexactinosida, Aulocalycoida and Lychniscosida. NIWA Biodiversity Memoirs 124:1176.Google Scholar
Reitner, J., and Mehl, D. 1995. Early Paleozoic diversification of sponges: new data and evidences. Geologisch-Paläontologische Mitteilungen Innsbruck 20:335347.Google Scholar
Rigby, J. K. 1986. Late Devonian sponges of western Australia. Reports of the Geological Survey of West Australia 18:144.Google Scholar
Rigby, J. K., and Gosney, T. C. 1983. First reported Triassic lyssakid sponges from North America. Journal of Paleontology 57:787796.Google Scholar
Rigby, J. K., Racki, G., and Wrzolek, T. 1981. Occurrence of dyctyid hexactinellid sponges in the Upper Devonian of the Holy Cross Mountains. Acta Geologica Polonica 31:163168.Google Scholar
Rigby, J. K., Pisera, A., Wrzolek, T., and Racki, G. 2001. Upper Devonian sponges from the Holy Cross Mountains, central Poland. Palaeontology 44:447488.Google Scholar
Rigby, J. K., Bell, G. L. Jr., and Thompson, K. 2007. Hexactinellid and associated sponges from the Upper Reef Trail Member of the Bell Canyon Formation, Southern Guadalupe Mountains National Park, Texas. Journal of Paleontology 81:12411256.Google Scholar
Salomon, D. 1990. Ein neuer lyssakiner Kieselschwamm, Regadrella leptotoichica (Hexasterophora, Hexactinellida) aus dem Untercenoman von Baddeckenstedt (Nordwestdeutschland). Neues Jahrbuch für Geologie und Paläontologie Monatshefte 1990:342352.Google Scholar
Savill, N. J., Hoyle, D. C., and Higgs, P. G. 2001. RNA sequence evolution with secondary structure constraints: comparison of substitution rate models using maximum-likelihood methods. Genetics 157:399411.Google Scholar
Schrammen, A. 1912. Die Kieselspongien der oberen Kreide von Nordwestdeutschland. II. Teil: Triaxonia (Hexactinellida). Paläontographica Supplement 5:177385.Google Scholar
Smith, A. B., and McGowan, A. J. 2007. The shape of the Phanerozoic marine palaeodiversity curve: how much can be predicted from the sedimentary rock record of Western Europe? Palaeontology 50:765774.Google Scholar
Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:26882690.Google Scholar
Steiner, M., Mehl, D., Reitner, J., and Erdtmann, B.-D. 1993. Oldest entirely preserved sponges and other fossils from the lowermost Cambrian and a new facies reconstruction of the Yangtze platform (China). Berliner Geowissenschaftliche Abhandlungen E 9:293329.Google Scholar
Waggoner, B., and Collins, A. G. 2004. Reductio ad absurdum: testing the evolutionary relationships of Ediacaran and Paleozoic problematic fossils using molecular divergence dates. Journal of Paleontology 78:5161.Google Scholar
Warnock, R. C. M., Yang, Z., and Donoghue, P. C. J. 2012. Exploring uncertainty in the calibration of the molecular clock. Biology Letters 8:156159.Google Scholar
Webby, B. D., and Trotter, J. 1993. Ordovician sponge spicules from New South Wales, Australia. Journal of Paleontology 67:2841.Google Scholar
Welch, J. J., and Bromham, L. 2005. Molecular dating when rates vary. Trends in Ecology and Evolution 20:320327.Google Scholar
Wörheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C., and Lavrov, D. V. 2012. Deep phylogeny and evolution of sponges (Phylum Porifera). Advances in Marine Biology 61:178.Google Scholar
Wu, W., Yang, A.-H., Janussen, D., Steiner, M., and Zhu, M.-Y. 2005. Hexactinellid sponges from the Early Cambrian black shale of South Anhui, China. Journal of Paleontology 79:10431051.Google Scholar
Xiao, S., Hu, J., Yuan, X., Parsley, R. L., and Cao, R. 2005. Articulated sponges from the Lower Cambrian Hetang Formation in southern Anhui, South China: their age and implications for the early evolution of sponges. Palaeogeography, Palaeoclimatology, Palaeoecology 220:89117.Google Scholar
Yang, Z. 2006. Computational molecular evolution. Oxford University Press, Oxford.Google Scholar
Yang, Z., and Rannala, B. 2006. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Molecular Biology and Evolution 23:212226.Google Scholar
Zhang, X.-g., and Pratt, B. R. 1994. New and extraordinary Early Cambrian sponge spicule assemblage from China. Geology 22:4346.Google Scholar
Zhang, X.-g., 2000. A varied Middle Ordovician sponge spicule assemblage from Western Newfoundland. Journal of Paleontology 74:386393.Google Scholar