Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T06:24:58.991Z Has data issue: false hasContentIssue false

Experimental signal dissection and method sensitivity analyses reaffirm the potential of fossils and morphology in the resolution of the relationship of angiosperms and Gnetales

Published online by Cambridge University Press:  30 July 2018

Mario Coiro
Affiliation:
Department of Systematic and Evolutionary Botany, University of Zurich, 8008 Zurich, Switzerland. E-mail: mario.coiro@systbot.uzh.ch
Guillaume Chomicki
Affiliation:
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom; and Queen’s College, University of Oxford, High Street, Oxford OX1 4AW, United Kingdom. E-mail: guillaume.chomicki@gmail.com
James A. Doyle
Affiliation:
Department of Evolution and Ecology, University of California, Davis, Davis, California 95616, USA. E-mail: jadoyle@ucdavis.edu

Abstract

The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmatic problems in plant evolution, with morphological analyses (which have usually included fossils) and molecular analyses pointing to very distinct topologies. Almost all morphology-based phylogenies group angiosperms with Gnetales and certain extinct seed plant lineages, while most molecular phylogenies link Gnetales with conifers. In this study, we investigate the phylogenetic signal present in published seed plant morphological data sets. We use parsimony, Bayesian inference, and maximum-likelihood approaches, combined with a number of experiments with the data, to address the morphological–molecular conflict. First, we ask whether the lack of association of Gnetales with conifers in morphological analyses is due to an absence of signal or to the presence of competing signals, and second, we compare the performance of parsimony and model-based approaches with morphological data sets. Our results imply that the grouping of Gnetales and angiosperms is largely the result of long-branch attraction (LBA), consistent across a range of methodological approaches. Thus, there is a signal for the grouping of Gnetales with conifers in morphological matrices, but it was swamped by convergence between angiosperms and Gnetales, both situated on long branches. However, this effect becomes weaker in more recent analyses, as a result of addition and critical reassessment of characters. Even when a clade including angiosperms and Gnetales is still weakly supported by parsimony, model-based approaches favor a clade of Gnetales and conifers, presumably because they are more resistant to LBA. Inclusion of fossil taxa weakens rather than strengthens support for a relationship of angiosperms and Gnetales. Our analyses finally reconcile morphology with molecules in favoring a relationship of Gnetales to conifers, and show that morphology may therefore be useful in reconstructing other aspects of the phylogenetic history of the seed plants.

Type
Articles
Copyright
© 2018 The Paleontological Society. All rights reserved. 

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

Literature Cited

Albert, V. A., Backlund, A., Bremer, K., Chase, M. W., Manhart, J. R., Mishler, B. D., and Nixon, K. C.. 1994. Functional constraints and rbcL evidence for land plant phylogeny. Annals of the Missouri Botanical Garden 81:534567.Google Scholar
Axsmith, B. J., Taylor, E. L., Taylor, T. N., and Cuneo, N. R.. 2000. New perspectives on the Mesozoic seed fern order Corystospermales based on attached organs from the Triassic of Antarctica. American Journal of Botany 87:757768.Google Scholar
Bateman, R. M., Hilton, J., and Rudall, P. J.. 2006. Morphological and molecular phylogenetic context of the angiosperms: contrasting the “top-down” and “bottom-up” approaches used to infer the likely characteristics of the first flowers. Journal of Experimental Botany 57:34713503.Google Scholar
Bauch, J., Liese, W., and Schultze, R.. 1972. The morphological variability of the bordered pit membranes in gymnosperms. Wood Science and Technology 6:165184.Google Scholar
Bergsten, J. 2005. A review of long-branch attraction. Cladistics 21:163193.Google Scholar
Bomfleur, B., Decombeix, A.-L., Schwendemann, A. B., Escapa, I. H., Taylor, E. L., Taylor, T. N., and McLoughlin, S.. 2014. Habit and ecology of the Petriellales, an unusual group of seed plants from the Triassic of Gondwana. International Journal of Plant Sciences 175:10621075.Google Scholar
Bomfleur, B., Grimm, G. W., and McLoughlin, S.. 2017. The fossil Osmundales (Royal Ferns)—a phylogenetic network analysis, revised taxonomy, and evolutionary classification of anatomically preserved trunks and rhizomes. PeerJ 5:e3433.Google Scholar
Bowe, L. M., Coat, C., and dePamphilis, C. W.. 2000. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proceedings of the National Academy of Sciences USA 97:40924097.Google Scholar
Brinkmann, H., van der Giezen, M., Zhou, Y., de Raucourt, G. P., and Philippe, H.. 2005. An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Systematic Biology 54:743757.Google Scholar
Brown, J. W., Parins-Fukuchi, C., Stull, G. W., Vargas, O. M., and Smith, S. A.. 2017. Bayesian and likelihood phylogenetic reconstructions of morphological traits are not discordant when taking uncertainty into consideration: a comment on Puttick et al. Proceedings of the Royal Society of London B 284:20170986.Google Scholar
Bryant, D., and Moulton, V.. 2004. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21:255265.Google Scholar
Burleigh, J. G., and Mathews, S.. 2007. Assessing systematic error in the inference of seed plant phylogeny. International Journal of Plant Sciences 168:125135.Google Scholar
Cantino, P. D., Doyle, J. A., Graham, S. W., Judd, W. S., Olmstead, R. G., Soltis, D. E., Soltis, P. S., and Donoghue, M. J.. 2007. Towards a phylogenetic nomenclature of Tracheophyta . Taxon 56:822846.Google Scholar
Carlquist, S. 1996. Wood, bark, and stem anatomy of Gnetales: a summary. International Journal of Plant Sciences 157(6, Suppl.) S58S76.Google Scholar
Cau, A., Brougham, T., and Naish, D.. 2015. The phylogenetic affinities of the bizarre Late Cretaceous Romanian theropod Balaur bondoc (Dinosauria, Maniraptora): dromaeosaurid or flightless bird? PeerJ 3:e1032.Google Scholar
Chaw, S.-M., Parkinson, C. L., Cheng, Y., Vincent, T. M, and Palmer, J. D.. 2000. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proceedings of the National Academy of Sciences USA 97:40864091.Google Scholar
Coiro, M., and Pott, C.. 2017. Eobowenia gen. nov. from the Early Cretaceous of Patagonia: indication for an early divergence of Bowenia? BMC Evolutionary Biology 17:97.Google Scholar
Cox, C. J., Li, B., Foster, P. G., Embley, T. M., and Civáň, P.. 2014. Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions. Systematic Biology 63:272279.Google Scholar
Crane, P. R. 1985a. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72:716793.Google Scholar
Crane, P. R. 1985b. Phylogenetic relationships in seed plants. Cladistics 1:329348.Google Scholar
Crepet, W. L., and Stevenson, D. W.. 2010. The Bennettitales (Cycadeoidales): a preliminary perspective on this arguably enigmatic group. Pp 215244 in C. T. Gee, ed. Plants in Mesozoic time: morphological innovations, phylogeny, ecosystems. Indiana University Press, Bloomington.Google Scholar
Dembo, M., Radovčić, D., Garvin, H. M., Laird, M. F., Schroeder, L., Scott, J. E., Brophy, J., Ackermann, R. R., Musiba, C. M., de Ruiter, D. J., and Mooers, A. Ø. 2016. The evolutionary relationships and age of Homo naledi: an assessment using dated Bayesian phylogenetic methods. Journal of Human Evolution 97:1726.Google Scholar
Denk, T., and Grimm, G. W.. 2009. The biogeographic history of beech trees. Review of Palaeobotany and Palynology 158:83100.Google Scholar
Donoghue, M. J., and Doyle, J. A.. 2000. Seed plant phylogeny: demise of the anthophyte hypothesis? Current Biology 10:R106R109.Google Scholar
Donoghue, M. J., Doyle, J. A., Gauthier, J., Kluge, A. G., and Rowe, T.. 1989. The importance of fossils in phylogeny reconstruction. Annual Review of Ecology and Systematics 20:431460.Google Scholar
Doyle, J. A. 1996. Seed plant phylogeny and the relationships of the Gnetales. International Journal of Plant Sciences 157(6, Suppl.) S3S39.Google Scholar
Doyle, J. A. 2006. Seed ferns and the origin of the angiosperms. Journal of the Torrey Botanical Society 133:169209.Google Scholar
Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169:816843.Google Scholar
Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40:301326.Google Scholar
Doyle, J. A. 2013. Phylogenetic analyses and morphological innovations in land plants. In B. A. Ambrose, and M. Purugganan, eds. The evolution of plant form. Annual Plant Reviews 45:150. Wiley-Blackwell, Oxford.Google Scholar
Doyle, J. A., and Donoghue, M. J.. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review 52:321431.Google Scholar
Doyle, J. A., and Donoghue, M. J.. 1987. The importance of fossils in elucidating seed plant phylogeny and macroevolution. Review of Palaeobotany and Palynology 50:6395.Google Scholar
Doyle, J. A., and Donoghue, M. J.. 1992. Fossils and seed plant phylogeny revisited. Brittonia 44:89106.Google Scholar
Doyle, J. A., and Endress, P. K.. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. International Journal of Plant Sciences 161(6, Suppl.) S121S153.Google Scholar
Doyle, J. A., and Endress, P. K.. 2014. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: ANITA lines and relatives of Chloranthaceae. International Journal of Plant Sciences 175:555600.Google Scholar
Endress, P. K., and Doyle, J. A.. 2009. Reconstructing the ancestral angiosperm flower and its initial specializations. American Journal of Botany 96:2266.Google Scholar
Felsenstein., J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27:401410.Google Scholar
Foley, N. M., Springer, M. S., and Teeling, E. C.. 2016. Mammal madness: is the mammal tree of life not yet resolved? Philosophical Transactions of the Royal Society of London B 371:20150140.Google Scholar
Friis, E. M., Doyle, J. A., Endress, P. K., and Leng, Q.. 2003. Archaefructus—angiosperm precursor or specialized early angiosperm? Trends in Plant Science 8:369373.Google Scholar
Friis, E. M., Crane, P. R., Pedersen, K. R., Bengtson, S., Donoghue, P. J. C., Grimm, G. W., and Stampanoni, M.. 2007. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450:549552.Google Scholar
Friis, E. M., Pedersen, K. R., and Crane, P. R.. 2009. Early Cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales-Erdtmanithecales-Gnetales group. American Journal of Botany 96:252283.Google Scholar
Gauthier, J., Kluge, A. G., and Rowe, T.. 1988. Amniote phylogeny and the importance of fossils. Cladistics 4:105209.Google Scholar
Gauthier, J., Kearney, M., Maisano, J. A., Rieppel, O., and Behlke, A. D. B.. 2012. Assembling the squamate tree of life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History 53:3308.Google Scholar
Givnish, T. J., and Sytsma, K. J. eds. 1997. Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge.Google Scholar
Godefroit, P., Cau, A., Hu, D.-Y., Escuillié, F., Wu, W., and Dyke, G.. 2013. A Jurassic avialan dinosaur from China resolves the early phylogenetic history of birds. Nature 498:359362.Google Scholar
Grimm, G. 2017. Should we try to infer trees on tree-unlikely matrices? The Genealogical World of Phylogenetic Networks. http://phylonetworks.blogspot.com/2017/07/should-we-try-to-infer-trees-on.html, accessed 5 July 2017.Google Scholar
Gugerli, F., Sperisen, C., Büchler, U., Brunner, I., Brodbeck, S., Palmer, J. D., and Qiu, Y.-L.. 2001. The evolutionary split of Pinaceae from other conifers: evidence from an intron loss and a multigene phylogeny. Molecular Phylogenetics and Evolution 21:167175.Google Scholar
Hamby, R.K., and Zimmer, E. A.. 1992. Ribosomal RNA as a phylogenetic tool in plant systematics. Pp. 5091 in P. S. Soltis, D. E. Soltis, and J. J. Doyle, eds. Molecular systematics of plants. Chapman and Hall, New York.Google Scholar
Harris, T. M. 1954. Mesozoic seed cuticles. Svensk Botanisk Tidskrift 48:281291.Google Scholar
Hill, C.R., and Crane, P. R.. 1982. Evolutionary cladistics and the origin of angiosperms. In K. A. Joysey, and A. E. Friday, eds. Problems of phylogenetic reconstruction. Systematics Association Special Volume 21:269361. Academic Press, London.Google Scholar
Hilton, J., and Bateman, R. M.. 2006. Pteridosperms are the backbone of seed plant phylogeny. Journal of the Torrey Botanical Society 133:119168.Google Scholar
Holland, B., Huber, K. T., Moulton, V., and Lockhart, P. J.. 2004. Using consensus networks to visualize contradictory evidence for species phylogeny. Molecular Biology and Evolution 21:14591461.Google Scholar
Huson, D.H., and Bryant, D.. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23:254267.Google Scholar
Jenner, R. A. 2004. Accepting partnership by submission? Morphological phylogenetics in a molecular millennium. Systematic Biology 53:333359.Google Scholar
Kass, R. E., and Raftery, A. E.. 1995. Bayes factors. Journal of the American Statistical Association 90:773795.Google Scholar
Kelley, D. R., and Gasser, C. S.. 2009. Ovule development: genetic trends and evolutionary considerations. Sexual Plant Reproduction 22:229234.Google Scholar
Klavins, S. D., Taylor, T. N., and Taylor, E. L.. 2002. Anatomy of Umkomasia (Corystospermales) from the Triassic of Antarctica. American Journal of Botany 89:664676.Google Scholar
Lee, M. S., and Palci, A.. 2015. Morphological phylogenetics in the genomic age. Current Biology 25:R922R929.Google Scholar
Lee, M. S., and Worthy, T. H.. 2012. Likelihood reinstates Archaeopteryx as a primitive bird. Biology Letters 8:299303.Google Scholar
Lee, M.S., Cau, A., Naish, D., and Dyke, G.J.. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562566.Google Scholar
Legg, D. A., Sutton, M. D., and Edgecombe, G. D.. 2013. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nature Communications 4:2485.Google Scholar
Lewis, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50:913925.Google Scholar
Lloyd, G. T. 2016. Estimating morphological diversity and tempo with discrete character‐taxon matrices: implementation, challenges, progress, and future directions. Biological Journal of the Linnean Society 118:131151.Google Scholar
Lockhart, P. J., and Cameron, S. A.. 2001. Trees for bees. Trends in Ecology and Evolution 16:8488.Google Scholar
Maddison, D. R., and Maddison, W. P.. 2003. MacClade 4: analysis of phylogeny and character evolution, version 4.06. Sinauer, Sunderland, Mass.Google Scholar
Magallón, S. 2010. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology 59:384399.Google Scholar
Magallón, S., and Sanderson, M. J.. 2002. Relationships among seed plants inferred from highly conserved genes: sorting conflicting phylogenetic signals among ancient lineages. American Journal of Botany 89:19912006.Google Scholar
Magallón, S., Hilu, K. W., and Quandt, D.. 2013. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany 100:556573.Google Scholar
Martens, P. 1971. Les Gnétophytes. Encyclopedia of plant anatomy 12(2). Borntraeger, Stuttgart.Google Scholar
Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany 96:228236.Google Scholar
Mathews, S., and Kramer, E.. 2012. The evolution of reproductive structures in seed plants: a re-examination based on insights from developmental genetics. New Phytologist 194:910923.Google Scholar
Mathews, S., Clements, M. D., and Beilstein, M. A.. 2010. A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Philosophical Transactions of the Royal Society of London B 365:383395.Google Scholar
Müller, K. F. 2005. The efficiency of different search strategies for estimating parsimony, jackknife, bootstrap, and Bremer support. BMC Evolutionary Biology 5:58.Google Scholar
Mundry, M., and Stützel, T.. 2004. Morphogenesis of the reproductive shoots of Welwitschia mirabilis and Ephedra distachya (Gnetales), and its evolutionary implications. Organisms Diversity and Evolution 4:91108.Google Scholar
Nickrent, D. L., Parkinson, C. L., Palmer, J. D., and Duff, R. J.. 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17:18851895.Google Scholar
Nixon, K. C., Crepet, W. L., Stevenson, D. W., and Friis, E. M.. 1994. A reevaluation of seed plant phylogeny. Annals of the Missouri Botanical Garden 81:484533.Google Scholar
O’Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B. P., Luo, Z.-X., Meng, J., Ni, X., Novacek, M. J., Perini, F. A., Randall, Z. S., Rougier, G. W., Sargis, E. J., Silcox, M. T., Simmons, N. B., Spaulding, M., Velazco, P. M., Weksler, M., Wible, J. R., and Cirranello, A. L.. 2013. The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339:662667.Google Scholar
O’Reilly, J. E., Puttick, M. N., Parry, L., Tanner, A. R., Tarver, J. E., Fleming, J., Pisani, D., and Donoghue, P. C. J.. 2016. Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data. Biology Letters 12:20160081.Google Scholar
Parenti, L. R. 1980. A phylogenetic analysis of the land plants. Biological Journal of the Linnean Society 13:225242.Google Scholar
Patterson, C. 1981. Significance of fossils in determining evolutionary relationships. Annual Review of Ecology and Systematics 12:195223.Google Scholar
Pott, C. 2016. Westersheimia pramelreuthensis from the Carnian (Upper Triassic) of Lunz, Austria: more evidence for a unitegmic seed coat in early Bennettitales. International Journal of Plant Sciences 177:771791.Google Scholar
Puttick, M. N., O’Reilly, J. E., Oakley, D., Tanner, A. R., Fleming, J. F., Clark, J., Holloway, L., Lozano-Fernandez, J., Parry, L. A., Tarver, J. E., Pisani, D., and Donoghue, P. C. J.. 2017a. Parsimony and maximum-likelihood phylogenetic analyses of morphology do not generally integrate uncertainty in inferring evolutionary history: a response to Brown et al. Proceedings of the Royal Society of London B 284:20171636.Google Scholar
Puttick, M. N., O’Reilly, J. E., Tanner, A. R., Fleming, J. F., Clark, J., Holloway, L., Lozano-Fernandez, J., Parry, L. A., Tarver, J. E., Pisani, D., and Donoghue, P. C. J.. 2017b. Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data. Proceedings of the Royal Society of London B 284:20162290.Google Scholar
Pyron, R. A. 2011. Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology 60:466481.Google Scholar
Pyron, R. A. 2015. Post-molecular systematics and the future of phylogenetics. Trends in Ecology and Evolution 30:384389.Google Scholar
Qiu, Y.-L., Li, L., Wang, B., Chen, Z., Dombrovska, O., Lee, J., Kent, L., Li, L., Jobson, R. W., Hendry, T. A., Taylor, D. W., Testa, C. M., and Ambros, M.. 2007. A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. International Journal of Plant Sciences 168:691708.Google Scholar
Rambaut, A., and Drummond, A. J.. 2007. Tracer: MCMC trace analysis tool, Version 1.4.1. http://tree.bio.ed.ac.uk/software.Google Scholar
R Core Team 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.Google Scholar
Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D. L., and Rasnitsyn, A. P.. 2012. A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Systematic Biology 61:973999.Google Scholar
Rota-Stabelli, O., Kayal, E., Gleeson, D., Daub, J., Boore, J. L., Telford, M. J., Pisani, D., Blaxter, M., and Lavrov, D. V.. 2010. Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biology and Evolution 2:425440.Google Scholar
Rothwell, G. W., and Serbet, R.. 1994. Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Systematic Botany 19:443482.Google Scholar
Rothwell, G. W., and Stockey, R. A.. 2013. Evolution and phylogeny of Gnetophytes: evidence from the anatomically preserved seed cone Protoephedrites eamesii gen. et sp. nov. and the seeds of several bennettitalean species. International Journal of Plant Sciences 174:511529.Google Scholar
Rothwell, G. W., and Stockey, R. A.. 2016. Phylogenetic diversification of Early Cretaceous seed plants: the compound seed cone of Doylea tetrahedrasperma . American Journal of Botany 103:923937.Google Scholar
Rothwell, G. W., Crepet, W. L., and Stockey, R. A.. 2009. Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales. American Journal of Botany 96:296322.Google Scholar
Rudall, P. J., and Bateman, R. M.. 2010. Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Philosophical Transactions of the Royal Society of London B 365:397409.Google Scholar
Rydin, C., and Källersjö, M.. 2002. Taxon sampling and seed plant phylogeny. Cladistics 18:484513.Google Scholar
Rydin, C., Källersjö, M., and Friis, E. M.. 2002. Seed plant relationships and the systematic position of Gnetales based on nuclear and chloroplast DNA: conflicting data, rooting problems, and the monophyly of conifers. International Journal of Plant Sciences 163:197214.Google Scholar
Sanderson, M. J., Wojciechowski, M. F., Hu, J.-M., Sher Khan, T., and Brady, S. G.. 2000. Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants. Molecular Biology and Evolution 17:782797.Google Scholar
Scotland, R. W., Olmstead, R. G., and Bennett, J. R.. 2003. Phylogeny reconstruction: the role of morphology. Systematic Biology 52:539548.Google Scholar
Singh, H. 1978. Embryology of gymnosperms (Handbuch der Pflanzenanatomie 10(2) Borntraeger, Berlin.Google Scholar
Springer, M. S., Burk-Herrick, A., Meredith, R., Eizirik, E., Teeling, E., O’Brien, S. J., and Murphy, W. J.. 2007. The adequacy of morphology for reconstructing the early history of placental mammals. Systematic Biology 56:673684.Google Scholar
Springer, M. S., Meredith, R. W., Teeling, E. C., and Murphy, W. J.. 2013. Technical comment on “The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 341:613.Google Scholar
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:13121313.Google Scholar
Stefanovic, S., Jager, M., Deutsch, J., Broutin, J., and Masselot, M.. 1998. Phylogenetic relationships of conifers inferred from partial 28S rRNA gene sequences. American Journal of Botany 85:688697.Google Scholar
Stockey, R. A., and Rothwell, G. W.. 2003. Anatomically preserved Williamsonia (Williamsoniaceae): evidence for bennettitalean reproduction in the Late Cretaceous of western North America. International Journal of Plant Sciences 164:251262.Google Scholar
Stockey, R. A., and Rothwell, G. W.. 2009. Distinguishing angiophytes from the earliest angiosperms: a Lower Cretaceous (Valanginian-Hauterivian) fruit-like reproductive structure. American Journal of Botany 96:323335.Google Scholar
Sun, G., Ji, Q., Dilcher, D. L., Zheng, S., Nixon, K. C., and Wang, X.. 2002. Archaefructaceae, a new basal angiosperm family. Science 296:899904.Google Scholar
Swofford, D. L. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods), Version 4. Sinauer, Sunderland, Mass.Google Scholar
Swofford, D. L., Waddell, P. J., Huelsenbeck, J. P., Foster, P. G., Lewis, P. O., and Rogers, J. S.. 2001. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Systematic Biology 50:525539.Google Scholar
Taylor, E. L., and Taylor, T. N.. 1992. Reproductive biology of the Permian Glossopteridales and their suggested relationship to flowering plants. Proceedings of the National Academy of Sciences USA 89:1149511497.Google Scholar
Taylor, T. N., Del Fueyo, G. M., and Taylor, E. L.. 1994. Permineralized seed fern cupules from the Triassic of Antarctica: implications for cupule and carpel evolution. American Journal of Botany 81:666677.Google Scholar
Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221244.Google Scholar
Wickett, N. J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N., Ayyampalayam, S., Barker, M. S., Burleigh, J. G., Gitzendanner, M. A., Ruhfel, B. R., Wafula, E., Der, J. P., Graham, S. W., Mathews, S., Melkonian, M., Soltis, D. E., Soltis, P. S., Miles, N. W., Rothfels, C. J., Pokorny, L., Shaw, A. J., DeGironimo, L., Stevenson, D. W., Surek, B., Villarreal, J. C., Roure, B., Philippe, H., dePamphilis, C. W., Chen, T., Deyholos, M. K., Baucom, R. S., Kutchan, T. M., Augustin, M. M., Wang, J., Zhang, Y., Tian, Z., Yan, Z., Wu, X., Sun, X., Wong, G. K. S., and Leebens-Mack., J. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences USA 111:E4859E4868.Google Scholar
Wieland, G. R. 1916. American fossil cycads, Vol. 2. Taxonomy. Carnegie Institution of Washington, Washington, D.C.Google Scholar
Wiens, J. J. 2005. Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Systematic Biology 54:731742.Google Scholar
Wiens, J. J., and Hollingsworth, B. D.. 2000. War of the iguanas: conflicting phylogenies, long-branch attraction, and disparate rates of molecular and morphological evolution in iguanid lizards. Systematic Biology 49:6985.Google Scholar
Wiens, J. J., and Tiu, J.. 2012. Highly incomplete taxa can rescue phylogenetic analyses from the negative impacts of limited taxon sampling. PLoS ONE 7:e42925.Google Scholar
Wiens, J. J., Chippindale, P. T., and Hillis, D. M.. 2003. When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. Systematic Biology 52:501514.Google Scholar
Wright, A. M., and Hills, D. M.. 2014. Bayesian analysis using a simple likelihood model outperforms parsimony for estimation of phylogeny from discrete morphological data. PLoS ONE 9:e109210.Google Scholar
Wright, A. M., Lloyd, G. T., and Hillis, D. M.. 2015. Modeling character change heterogeneity in phylogenetic analyses of morphology through the use of priors. Systematic Biology 65:602611.Google Scholar
Xie, W., Lewis, P. O., Fan, Y., Kuo, L., and Chen, M.-H.. 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology 60:150160.Google Scholar
Zander, R. H. 2004. Minimal values of reliability of bootstrap and jackknife proportions, decay index, and Bayesian posterior probability. PhyloInformatics 2:113.Google Scholar
Zhang, C., Stadler, T., Klopfstein, S., Heath, T. A., and Ronquist, F.. 2016. Total-evidence dating under the fossilized birth-death process. Systematic Biology 65:228249.Google Scholar
Zhong, B., Deusch, O., Goremkin, V. V., Penny, D., Briggs, P. J., Atherton, R. A., Nikiforova, S. V., and Lockhart, P. J.. 2011. Systematic error in seed plant phylogenomics. Genome Biology and Evolution 3:13401348.Google Scholar
Zou, Z., and Zhang, J.. 2016. Morphological and molecular convergences in mammalian phylogenetics. Nature Communications 7:12758.Google Scholar
Supplementary material: File

Coiro et al. supplementary material

Coiro et al. supplementary material 1

Download Coiro et al. supplementary material(File)
File 13.7 KB