Hidden functional complexity in the flora of an early land ecosystem

Summary The first land ecosystems were composed of organisms considered simple in nature, yet the morphological diversity of their flora was extraordinary. The biological significance of this diversity remains a mystery largely due to the absence of feasible study approaches. To study the functional biology of Early Devonian flora, we have reconstructed extinct plants from fossilised remains in silico. We explored the morphological diversity of sporangia in relation to their mechanical properties using finite element method. Our approach highlights the impact of sporangia morphology on spore dispersal and adaptation. We discovered previously unidentified innovations among early land plants, discussing how different species might have opted for different spore dispersal strategies. We present examples of convergent evolution for turgor pressure resistance, achieved by homogenisation of stress in spherical sporangia and by torquing force in Tortilicaulis‐like specimens. In addition, we show a potential mechanism for stress‐assisted sporangium rupture. Our study reveals the deceptive complexity of this seemingly simple group of organisms. We leveraged the quantitative nature of our approach and constructed a fitness landscape to understand the different ecological niches present in the Early Devonian Welsh Borderland flora. By connecting morphology to functional biology, these findings facilitate a deeper understanding of the diversity of early land plants and their place within their ecosystem.

[1]  Stuart A. Casson,et al.  The origin and evolution of stomata , 2022, Current Biology.

[2]  Richard S. Smith,et al.  How Cell Geometry and Cellular Patterning Influence Tissue Stiffness , 2022, International journal of molecular sciences.

[3]  Allison K. Shaw,et al.  Understanding the drivers of dispersal evolution in range expansions and their ecological consequences , 2022, Evolutionary Ecology.

[4]  D. Edwards,et al.  Piecing together the eophytes - a new group of ancient plants containing cryptospores. , 2021, The New phytologist.

[5]  D. Edwards,et al.  Earliest record of transfer cells in Lower Devonian plants. , 2021, The New phytologist.

[6]  J. Duckett,et al.  Picking up the pieces: New charcoalified plant mesofossils (eophytes) from a Lower Devonian Lagerstӓtte in the Welsh Borderland, UK , 2021, Review of Palaeobotany and Palynology.

[7]  R. Gess,et al.  An early Devonian flora from the Baviaanskloof Formation (Table Mountain Group) of South Africa , 2021, Scientific Reports.

[8]  Sulin Zhang,et al.  Molecular insights into the complex mechanics of plant epidermal cell walls , 2021, Science.

[9]  J. Marshall,et al.  The Devonian landscape factory: plant–sediment interactions in the Old Red Sandstone of Svalbard and the rise of vegetation as a biogeomorphic agent , 2021, Journal of the Geological Society.

[10]  S. McDaniel Bryophytes are not early diverging land plants. , 2021, The New phytologist.

[11]  A. Hetherington,et al.  Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata , 2020, Current Biology.

[12]  L. Dolan,et al.  Rhynie chert fossils demonstrate the independent origin and gradual evolution of lycophyte roots. , 2019, Current opinion in plant biology.

[13]  C. Cox,et al.  Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp.). , 2018, The New phytologist.

[14]  A. Boudaoud,et al.  Cellular Heterogeneity in Pressure and Growth Emerges from Tissue Topology and Geometry , 2018, Current Biology.

[15]  J. Kvaček,et al.  Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous , 2018, Nature Plants.

[16]  Mark N. Puttick,et al.  The Interrelationships of Land Plants and the Nature of the Ancestral Embryophyte , 2018, Current Biology.

[17]  W. McMahon,et al.  Evolution of alluvial mudrock forced by early land plants , 2018, Science.

[18]  P. Prusinkiewicz,et al.  Why plants make puzzle cells, and how their shape emerges , 2018, eLife.

[19]  H. Kerp Organs and tissues of Rhynie chert plants , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  L. Dolan,et al.  History and contemporary significance of the Rhynie cherts—our earliest preserved terrestrial ecosystem , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  Christopher P. Reed,et al.  Oxygenation history of the Neoproterozoic to early Phanerozoic and the rise of land plants , 2017 .

[22]  S. Strauss,et al.  On the micro-indentation of plant cells in a tissue context , 2017, Physical Biology.

[23]  T. Lenton,et al.  Earliest land plants created modern levels of atmospheric oxygen , 2016, Proceedings of the National Academy of Sciences.

[24]  Yiannis Ventikos,et al.  Morphomechanical Innovation Drives Explosive Seed Dispersal , 2016, Cell.

[25]  Daniel Kierzkowski,et al.  A Mechanical Feedback Restricts Sepal Growth and Shape in Arabidopsis , 2016, Current Biology.

[26]  Arezki Boudaoud,et al.  Mechanically, the Shoot Apical Meristem of Arabidopsis Behaves like a Shell Inflated by a Pressure of About 1 MPa , 2015, Front. Plant Sci..

[27]  J. Marshall,et al.  Investigating Devonian trees as geo‐engineers of past climates: linking palaeosols to palaeobotany and experimental geobiology , 2015 .

[28]  S. Burns The Theory of Materials Failure, by Richard M. Christensen , 2015 .

[29]  Anne-Lise Routier-Kierzkowska,et al.  Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments , 2015, Journal of experimental botany.

[30]  Corina E. Tarnita,et al.  Fitness tradeoffs between spores and nonaggregating cells can explain the coexistence of diverse genotypes in cellular slime molds , 2015, Proceedings of the National Academy of Sciences.

[31]  G. Bassel,et al.  Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo , 2014, Proceedings of the National Academy of Sciences.

[32]  D. Edwards,et al.  Cryptospores and cryptophytes reveal hidden diversity in early land floras. , 2014, The New phytologist.

[33]  S. Wyatt,et al.  Early evolution of the vascular plant body plan - the missing mechanisms. , 2014, Current opinion in plant biology.

[34]  D. Shah Developing plant fibre composites for structural applications by optimising composite parameters: a critical review , 2013, Journal of Materials Science.

[35]  D. Edwards,et al.  New dyad-producing plants from the Lower Devonian (Lochkovian) of the Welsh Borderland , 2012 .

[36]  J Dumais,et al.  The Fern Sporangium: A Unique Catapult , 2012, Science.

[37]  D. Edwards,et al.  A new group of Early Devonian plants with valvate sporangia containing sculptured permanent dyads , 2012 .

[38]  Charles H. Wellman,et al.  A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  M. Gibling,et al.  Palaeozoic landscapes shaped by plant evolution , 2012 .

[40]  Woodward W. Fischer,et al.  Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants , 2011, Geobiology.

[41]  Marcus Roper,et al.  Dispersal of fungal spores on a cooperatively generated wind , 2010, Proceedings of the National Academy of Sciences.

[42]  D. Whitaker,et al.  Sphagnum Moss Disperses Spores with Vortex Rings , 2010, Science.

[43]  Bernt-Erik Sæther,et al.  An evolutionary maximum principle for density-dependent population dynamics in a fluctuating environment , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  A. Knoll,et al.  Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant , 2008, Paleobiology.

[45]  D. J. Davis,et al.  The Fastest Flights in Nature: High-Speed Spore Discharge Mechanisms among Fungi , 2008, PloS one.

[46]  J. Schneller,et al.  Speed and force of spore ejection in Selaginella martensii , 2008, Botanica Helvetica.

[47]  C. Boyce How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage , 2008, Paleobiology.

[48]  Tony Farquhar,et al.  Fracture mechanics and its relevance to botanical structures. , 2006, American journal of botany.

[49]  T. Taylor,et al.  Life history biology of early land plants: deciphering the gametophyte phase. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. Edwards,et al.  Charcoal in the Silurian as evidence for the earliest wildfire , 2004 .

[51]  T. Taylor,et al.  Fungi from the Rhynie chert: a view from the dark side , 2003, Transactions of the Royal Society of Edinburgh: Earth Sciences.

[52]  D. Edwards,et al.  New perspectives on Cooksonia from the Lower Devonian of the Welsh Borderland , 2002 .

[53]  J. Basinger,et al.  Morphologically complex plant macrofossils from the Late Silurian of Arctic Canada. , 2002, American journal of botany.

[54]  D. Beerling,et al.  Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era , 2001, Nature.

[55]  P. Gensel,et al.  6. The Posongchong Floral Assemblages of Southeastern Yunnan, China—Diversity and Disparity in Early Devonian Plant Assemblages , 2001 .

[56]  D. Edwards,et al.  Ultrastructure of laevigate hilate spores in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland , 1998 .

[57]  T. Speck,et al.  EARLY EVOLUTION OF LAND PLANTS: Phylogeny, Physiology, and Ecology of the Primary Terrestrial Radiation , 1998 .

[58]  Thomas J. Algeo,et al.  Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events , 1998 .

[59]  D. Edwards New insights into early land ecosystems: a glimpse of a lilliputian world , 1996 .

[60]  D. Edwards,et al.  Lower Devonian coalified sporangia from Shropshire: Salopella Edwards & Richardson and Tortilicaulis Edwards , 1994 .

[61]  D. Edwards,et al.  A diverse assemblage of early land plants from the Lower Devonian of the Welsh Borderland , 1992 .

[62]  Peter J. Rousseeuw,et al.  Finding Groups in Data: An Introduction to Cluster Analysis , 1990 .

[63]  David Edwards,et al.  Aglaophyton major, a non-vascular land-plant from the Devonian Rhynie Chert , 1986 .

[64]  M. A. Cichan Conductance in the wood of selected Carboniferous plants , 1986, Paleobiology.

[65]  K. Niklas The aerodynamics of wind pollination , 1985, The Botanical Review.

[66]  K. Niklas THE INFLUENCE OF PALEOZOIC OVULE AND CUPULE MORPHOLOGIES ON WIND POLLINATION , 1983, Evolution; international journal of organic evolution.

[67]  W. Remy Lower Devonian Gametophytes: Relation to the Phylogeny of Land Plants , 1982, Science.

[68]  S. P. Lloyd,et al.  Least squares quantization in PCM , 1982, IEEE Trans. Inf. Theory.

[69]  J. Feehan,et al.  Records of Cooksonia-type sporangia from late Wenlock strata in Ireland , 1980, Nature.

[70]  P. H. Gregory,et al.  Microbiology of the Atmosphere , 1962, Nature.

[71]  Robert R. Sokal,et al.  A statistical method for evaluating systematic relationships , 1958 .

[72]  Eric H. Metzler,et al.  Plant Biomechanics : An Engineering Approach to Plant Form and Function , 2017 .

[73]  C. Wellman,et al.  Embryophytes on land: the Ordovician to Lochkovian (Lower Devonian) record , 2001 .

[74]  Cheng-Sen Li,et al.  A new genus of early land plants with novel strobilar construction from the Lower Devonian Posongchong Formation, Yunnan Province, China , 1992 .

[75]  J. B. Richardson,et al.  Silurian and Devonian spore zones of the Old Red Sandstone Continent and adjacent regions , 1986 .

[76]  J. Shaw,et al.  Considerations on the evolution of the moss operculum , 1984 .

[77]  W. H. Lang,et al.  XXXII.—On Old Red Sandstone Plants showing Structure, from the Rhynie Chert Bed, Aberdeenshire. Part IV. Restorations of the Vascular Cryptogams, and Discussion of their bearing on the General Morphology of the Pteridophyta and the Origin of the Organisation of Land-Plants , 1921, Transactions of the Royal Society of Edinburgh.