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Major Events in the Evolution of Plants


Abstract

This page provides a high level review of some of the main threads of the evolution of embryophytes (“plants”), from their first appearance in the fossil record to the present day.

Keywords: evolution, plants

Introduction

Before going any further we should define what we mean by “plants”. The most familiar plants are the land plants; these are by far the most commonly treated in paleobotany textbooks, and they will be here, too. However, there are several groups of organisms frequently thought of as plants simply because they are green and photosynthesise – some dinoflagellates, for example. But, from their phylogenetic position, these organisms are no more “plants” than an elephant is. That is to say, an elephant is more closely related to an oak tree, for example, than the dinoflagellate is to either. (I’ll also take this opportunity to overturn a common fallacy concerning acritarchs. By definition, acritarchs are single celled organisms of unknown affinity. If something is a plant it cannot be an acritarch, and vice versa.) Discussion of acritarchs and other “algae” is often included in general paleobotanical texts (such as the excellent Taylor et al. 2008) but it is important to understand that this is an association of convenience; not a real one.

In this essay, the “plants” we will be considering are the green plants, or Viridiplantae, which “comprise an estimated 450,000–500,000 species, encompass a high level of diversity and evolutionary timescales, and have important roles in all terrestrial and most aquatic ecosystems. This ecological diversity derives from developmental, morphological and physiological innovations that enabled the colonization and exploitation of novel and emergent habitats (Leebens-Mack et al. 2019).

However, we should at least make some passing mention of the early diverging Chlorophyta and Streptophyta lineages.

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“[Land] plants – with three phyla of bryophytes (mosses, liverworts, and hornworts) and the seven living, or extant, phyla of vascular plants – constitute a kingdom of photosynthetic organisms adapted for life on land…. All plants are multicellular and are composed of eukaryotic cells that contain vacuoles and are surrounded by cell walls that contain cellulose. Their principle mode of nutrition is photosynthesis, although a few plants have become heterotrophic. … Reproduction in plants is primarily sexual, with cycles of alternating haploid and diploid generations. … The unifying character of the Plantae is the presence of an embryo during the sporophytic [diploid] phase of the lifecycle” (Raven et al. 2005, p. 233, 235). “They exhibit key innovations, including protected reproductive organs (archegonia and antheridia) and the development of the zygote within an archegonium into an embryo that receives maternal nutrition” (Leebens-Mack et al. 2019).

“Tracing early plant evolution is often focused on individual taxa, their taxonomy, appearances and stratigraphic ranges” Kraft et al. 2019, p. 144).

Origin

The most basal embryophytes (land plants) are bryophytes: hornworts, liverworts and mosses. However, resolving the relationships between these groups, and of bryophytes as a whole “to the remaining land plants has long been problematic, but is critical for understanding the evolution of fundamental innovations within land plants, including the tolerance to desiccation, shifts in the dominance of multicellular haploid and diploid generations, and parental retention of a multicellular embryo” (Leebens-Mack et al. 2019, p. 681). This study recovered extant bryophytes as monophyletic, “with hornworts sister to a moss and liverwort clade. All analyses rejected the hypothesis that liverworts are sister to all other extant land plant lineages. The largest number of gene-family expansions in our analyses was associated with the origin of land plants and the evolution of bryophytes” (Leebens-Mack et al. 2019, p. 681).

“Although the oldest macrofossil evidence of land plants is of middle Silurian (Wenlock) age, palynology indicates that they probably first appeared in late Ordovician times” (Cleal & Thomas 2009, p. 203).

“The search for the oldest land plant (embryophyte) reflects an effort to prove a substantial step of terrestrialization. It is of importance for molecular biologists and (neo)botanists to calibrate the molecular clock and establish a starting point for phylogenetic studies of early vascular plants (e.g. Clarke et al. 2011; Kenrick et al. 2012; Gerrienne et al. 2016). The first appearance of such plants, based on macroscopic evidence, can be provisionally considered to have occurred in the Late Ordovician in Poland (Salamon et al. 2018). However, the earliest unequivocal record based on Cooksonia (the oldest accepted macrofossil land plant; Fig. 1, left) from almost coeval sites in Ireland (Edwards et al. 1983) and Bohemia (Libertin et al. 2003, 2018a), points to the appearance of land plants in the Wenlock (middle Silurian). On the other hand, fossil spores and isolated sporangia indicate a much older appearance of embryophytes, probably as early as in the Middle Ordovician (Clarke et al. 2011; Gerrienne et al. 2016; Vavrdova 1984), even if a coeval macrofossil record is missing” (Kraft et al. 2019, p. 144).

Ordovician

Colonisation of the land by plants occurred in stages. The first, a bryophytic phase, lasting from the Ordovician to the Early Devonian, is evidenced by fossil spores and cuticles.

Silurian

“Throughout Silurian times, only small rhyniophytes (or rhyniophytoids) and lycophytes are known…. Remarkably, even in these early phases of their evolution, plants had an almost worldwide distribution with records from North and South America, Europe, Africa, central Asia, China and Australia, presumably reflecting the wide dispersal potential of their spores and the lack of any competition. The global composition of these floras also appears to be fairly uniform, although this may in part be due to the problems of differentiating biological species within the plexus of these morphologically very simple plants” (Cleal & Thomas 2009, p. 203).

The first major diversification of land plant life, such as rhyniophytes, zosterophylls, drepanophycaleans, lycophytes, trimerophytes, and (in the southern hemisphere) Baragwanathia (Fig. 1, right), began as early as Late Ludlow (Late Silurian) in Australia through Gedinnian (Early Devonian) on Laurentia. Plants of this “rhyniophytoid phase” were small vascular plants having an axial organisation and terminal sporangia such as Cooksonia.

Cooksonia, the early or even primordial land plant, apparently played a key role: it has been described from a number of regions, ranges widely from the Silurian to the early Devonian, and is represented by several species such as C. pertoni, C. paranensis, C. banksii, and doubtfully C. cambrensis, C. hemisphaerica (Gonez and Gerrienne 2010a) with many other specimens having been described in open nomenclature. Cooksonia also occupies a special position in the colonization of terrestrial habitats, which is a major aspect of early plant research based on broad studies of associations, their successions and distributions (e.g. Edwards & Wellman 2001; Kenrick et al. 2012). This complex paleoecological approach has attracted considerable attention over the past two decades” Kraft et al. 2019, p. 144).

Kraft et al. 2019 envisage an “Initial Plant Diversification and Dispersal Event” to be one of the key steps in global terrestrialization. This first significant diversification and dispersal episode of vascular plants, which occurred in the Prídolí (latest Silurian) in several paleoregions representing wide paleolatitude and paleoclimatic ranges, such as Avalonia, Laurentia, Baltica, Gondwana, South and North China and Kazakhstania (e.g., Edwards & Wellman 2001, Wellman et al. 2013, and other references in Kraft et al. 2019).

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Fig. 1: Cooksonia cf. hemisphaerica, left, and Baragwanathia brevifolia (Kraft et al. 2019, fig. 4).

Devonian

“From its primitive rhyniophyte and lycophyte precursors, land vegetation rapidly diversified during Devonian times. By the end of the period, all of the major divisions of vascular plants except the flowering plants had appeared, with the first record of ferns (or at least their pre-fern ancestors) being in Middle Devonian times, and of sphenophytes and gymnosperms in Late Devonian times…” (Cleal & Thomas 2009, p. 203).

“The Devonian was pivotal in the evolutionary history of land plants: a diverse range of plant architectures evolved and plants radiated into a remarkable array of ecological niches (Gensel & Andrews 1984, Gerrienne et al. 2004, Stein et al. 2012)” (Xu et al. 2017, p. 524).

“The Devonian Period also saw the development of several structures that made the vascular plants better adapted to life on land…. Secondary wood is the most widely adopted means by which plants can significantly increase their stature and it is first seen in the fossil record in the Middle Devonian Series. The resulting trees (and therefore presumably forests) must have had a dramatic impact on the Devonian landscape. Photosynthetic efficiency was also enhanced by the development of planated leaves in Devonian times” (Cleal & Thomas 2009, p. 203).

Numerous plant taxa have been reported from Devonian deposits around the world and phytogeographical provincialism began to develop in the global flora (see Raymond et al. 2006). However, plants with simple form and diminutive size, i.e., with axis widths less than 2 mm, from the Early–Middle Devonian, have been paid little attention (see Cai & Wang 1995, Wang & Berry 2003, Wang et al. 2004, 2007). Those basal euphyllophytes have quite distinct morphological characters in their branching patterns and sporangial attachment, and played key roles in the evolution of early land plants (Stewart & Rothwell 1993, Kenrick & Crane 1997)” (Xu et al. 2017, p. 524; Fig. 2).

The lycopsids apparently arose in the Silurian (Kotyk et al. 2002) but their fossil record is better known from the Devonian onwards.

The sphenophytes appear to have arisen in the Devonian.

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Fig. 2: The Early Devonian plant, Pauthecophyton; composite from Xu et al. 2019, fig. 3A and D.

Carboniferous

“In Pennsylvanian [= Late Carboniferous] times, there was a dramatic change in vegetation. In low paleolatitudes, the very first tropical rain forests appeared: the so-called ‘Coal Forests’ of europe, North America and China (known as the Amerosinian Palaeokingdom...), so named because of the vast reserves of coal-forming peat that were laid down by them…. These forests were dominated by the giant lycophytes…, which were perfectly adapted to the wetland habitats that existed over much of the then tropics” (Cleal & Thomas 2009, p. 205-206).

Triassic

Although the Triassic flora “included various holdovers from the Paleozoic, in addition, there were many new families as well as one new order, the Bennettitales. In fact, … the Triassic vegetation can be considered a mixture of ancient and modern. Indeed, some Triassic species are considered to be members of living genera, whereas others bear no resemblance whatsoever to modern-day taxa. There was a clear distinction during the Triassic between the land floras of the northern and southern hemispheres. Certain ferns grew in both hemispheres, but in general, there were relatively few taxa common to both the north and the south. … Although angiosperms … did not exist during the early Mesozoic, there were many other Triassic and Jurassic foliage taxa that would likely have formed dense ground cover. Herbaceous seed ferns and extensive stands of horsetails and ferns were probably common. There is certainly every reason to think that open, verdant hillsides, wooded and forested slopes, and hot and steamy forests and swamps were very much part of the Triassic landscape” (Fraser & Henderson (2006), p. 53, 54-55).

Lycopods were widely distributed, but these were herbaceous taxa similar to the modern day Lycopodium rather than the large, tree-like forms (Lepidodendron etc.) of earlier periods. Equisetales (horsetails) were also smaller than their Paleozoic ancestors, although many were still respectable trees. Having declined through the Permian, Filicales (true ferns) underwent a resurgence in diversity during the Triassic, including the appearance of some modern families such as the Osmundaceae, represented by the commonly found fossil, Cladophlebis. Cycads were more widespread than today, achieving a global distribution. Another very commonly found fossil, Taenopteris, belongs to this group. Bennettitales and Gingkoales were important floral taxa. Conifers, including araucarians (a sister group to the podocarps, such as the New Zealand kauri), included both smaller shrubs and large woody trees, such as the massive tree trunks of Araucarioxylon arizonicum, the state fossil of Arizona. (Summarised from Fraser & Henderson (2006), p. 55-60.)

Cretaceous

Early Cretaceous vegetation was broadly similar to that of Late Jurassic times, both in distribution and general composition. Low paleolatitudes at that time were arid, having desert and sub-desert conditions, and here the floras were dominated by cheirolepidiacean conifers and matoniacean ferns. Northern mid paleolatitude floras were more diverse, including ferns, bennettitaleans, cycads, conifers and some ginkgos. At higher latitudes, diversity declined again, the floras dominated by leptostrobaleans and ginkgos. Southern mid paleolatitudes were dominated by bennettitaleans and cheirolepidiacean conifers. (Adapted from Cleal & Thomas 2009.)

The most striking event in the evolution of plants during the Cretaceous was certainly the enormous radiation of angiosperms.

The angiosperms (flowering plants) are the most diverse group of land plants living today, comprising some 270,000 described species – more than all other groups of land plants combined – placed in about 380 families and 83 orders (Mayr 2001, p. 64) and dominating modern plant ecosystems. “In theior rise to ecological dominance angiosperms have exhibited extraordinary developmental and evolutionary plasticity. This has resulted in overwhelming morphological diversity and a great variety of adaptive types. Angiosperms are far more diverse in vegetative form and in the structure of their reproductive organs than any other group of land plants” (Friis et al. 2011, p. 1).

The group may have evolved from either the Gnetales or possibly the Bennettitales (Willis & McElwain 2002, p. 184).

The enormous radiation of this group has largely occurred since the mid-Cretaceous, coevolving with a similar radiation of insects. However, the angiosperms must have arisen earlier: The most recent common ancestor of all living flowering plants is estimated to have existed perhaps as early as the Triassic or even the late Carboniferous (Qui et al. 1999) or, more conservatively, “between the Triassic and the Early Cretaceous (~247–136 million years ago” (Ramirez-Barahona et al. 2020). Evidence supporting the earliest date estimates is mainly provided by calibrated genetic divergence studies, though fossil angiosperm-like pollen and leaves have been found dating back to the late Triassic. Several form-species of Crinopolles-type pollen possessing a tectate wall have been described, dating to perhaps 220 Ma. The oldest leaves are somewhat younger, perhaps 210 Ma (Norian; Late Triassic), and include the problematic taxa Furcula and Sanmiguelia.

That being said, however, current orthodoxy is that the first true angiosperms evolved in the Early Cretaceous, probably in the Valanginian (~140 to ~133 Ma) or Hauterivian (~133 to ~129 Ma) ages. The oldest unequivocal angiosperm pollen grains first appear in the fossil record “during the Valanginian-Hauterivian; they spread out of the tropics in the Aptian and Albian [~125.0 to 100.5 Ma], and radiated in the Late Cretaceous” (Harris & Arens 2016, p. 640).

Some of the earliest “body” fossils are “small plants, possibly rooted aquatics or wetland herbs” (Wing 2004, p. 90). “Compression flowers in general, however, are rare, and it is usually only the large ones which are seen. Some years ago, sieving techniques used for Tertiary sediments were applied to the Cretaceous, and yielded a previously unimagined diversity of Cretaceous angiosperm flowers, from sites in North America, Sweden, Portugal, Kazachstan, and Japan. It is now becoming clear how lineages are related. The earliest pollen is 135 million years old, and many basal eudicot lineages were fully established by about 110 Ma. Insect pollination is overwhelmingly supported by the evidence, and was probably important for enhancing speciation rates. Once started, the radiation of angiosperms, especially in low latitudes, kept rising, and shows no sign of levelling off in the Tertiary” (Clarkson 1999, p. 53).

“The earliest unequivocal fossils assignable to angiosperms, probably representing small understorey plants thriving under warm climates, appear in the Early Cretaceous of northern Gondwana (~133–125 Ma), in areas roughly corresponding to the present-day Mediterranean region. Shortly thereafter, angiosperms experienced a major burst of morphological and ecological diversification, which by the middle Cretaceous (~115–100 Ma) had triggered the evolution of most extant lineages. Overwhelming palaeobotanical evidence indicates that, in many regions, the initial burst of diversification of angiosperms was not reflected in their ecological dominance” (Ramirez-Barahona et al. 2020; references elided).

“Until the 1970s not a great deal was known about fossil flowers. Since then our knowledge has grown explosively. For example, the mid-Cretaceous Archaeanthus, from Russell, Kansas, now one of the best-known early flowers, has been the subject of extensive research. The flower is borne terminally on a long axis, and the seeds can be macerated out. The stamens and tepals are known from scars, resin bodies are scattered in the fruit and tepals, and all these features, together with the morphology, indicate an evident relation to the extant Magnoliacea” (Clarkson 1999, p. 53).

Genetic evidence (Zanis et al. 2002) strongly suggests that the most ‘primitive’ (basal) living angiosperm is a little known shrub called Amborella trichopoda; a small shrub with tiny greenish-yellow flowers and red fruit, native to the South Pacific island of New Caledonia. The Nymphaeales (waterlilies and their relatives) are also contenders for the distinction of being the most basal living angiosperms.

Perhaps the most basal fossil group yet to be well-delineated within the angiosperm clade is the Archaefructaceae, a family of herbaceous aquatic plants recovered from the Lower Cretaceous or possibly uppermost Jurassic Yixian Formation of western Liaoning, China. These plants had reproductive axes that lacked petals and sepals, and bore stamens in pairs below conduplicate (sharply folded together lengthwise) carpels. One combined morphological and molecular “total evidence” analysis places the Archaefructaceae as a sister group to all extant angiosperms, including Amborella and the Nymphaeales (Sun et al. 2002, p. 900).

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Fig. 3: Amborella trichopoda. [Photograph by Tim Stephens, courtesy of the Arboretum of the University of California, Santa Cruz.]

References

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