The three-dimensionally articulated oral apparatus of a Devonian heterostracan sheds light on feeding in Palaeozoic jawless fishes.

Attempts to explain the origin and diversification of vertebrates have commonly invoked the evolution of feeding ecology, contrasting the passive suspension feeding of invertebrate chordates and larval lampreys with active predation in living jawed vertebrates. Of the extinct jawless vertebrates that phylogenetically intercalate these living groups, the feeding apparatus is well-preserved only in the early diverging stem-gnathostome heterostracans. However, its anatomy remains poorly understood. Here, we use X-ray microtomography to characterize the feeding apparatus of the pteraspid heterostracan Rhinopteraspis dunensis (Roemer, 1855). The apparatus is composed of 13 plates arranged approximately bilaterally, most of which articulate from the postoral plate. Our reconstruction shows that the oral plates were capable of rotating around the transverse axis, but likely with limited movement. It also suggests the nasohypophyseal organs opened internally, into the pharynx. The functional morphology of the apparatus in Rhinopteraspis precludes all proposed interpretations of feeding except for suspension/deposit feeding and we interpret the apparatus as having served primarily to moderate the oral gape. This is consistent with evidence that at least some early jawless gnathostomes were suspension feeders and runs contrary to macroecological scenarios that envisage early vertebrate evolution as characterized by a directional trend towards increasingly active food acquisition.

Plant evolution: Streptophyte multicellularity, ecology, and the acclimatisation of plants to life on land.

Land plants are celebrated as one of the three great instances of complex multicellularity, but new phylogenomic and phenotypic analyses are revealing deep evolutionary roots of multicellularity among algal relatives, prompting questions about the causal basis of this major evolutionary transition.

Cryogenian Origins of Multicellularity in Archaeplastida.

Earth was impacted by global glaciations during the Cryogenian (720 to 635 million years ago; Ma), events invoked to explain both the origins of multicellularity in Archaeplastida and radiation of the first land plants. However, the temporal relationship between these environmental and biological events is poorly established, due to a paucity of molecular and fossil data, precluding resolution of the phylogeny and timescale of archaeplastid evolution. We infer a time-calibrated phylogeny of early archaeplastid evolution based on a revised molecular dataset and reappraisal of the fossil record. Phylogenetic topology testing resolves deep archaeplastid relationships, identifying two clades of Viridiplantae and placing Bryopsidales as sister to the Chlorophyceae. Our molecular clock analysis infers an origin of Archaeplastida in the late-Paleoproterozoic to early-Mesoproterozoic (1712 to 1387 Ma). Ancestral state reconstruction of cytomorphological traits on this time-calibrated tree reveals many of the independent origins of multicellularity span the Cryogenian, consistent with the Cryogenian multicellularity hypothesis. Multicellular rhodophytes emerged 902 to 655 Ma while crown-Anydrophyta (Zygnematophyceae and Embryophyta) originated 796 to 671 Ma, broadly compatible with the Cryogenian plant terrestrialization hypothesis. Our analyses resolve the timetree of Archaeplastida with age estimates for ancestral multicellular archaeplastids coinciding with the Cryogenian, compatible with hypotheses that propose a role of Snowball Earth in plant evolution.

Hagfish genome elucidates vertebrate whole-genome duplication events and their evolutionary consequences.

Polyploidy or whole-genome duplication (WGD) is a major event that drastically reshapes genome architecture and is often assumed to be causally associated with organismal innovations and radiations. The 2R hypothesis suggests that two WGD events (1R and 2R) occurred during early vertebrate evolution. However, the timing of the 2R event relative to the divergence of gnathostomes (jawed vertebrates) and cyclostomes (jawless hagfishes and lampreys) is unresolved and whether these WGD events underlie vertebrate phenotypic diversification remains elusive. Here we present the genome of the inshore hagfish, Eptatretus burgeri. Through comparative analysis with lamprey and gnathostome genomes, we reconstruct the early events in cyclostome genome evolution, leveraging insights into the ancestral vertebrate genome. Genome-wide synteny and phylogenetic analyses support a scenario in which 1R occurred in the vertebrate stem-lineage during the early Cambrian, and 2R occurred in the gnathostome stem-lineage, maximally in the late Cambrian-earliest Ordovician, after its divergence from cyclostomes. We find that the genome of stem-cyclostomes experienced an additional independent genome triplication. Functional genomic and morphospace analyses demonstrate that WGD events generally contribute to developmental evolution with similar changes in the regulatory genome of both vertebrate groups. However, appreciable morphological diversification occurred only in the gnathostome but not in the cyclostome lineage, calling into question the general expectation that WGDs lead to leaps of bodyplan complexity.

ATP synthase evolution on a cross-braced dated tree of life.

The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating back to more than 4 Ga, potentially predating the diversification of Archaea and Bacteria. Our cross-braced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19 Ga) and bacterial (2.58-2.12 Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

Defining eukaryotes to dissect eukaryogenesis.

The origin of eukaryotes is among the most contentious debates in evolutionary biology, attracting multiple seemingly incompatible theories seeking to explain the sequence in which eukaryotic characteristics were acquired. Much of the controversy arises from differing views on the defining characteristics of eukaryotes. We argue that eukaryotes should be defined phylogenetically, and that doing so clarifies where competing hypotheses of eukaryogenesis agree and how we may test among aspects of disagreement. Some hypotheses make predictions about the phylogenetic origins of eukaryotic genes and are distinguishable on that basis. However, other hypotheses differ only in the order of key evolutionary steps, like mitochondrial endosymbiosis and nuclear assembly, which cannot currently be distinguished phylogenetically. Stages within eukaryogenesis may be made identifiable through the absolute dating of gene duplicates that map to eukaryotic traits, such as in genes of host or mitochondrial origin that duplicated and diverged functionally prior to emergence of the last eukaryotic common ancestor. In this way, it may finally be possible to distinguish heat from light in the debate over eukaryogenesis.

Evolution of phenotypic disparity in the plant kingdom.

The plant kingdom exhibits diverse bodyplans, from single-celled algae to complex multicellular land plants, but it is unclear how this phenotypic disparity was achieved. Here we show that the living divisions comprise discrete clusters within morphospace, separated largely by reproductive innovations, the extinction of evolutionary intermediates and lineage-specific evolution. Phenotypic complexity correlates not with disparity but with ploidy history, reflecting the role of genome duplication in plant macroevolution. Overall, the plant kingdom exhibits a pattern of episodically increasing disparity throughout its evolutionary history that mirrors the evolutionary floras and reflects ecological expansion facilitated by reproductive innovations. This pattern also parallels that seen in the animal and fungal kingdoms, suggesting a general pattern for the evolution of multicellular bodyplans.

Fossilization can mislead analyses of phenotypic disparity.

Analyses of morphological disparity can incorporate living and fossil taxa to facilitate the exploration of how phenotypic variation changes through time. However, taphonomic processes introduce non-random patterns of data loss in fossil data and their impact on perceptions of disparity is unclear. To address this, we characterize how measures of disparity change when simulated and empirical data are degraded through random and structured data loss. We demonstrate that both types of data loss can distort the disparity of clades, and that the magnitude and direction of these changes varies between the most commonly employed distance metrics and disparity indices. The inclusion of extant taxa and exceptionally preserved fossils mitigates these distortions and clarifies the full extent of the data lost, most of which would otherwise go uncharacterized. This facilitates the use of ancestral state estimation and evolutionary simulations to further control for the effects of data loss. Where the addition of such reference taxa is not possible, we urge caution in the extrapolation of general patterns in disparity from datasets that characterize subsets of phenotype, which may represent no more than the traits that they sample.

Postcranial disparity of galeaspids and the evolution of swimming speeds in stem-gnathostomes.

Galeaspids are extinct jawless relatives of living jawed vertebrates whose contribution to understanding the evolutionary assembly of the gnathostome bodyplan has been limited by absence of postcranial remains. Here, we describe Foxaspis novemura gen. et sp. nov., based on complete articulated remains from a newly discovered Konservat-Lagerstätte in the Early Devonian (Pragian, ∼410 Ma) of Guangxi, South China. F. novemura had a broad, circular dorso-ventrally compressed headshield, slender trunk and strongly asymmetrical hypochordal tail fin comprised of nine ray-like scale-covered digitations. This tail morphology contrasts with the symmetrical hypochordal tail fin of Tujiaaspis vividus, evidencing disparity in galeaspid postcranial anatomy. Analysis of swimming speed reveals galeaspids as moderately fast swimmers, capable of achieving greater cruising swimming speeds than their more derived jawless and jawed relatives. Our analyses reject the hypothesis of a driven trend towards increasingly active food acquisition which has been invoked to characterize early vertebrate evolution.

A timescale for placental mammal diversification based on Bayesian modeling of the fossil record.

The timing of the placental mammal radiation has been the focus of debate over the efficacy of competing methods for establishing evolutionary timescales. Molecular clock analyses estimate that placental mammals originated before the Cretaceous-Paleogene (K-Pg) mass extinction, anywhere from the Late Cretaceous to the Jurassic. However, the absence of definitive fossils of placentals before the K-Pg boundary is compatible with a post-Cretaceous origin. Nevertheless, lineage divergence must occur before it can be manifest phenotypically in descendent lineages. This, combined with the non-uniformity of the rock and fossil records, requires the fossil record to be interpreted rather than read literally. To achieve this, we introduce an extended Bayesian Brownian bridge model that estimates the age of origination and, where applicable, extinction through a probabilistic interpretation of the fossil record. The model estimates the origination of placentals in the Late Cretaceous, with ordinal crown groups originating at or after the K-Pg boundary. The results reduce the plausible interval for placental mammal origination to the younger range of molecular clock estimates. Our findings support both the Long Fuse and Soft Explosive models of placental mammal diversification, indicating that the placentals originated shortly prior to the K-Pg mass extinction. The origination of many modern mammal lineages overlapped with and followed the K-Pg mass extinction.

The unbearable uncertainty of panarthropod relationships.

Panarthropoda, the clade comprising the phyla Onychophora, Tardigrada and Euarthropoda, encompasses the largest majority of animal biodiversity. The relationships among the phyla are contested and resolution is key to understanding the evolutionary assembly of panarthropod bodyplans. Molecular phylogenetic analyses generally support monophyly of Onychophora and Euarthropoda to the exclusion of Tardigrada (Lobopodia hypothesis), which is also supported by some analyses of morphological data. However, analyses of morphological data have also been interpreted to support monophyly of Tardigrada and Euarthropoda to the exclusion of Onychophora (Tactopoda hypothesis). Support has also been found for a clade of Onychophora and Tardigrada that excludes Euarthropoda (Protarthropoda hypothesis). Here we show, using a diversity of phylogenetic inference methods, that morphological datasets cannot discriminate statistically between the Lobopodia, Tactopoda and Protarthropoda hypotheses. Since the relationships among the living clades of panarthropod phyla cannot be discriminated based on morphological data, we call into question the accuracy of morphology-based phylogenies of Panarthropoda that include fossil species and the evolutionary hypotheses based upon them.

Constraining Whole-Genome Duplication Events in Geological Time.

The timing of whole-genome duplication (WGD) events is crucial to understanding their role in evolution and underpins many hypotheses linking WGD to increased diversity and complexity. As such, means of estimating the timing of the WGD events relative to their macroevolutionary outcomes are of considerable importance. Molecular clock methods facilitate direct estimation of the absolute timing of WGD events, integrating information on the rate of sequence evolution between species while accommodating the uncertainty inherent to the fossil record. We present an explanation of the best practice for constructing fossil calibrations and estimating the age of WGD events via molecular clock methods in the program MCMCtree, with an example dataset based on a well-characterized WGD event within the flowering dogwoods (Cornus). The approach presented herein allows for the estimation of the age of WGD events and subsequent speciation events, allowing the relationship between WGD and the macroevolutionary outcomes to be explored. In our example, we show that in the case of flowering dogwoods, the WGD event long predates the end-Cretaceous mass extinction and that the two events may be independent.

The origin and early evolution of plants.

Plant (archaeplastid) evolution has transformed the biosphere, but we are only now beginning to learn how this took place through comparative genomics, phylogenetics, and the fossil record. This has illuminated the phylogeny of Archaeplastida, Viridiplantae, and Streptophyta, and has resolved the evolution of key characters, genes, and genomes - revealing that many key innovations evolved long before the clades with which they have been casually associated. Molecular clock analyses estimate that Streptophyta and Viridiplantae emerged in the late Mesoproterozoic to late Neoproterozoic, whereas Archaeplastida emerged in the late-mid Palaeoproterozoic. Together, these insights inform on the coevolution of plants and the Earth system that transformed ecology and global biogeochemical cycles, increased weathering, and precipitated snowball Earth events, during which they would have been key to oxygen production and net primary productivity (NPP).

Internal anatomy of a fossilized embryonic stage of the Cambrian-Ordovician scalidophoran Markuelia.

The Wangcun fossil Lagerstätte in Hunan, South China, has yielded hundreds of fossilized embryos of Markuelia hunanensis representing different developmental stages. Internal tissues have only rarely been observed, impeding further understanding of the soft tissue anatomy, phylogenetic affinity and evolutionary significance of Markuelia. In this study, we used synchrotron radiation X-ray tomographic microscopy (SRXTM) to study a new collection of fossil embryos from the Wangcun fossil Lagerstätte. We describe specimens exhibiting a spectrum of preservation states, the best of which preserves palisade structures underneath the cuticle of the head and tail, distinct from patterns of centripetal mineralization of the cuticle and centrifugal mineralization of hypha-like structures, seen elsewhere in this specimen and other fossils within the same assemblage. Our computed tomographic reconstruction of these mineralization phases preserves the gross morphology of (i) longitudinal structures associated with the tail spines, which we interpret as the proximal ends of longitudinal muscles, and (ii) a ring-shaped structure internal to the introvert, which we interpret as a ring-shaped brain, as anticipated of the cycloneuralian affinity of Markuelia. This is the first record of a fossilized nervous system in a scalidophoran, and the first instance in Orsten-style preservation, opening the potential for further such records within this widespread mode of high-fidelity three-dimensional preservation.

Galeaspid anatomy and the origin of vertebrate paired appendages.

Paired fins are a major innovation1,2 that evolved in the jawed vertebrate lineage after divergence from living jawless vertebrates3. Extinct jawless armoured stem gnathostomes show a diversity of paired body-wall extensions, ranging from skeletal processes to simple flaps4. By contrast, osteostracans (a sister group to jawed vertebrates) are interpreted to have the first true paired appendages in a pectoral position, with pelvic appendages evolving later in association with jaws5. Here we show, on the basis of articulated remains of Tujiaaspis vividus from the Silurian period of China, that galeaspids (a sister group to both osteostracans and jawed vertebrates) possessed three unpaired dorsal fins, an approximately symmetrical hypochordal tail and a pair of continuous, branchial-to-caudal ventrolateral fins. The ventrolateral fins are similar to paired fin flaps in other stem gnathostomes, and specifically to the ventrolateral ridges of cephalaspid osteostracans that also possess differentiated pectoral fins. The ventrolateral fins are compatible with aspects of the fin-fold hypothesis for the origin of vertebrate paired appendages6-10. Galeaspids have a precursor condition to osteostracans and jawed vertebrates in which paired fins arose initially as continuous pectoral-pelvic lateral fins that our computed fluid-dynamics experiments show passively generated lift. Only later in the stem lineage to osteostracans and jawed vertebrates did pectoral fins differentiate anteriorly. This later differentiation was followed by restriction of the remaining field of fin competence to a pelvic position, facilitating active propulsion and steering.

Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants.

The origin of plants and their colonization of land fundamentally transformed the terrestrial environment. Here we elucidate the basis of this formative episode in Earth history through patterns of lineage, gene and genome evolution. We use new fossil calibrations, a relative clade age calibration (informed by horizontal gene transfer) and new phylogenomic methods for mapping gene family origins. Distinct rooting strategies resolve tracheophytes (vascular plants) and bryophytes (non-vascular plants) as monophyletic sister groups that diverged during the Cambrian, 515-494 million years ago. The embryophyte stem is characterized by a burst of gene innovation, while bryophytes subsequently experienced an equally dramatic episode of reductive genome evolution in which they lost genes associated with the elaboration of vasculature and the stomatal complex. Overall, our analyses reveal that extant tracheophytes and bryophytes are both highly derived from a more complex ancestral land plant. Understanding the origin of land plants requires tracing character evolution across a diversity of modern lineages.

Integrative Phylogenetics: Tools for Palaeontologists to Explore the Tree of Life.

The modern era of analytical and quantitative palaeobiology has only just begun, integrating methods such as morphological and molecular phylogenetics and divergence time estimation, as well as phenotypic and molecular rates of evolution. Calibrating the tree of life to geological time is at the nexus of many disparate disciplines, from palaeontology to molecular systematics and from geochronology to comparative genomics. Creating an evolutionary time scale of the major events that shaped biodiversity is key to all of these fields and draws from each of them. Different methodological approaches and data employed in various disciplines have traditionally made collaborative research efforts difficult among these disciplines. However, the development of new methods is bridging the historical gap between fields, providing a holistic perspective on organismal evolutionary history, integrating all of the available evidence from living and fossil species. Because phylogenies with only extant taxa do not contain enough information to either calibrate the tree of life or fully infer macroevolutionary dynamics, phylogenies should preferably include both extant and extinct taxa, which can only be achieved through the inclusion of phenotypic data. This integrative phylogenetic approach provides ample and novel opportunities for evolutionary biologists to benefit from palaeontological data to help establish an evolutionary time scale and to test core macroevolutionary hypotheses about the drivers of biological diversification across various dimensions of organisms.

Evolutionary analysis of swimming speed in early vertebrates challenges the 'New Head Hypothesis'.

The ecological context of early vertebrate evolution is envisaged as a long-term trend towards increasingly active food acquisition and enhanced locomotory capabilities culminating in the emergence of jawed vertebrates. However, support for this hypothesis has been anecdotal and drawn almost exclusively from the ecology of living taxa, despite knowledge of extinct phylogenetic intermediates that can inform our understanding of this formative episode. Here we analyse the evolution of swimming speed in early vertebrates based on caudal fin morphology using ancestral state reconstruction and evolutionary model fitting. We predict the lowest and highest ancestral swimming speeds in jawed vertebrates and microsquamous jawless vertebrates, respectively, and find complex patterns of swimming speed evolution with no support for a trend towards more active lifestyles in the lineage leading to jawed groups. Our results challenge the hypothesis of an escalation of Palaeozoic marine ecosystems and shed light into the factors that determined the disparate palaeobiogeographic patterns of microsquamous versus macrosquamous armoured Palaeozoic jawless vertebrates. Ultimately, our results offer a new enriched perspective on the ecological context that underpinned the assembly of vertebrate and gnathostome body plans, supporting a more complex scenario characterized by diverse evolutionary locomotory capabilities reflecting their equally diverse ecologies.