Carbon isotopes support the presence of extensive land floras pre-dating the origin of vascular plants

Multiple lines of evidence indicate that Earth's land masses became green some 2.7 Ga ago, about 1 billion years after the advent of life. About 2.2 billion years later, land plants abruptly appear in the fossil record and diversify marking the onset of ecologically complex terrestrial communities that persist to the present day. Given this long history of land colonization, surprisingly few studies report direct fossil evidence of emergent vegetation prior to the continuous record of life on land that starts in the mid-Silurian (ca. 420–425 Ma ago). Here we compare stable carbon isotope signatures of fossils from seven Ordovician–Silurian (450–420 Ma old) Appalachian biotas with signatures of coeval marine organic matter and with stable carbon isotope values predicted for Ordovician and Silurian liverworts (BRYOCARB model). The comparisons support a terrestrial origin for fossils in six of the biotas analyzed, and indicate that some of the fossils represent bryophyte-grade plants. Our results demonstrate that extensive land floras pre-dated the advent of vascular plants by at least 25 Ma. The Appalachian fossils represent the oldest direct evidence of widespread colonization of continents. These findings provide a new search image for macrofossil assemblages that contain the earliest stages of land plant evolution. We anticipate they will fuel renewed efforts to search for direct fossil evidence to track the origin of land plants and eukaryotic life on continents further back in geologic time.     

The relationships of vascular plants

Recent phylogenetic research indicates that vascular plants evolved from bryophyte-like ancestors and that this involved extensive modifications to the life cycle. These conclusions are supported by a range of systematic data, including gene sequences, as well as evidence from comparative morphology and the fossil record. Within vascular plants, there is compelling evidence for two major clades, which have been termed lycophytes (clubmosses) and euphyllophytes (seed plants, ferns, horsetails). The implications of recent phylogenetic work are discussed with reference to life cycle evolution and the interpretation of stratigraphic inconsistencies in the early fossil record of land plants. Life cycles are shown to have passed through an isomorphic phase in the early stages of vascular plant evolution. Thus, the gametophyte generation of all living vascular plants is the product of massive morphological reduction. Phylogenetic research corroborates earlier suggestions of a major representational bias in the early fossil record. Mega-fossils document a sequence of appearance of groups that is at odds with that predicted by cladogram topology. It is argued here that the pattern of appearance and diversification of plant megafossils owes more to changing geological conditions than to rapid biological diversification.     

ALTERNATION OF GENERATIONS IN LAND PLANTS: NEW PHYLOGENETIC AND PALAEOBOTANICAL EVIDENCE

Current ideas on the evolution of alternation of generations in land plants are reviewed in the context of important recent advances in plant systematics and the discovery of remarkable new palaeobotanical evidence on early embryophyte life cycles. An overview of relationships in major groups of green plants is presented together with a brief review of the early fossil record as a prelude to discussing hypotheses of life cycle evolution. Recent discoveries of life cycles in the early fossil record are described and assessed. The newly discovered gametophyte and sporophyte associations are based on exceptionally well-preserved material from the Rhynie Chert, Scotland (Middle Devonian: 380–408 Myr) and compression fossils from other Devonian localities. These data document diplobiontic life cycles in plants at the ‘protracheophyte’ and early tracheophyte level of organization. Furthermore, the early fossils have a more or less isomorphic alternation of generations, a striking departure from life cycles in extant embryophytes. This unexpected similarity between gametophyte and sporophyte calls for a cautious approach in identifying ploidy level in early groups. Viewed in a systematic context, the neontological and palaeontological data contribute towards the formulation of a coherent hypothesis of life cycle evolution in major, early embryophyte groups. Evidence from extant groups strongly supports a single direct origin of the diplobiontic life cycles of land plants from haploid, haplobiontic life cycles in ancestral ‘charophycean algae’. The interest of the new palaeobotanical data lies in its relevance to life cycle evolution at the restricted level of vascular plants rather than at the more general level of embryophytes (vascular plants plus ‘bryophytes’). The occurrence of morphologically complex, axial gametophytes in early vascular plants is consistent with the moss sister-group proposed in some cladistic analyses. Similarities of moss gametophytes to fossils in the vascular plant stem-group are discussed, and it is argued that the late appearance of mosses in the macrofossil record may be due to the problem of recognizing stem-group taxa. The new palaeobotanical evidence conflicts with previous hypotheses based on extant groups that interpret morphological simplicity as the plesiomorphic condition in the gametophytes of vascular plants. These new data indicate that a significant elaboration of both gametophyte and sporophyte occurred early in the tracheophyte lineage, and that the gametophytes of extant ‘pteridophytes’ are highly reduced compared to those of some of the earliest ‘protracheophytes’. Vestiges of this early morphological complexity may remain in the gametophytes of some extant groups such as Lycopodiaceae.     

The early evolution of land plants,from fossils to genomics: a commentary on Lang (1937) ‘On the plant-remains from the Downtonian of England and Wales'

During the 1920s, the botanist W. H. Lang set out to collect and investigate some very unpromising fossils of uncertain affinity, which predated the known geological record of life on land. His discoveries led to a landmark publication in 1937, ‘On the plant-remains from the Downtonian of England and Wales’, in which he revealed a diversity of small fossil organisms of great simplicity that shed light on the nature of the earliest known land plants. These and subsequent discoveries have taken on new relevance as botanists seek to understand the plant genome and the early evolution of fundamental organ systems. Also, our developing knowledge of the composition of early land-based ecosystems and the interactions among their various components is contributing to our understanding of how life on land affects key Earth Systems (e.g. carbon cycle). The emerging paradigm is one of early life on land dominated by microbes, small bryophyte-like organisms and lichens. Collectively called cryptogamic covers, these are comparable with those that dominate certain ecosystems today. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society.     

A molecular timeline for the origin of photosynthetic eukaryotes

The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.     

Bees diversified in the age of eudicots

Reliable estimates on the ages of the major bee clades are needed to further understand the evolutionary history of bees and their close association with flowering plants. Divergence times have been estimated for a few groups of bees, but no study has yet provided estimates for all major bee lineages. To date the origin of bees and their major clades, we first perform a phylogenetic analysis of bees including representatives from every extant family, subfamily and almost all tribes, using sequence data from seven genes. We then use this phylogeny to place 14 time calibration points based on information from the fossil record for an uncorrelated relaxed clock divergence time analysis taking into account uncertainties in phylogenetic relationships and the fossil record. We explore the effect of placing a hard upper age bound near the root of the tree and the effect of different topologies on our divergence time estimates. We estimate that crown bees originated approximately 123 Ma (million years ago) (113–132 Ma), concurrently with the origin or diversification of the eudicots, a group comprising 75 per cent of angiosperm species. All of the major bee clades are estimated to have originated during the Middle to Late Cretaceous, which is when angiosperms became the dominant group of land plants.     

The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence

It is often assumed that life originated and diversified in the oceans prior to colonizing the land. However, environmental constraints in chemical evolution models point towards critical steps leading to the origin of life as having occurred in subaerial settings. The earliest fossil record does not include finds from terrestrial deposits, so much of our understanding about the presence of a terrestrial microbial cover prior to the Proterozoic is based on inference and geochemical proxies that indicate biospheric carbon cycling during the Archaean. Our assessment is that by 2.7 Ga, microbial ecosystems in terrestrial settings were driven by oxygen‐generating, photosynthetic cyanobacteria. Studies of modern organisms indicate that both the origin and primary diversification of the eukaryotes could have occurred in terrestrial settings, shortly after 2.0 Ga, but there is no direct fossil evidence of terrestrial eukaryotes until about 1.1 Ga. At this time, it appears that the diversity of life in non‐marine habitats exceeded that found in marine settings where sulphidic seas may have impaired eukaryotic physiology and retarded evolution. Geochemical proxies indicate the establishment of an extensive soil‐forming microbial cover by 850 Ma, and it is possible that a rise in atmospheric oxygen at this time was due to the evolutionary expansion of green algae into terrestrial habitats. Direct fossil evidence of the earliest terrestrial biotas in the Phanerozoic consists of problematical palynomorphs from the Cambro‐Ordovician of Laurentia. These indicate that the evolution of the first land plants (embryophytes) during the Middle Ordovician took place within a landscape that included aeroterrestrial algae which were actively adapting to selection in subaerial settings.     

The origin and early evolution of tracheids in vascular plants: integration of palaeobotanical and neobotanical data

Although there is clear evidence for the establishment of terrestrial plant life by the end of the Ordovician, the fossil record indicates that land plants remained extremely small and structurally simple until the Late Silurian. Among the events associated with this first major radiation of land plants is the evolution of tracheids, complex water-conducting cells defined by the presence of lignified secondary cell wall thickenings. Recent palaeobotanical analyses indicate that Early Devonian tracheids appear to possess secondary cell wall thickenings composed of two distinct layers: a degradation-prone layer adjacent to the primary cell wall and a degradation-resistant (possibly lignified) layer next to the cell lumen. In order to understand better the early evolution of tracheids, developmental and comparative studies of key basal (and potentially plesiomorphic) extant vascular plants have been initiated. Ultrastructural analysis and enzyme degradation studies of wall structure (to approximate diagenetic alterations of fossil tracheid structure) have been conducted on basal members of each of the two major clades of extant vascular plants: Huperzia (Lycophytina) and Equisetum (Euphyllophytina. This research demonstrates that secondary cell walls of extant basal vascular plants include a degradation-prone layer ('template layer') and a degradation-resistant layer ('resistant layer'). This pattern of secondary cell wall formation in the water-conducting cells of extant vascular plants matches the pattern of wall thickenings in the tracheids of early fossil vascular plants and provides a key evolutionary link between tracheids of living vascular plants and those of their earliest fossil ancestors. Further studies of tracheid development and structure among basal extant vascular plants will lead to a more precise reconstruction of the early evolution of water-conducting tissues in land plants, and will add to the current limited knowledge of spatial, temporal and cytochemical aspects of cell wall formation in tracheary elements of vascular plants.     

Large-Scale Phylogenomic Analyses Reveal the Monophyly of Bryophytes and Neoproterozoic Origin of Land Plants

The relationships among the four major embryophyte lineages (mosses, liverworts, hornworts, vascular plants) and the timing of the origin of land plants are enigmatic problems in plant evolution. Here, we resolve the monophyly of bryophytes by improving taxon sampling of hornworts and eliminating the effect of synonymous substitutions. We then estimate the divergence time of crown embryophytes based on three fossil calibration strategies, and reveal that maximum calibration constraints have a major effect on estimating the time of origin of land plants. Moreover, comparison of priors and posteriors provides a guide for evaluating the optimal calibration strategy. By considering the reliability of fossil calibrations and the influences of molecular data, we estimate that land plants originated in the Precambrian (980–682 Ma), much older than widely recognized. Our study highlights the important contribution of molecular data when faced with contentious fossil evidence, and that fossil calibrations used in estimating the timescale of plant evolution require critical scrutiny.     

THE ORIGIN OF THE LAND PLANT SPOROPHYTE: AN INTERPOLATIONAL SCENARIO

The origin of terrestrial plants from a charophycean ancestor is assumed as a basis for the consideration of the origin of life histories amongst this group. Charophycean algae are vegetatively gametophytic, thus requiring the interpolation of the multicellular sporophytic stage. The model presented here derives the sporophyte and typical sporangial contents from the zygospore produced from the reproductive structure of a hypothetical charophycean land plant ancestor. The presence of monads, dyads, and various forms of tetrads in the fossil record of presumed land plants add support to this model. In addition, such spore types suggest that the temporal relationship of meiosis to sporopollenin deposition was less strictly controlled than in extant land plants.     

The origin and early evolution of whales: macroevolution documented on the Indian Subcontinent

The origin of whales (order Cetacea) from a four-footed land animal is one of the best understood examples of macroevolutionary change. This evolutionary transition has been substantially elucidated by fossil finds from the Indian subcontinent in the past decade and a half. Here, we review the first steps of whale evolution, i.e. the transition from a land mammal to obligate marine predators, documented by the Eocene cetacean families of the Indian subcontinent: Pakicetidae, Ambulocetidae, Remingtonocetidae, Protocetidae, and Basilosauridae, as well as their artiodactyl sister group, the Raoellidae. We also discuss the influence that the excellent fossil record has on the study of the evolution of organ systems, in particular the locomotor and hearing systems.     

Environmental Damage Assessment of Carbon Capture and Storage

An end‐point life cycle impact assessment is used to evaluate the damages of electricity generation from fossil fuel‐based power plants with carbon dioxide capture and storage (CCS) technology. Pulverized coal (PC), integrated gasification combined cycle (IGCC), and natural gas combined cycle (NGCC) power plants are assessed for carbon dioxide (CO₂) capture, pipeline transport, and storage in a geological formation. Results show that the CCS systems reduce the climate change‐related damages but increase the damages from toxicity, acidification, eutrophication, and resource consumption. Based on the currently available damage calculation methods, it is concluded that the benefit of reducing damage from climate change is larger than the increases in other damage categories, such as health effects from particulates or toxic chemicals. CCS significantly reduces the overall environmental damage, with a net reduction of 60% to 70% in human health damage and 65% to 75% in ecosystem damage. Most of the damage is due to fuel production and combustion processes. The energy and infrastructure demands of CCS cause increases in the depletion of natural resources by 33% for PC, 19% for IGCC, and 18% for NGCC power plants, mostly due to increased fossil fuel consumption.     

Consensus,uncertainties and challenges for perennial bioenergy crops and land use

Perennial bioenergy crops have significant potential to reduce greenhouse gas (GHG) emissions and contribute to climate change mitigation by substituting for fossil fuels; yet delivering significant GHG savings will require substantial land‐use change, globally. Over the last decade, research has delivered improved understanding of the environmental benefits and risks of this transition to perennial bioenergy crops, addressing concerns that the impacts of land conversion to perennial bioenergy crops could result in increased rather than decreased GHG emissions. For policymakers to assess the most cost‐effective and sustainable options for deployment and climate change mitigation, synthesis of these studies is needed to support evidence‐based decision making. In 2015, a workshop was convened with researchers, policymakers and industry/business representatives from the UK, EU and internationally. Outcomes from global research on bioenergy land‐use change were compared to identify areas of consensus, key uncertainties, and research priorities. Here, we discuss the strength of evidence for and against six consensus statements summarising the effects of land‐use change to perennial bioenergy crops on the cycling of carbon, nitrogen and water, in the context of the whole life‐cycle of bioenergy production. Our analysis suggests that the direct impacts of dedicated perennial bioenergy crops on soil carbon and nitrous oxide are increasingly well understood and are often consistent with significant life cycle GHG mitigation from bioenergy relative to conventional energy sources. We conclude that the GHG balance of perennial bioenergy crop cultivation will often be favourable, with maximum GHG savings achieved where crops are grown on soils with low carbon stocks and conservative nutrient application, accruing additional environmental benefits such as improved water quality. The analysis reported here demonstrates there is a mature and increasingly comprehensive evidence base on the environmental benefits and risks of bioenergy cultivation which can support the development of a sustainable bioenergy industry.     

Delayed recovery of non-marine tetrapods after the end-Permian mass extinction tracks global carbon cycle

During the end-Permian mass extinction, marine ecosystems suffered a major drop in diversity, which was maintained throughout the Early Triassic until delayed recovery during the Middle Triassic. This depressed diversity in the Early Triassic correlates with multiple major perturbations to the global carbon cycle, interpreted as either intrinsic ecosystem or external palaeoenvironmental effects. In contrast, the terrestrial record of extinction and recovery is less clear; the effects and magnitude of the end-Permian extinction on non-marine vertebrates are particularly controversial. We use specimen-level data from southern Africa and Russia to investigate the palaeodiversity dynamics of non-marine tetrapods across the Permo-Triassic boundary by analysing sample-standardized generic richness, evenness and relative abundance. In addition, we investigate the potential effects of sampling, geological and taxonomic biases on these data. Our analyses demonstrate that non-marine tetrapods were severely affected by the end-Permian mass extinction, and that these assemblages did not begin to recover until the Middle Triassic. These data are congruent with those from land plants and marine invertebrates. Furthermore, they are consistent with the idea that unstable low-diversity post-extinction ecosystems were subject to boom-bust cycles, reflected in multiple Early Triassic perturbations of the carbon cycle.     

Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record

Major fluctuations in the concentrations of atmospheric CO₂ and O₂, are predicted by historical long-term carbon and oxygen cycle models of atmospheric evolution and will have impacted directly on past climates, plant function and evolutionary processes. Here, palaeobotanical evidence is presented from the stomatal density record of fossil leaves spanning the past 400 Myr supporting the predicted changes in atsmopheric CO₂. Evidence from experiments on plants exposed to long-term high CO₂, environments and the newly-assembled fossil data indicate the potential for genetic modification of stomatal characters. The influence of the changes in fossil stomatal characteristics and atmospheric composition on the rates of leaf gas exchange over the course of land plant evolution has been investigated through modelling. Three contrasting eras of plain water economics emerge in the Devonian (high), Carboniferous (low) and from the Upper Jurassic to the present-day (high but declining). These patterns of change result from structural changes of the leaves and the impact of atmospheric CO₂, and O₂, concentrations on RuBisCo function and are consistent with the fossil evidence of sequential appearances of novel plant anatomical changes. The modelling approach is tested by comparing predicted leaf stable carbon isotope ratios with those measured on fossil plant and organic material. Viewed in a geological context, current and future increases in the concentration of atmospheric CO₂, might be considered as restoring plant function to that more typically experienced by plants over the majority of their evolutionary history.     

Implications of land class and environmental factors on life cycle GHG emissions of Miscanthus as a bioenergy feedstock

Replacement of fossil fuels with sustainably produced biomass crops for energy purposes has the potential to make progress in addressing climate change concerns, nonrenewable resource use, and energy security. The perennial grass Miscanthus is a dedicated energy crop candidate being field tested in Ontario, Canada, and elsewhere. Miscanthus could potentially be grown in areas of the province that differ substantially in terms of agricultural land class, environmental factors and current land use. These differences could significantly affect Miscanthus yields, input requirements, production practices, and the types of crops being displaced by Miscanthus establishment. This study assesses implications on life cycle greenhouse gas (GHG) emissions of these differences through evaluating five Miscanthus production scenarios within the Ontario context. Emissions associated with electricity generation with Miscanthus pellets in a hypothetically retrofitted coal generating station are examined. Indirect land use change impacts are not quantified but are discussed. The net life cycle emissions for Miscanthus production varied greatly among scenarios (?90–170 kg CO₂eq per oven dry tonne of Miscanthus bales at the farm gate). In some cases, the carbon stock dynamics of the agricultural system offset the combined emissions of all other life cycle stages (i.e., production, harvest, transport, and processing of biomass). Yield and soil C of the displaced agricultural systems are key parameters affecting emissions. The systems with the highest potential to provide reductions in GHG emissions are those with high yields, or systems established on land with low soil carbon. All scenarios have substantially lower life cycle emissions (?20–190 g CO₂eq kWh^?1) compared with coal‐generated electricity (1130 g CO₂eq kWh^?1). Policy development should consider the implication of land class, environmental factors, and current land use on Miscanthus production.     

Photorespiration has a dual origin and manifold links to central metabolism

Photorespiration is a Janus-headed metabolic process: it makes oxygenic photosynthesis possible by scavenging its major toxic by-product, 2-phosphoglycolate, but also leads to high losses of freshly assimilated CO(2) from most land plants. Photorespiration has been often classified as a wasteful process but is now increasingly appreciated as a key ancillary component of photosynthesis and therefore the global carbon cycle. As such, the photorespiratory cycle is one of the major highways for the flow of carbon in the terrestrial biosphere. Recent research revealed that this important pathway originated as a partner of oxygenic photosynthesis billions of years ago and is multiply linked to other pathways of central metabolism of contemporary land plants.     

Early evolution of life cycles in embryophytes:A focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity

Embryophytes (land plants) are distinguished from their green algal ancestors by diplobiontic life cycles,that is,alternation of multicellular gametophytic and sporophytic generations.The bryophyte sporophyte is small and matrotrophic on the dominant gametophyte; extant vascular plants have an independent,dominant sporophyte and a reduced gametophyte.The elaboration of the diplobiontic life cycle in embryophytes has been thoroughly discussed within the context of the Antithetic and the Homologous Theories.The Antithetic Theory proposes a green algal ancestor with a gametophyte-dominant haplobiontic life cycle.The Homologous Theory suggests a green algal ancestor with alternation of isomorphic generations.The shifts that led from haplobiontic to diplobiontic life cycles and from gametophytic to sporophytic dominance are most probably related with terrestrial habitats.Cladistic studies strongly support the Antithetic Theory in repeatedly identifying charophycean green algae as the closest relatives of land plants.In recent years,exceptionally well-preserved axial gametophytes have been described from the Rhynie chert (Lower Devonian,410 Ma),and the complete life cycle of several Rhynie chert plants has been reconstructed.All show an alternation of more or less isomorphic generations,which is currently accepted as the plesiomorphic condition among all early polysporangiophytes,including basal tracheophytes.Here we review the existing evidence for early embryophyte gametophytes.We also discuss some recently discovered plants preserved as compression fossils and interpreted as gametophytes.All the fossil evidence supports the Antithetic Theory and indicates that the gametophytic generation/sporophytic generation size and complexity ratios show a gradual decrease along the land plant phylogenetic tree.     

Early evolution of life cycles in embryophytes: A focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity

Abstract Embryophytes (land plants) are distinguished from their green algal ancestors by diplobiontic life cycles, that is, alternation of multicellular gametophytic and sporophytic generations. The bryophyte sporophyte is small and matrotrophic on the dominant gametophyte; extant vascular plants have an independent, dominant sporophyte and a reduced gametophyte. The elaboration of the diplobiontic life cycle in embryophytes has been thoroughly discussed within the context of the Antithetic and the Homologous Theories. The Antithetic Theory proposes a green algal ancestor with a gametophyte‐dominant haplobiontic life cycle. The Homologous Theory suggests a green algal ancestor with alternation of isomorphic generations. The shifts that led from haplobiontic to diplobiontic life cycles and from gametophytic to sporophytic dominance are most probably related with terrestrial habitats. Cladistic studies strongly support the Antithetic Theory in repeatedly identifying charophycean green algae as the closest relatives of land plants. In recent years, exceptionally well‐preserved axial gametophytes have been described from the Rhynie chert (Lower Devonian, 410 Ma), and the complete life cycle of several Rhynie chert plants has been reconstructed. All show an alternation of more or less isomorphic generations, which is currently accepted as the plesiomorphic condition among all early polysporangiophytes, including basal tracheophytes. Here we review the existing evidence for early embryophyte gametophytes. We also discuss some recently discovered plants preserved as compression fossils and interpreted as gametophytes. All the fossil evidence supports the Antithetic Theory and indicates that the gametophytic generation/sporophytic generation size and complexity ratios show a gradual decrease along the land plant phylogenetic tree.