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.

Rooting Species Trees Using Gene Tree-Species Tree Reconciliation.

Interpreting phylogenetic trees requires a root, which provides the direction of evolution and polarizes ancestor-descendant relationships. But inferring the root using genetic data is difficult, particularly in cases where the closest available outgroup is only distantly related, which are common for microbes. In this chapter, we present a workflow for estimating rooted species trees and the evolutionary history of the gene families that evolve within them using probabilistic gene tree-species tree reconciliation. We illustrate the pipeline using a small dataset of prokaryotic genomes, for which the example scripts can be run using modest computer resources. We describe the rooting method used in this work in the context or other rooting strategies and discuss some of the limitations and opportunities presented by probabilistic gene tree-species tree reconciliation methods.

The origin and evolution of stomata.

The acquisition of stomata is one of the key innovations that led to the colonisation of the terrestrial environment by the earliest land plants. However, our understanding of the origin, evolution and the ancestral function of stomata is incomplete. Phylogenomic analyses indicate that, firstly, stomata are ancient structures, present in the common ancestor of land plants, prior to the divergence of bryophytes and tracheophytes and, secondly, there has been reductive stomatal evolution, especially in the bryophytes (with complete loss in the liverworts). From a review of the evidence, we conclude that the capacity of stomata to open and close in response to signals such as ABA, CO2 and light (hydroactive movement) is an ancestral state, is present in all lineages and likely predates the divergence of the bryophytes and tracheophytes. We reject the hypothesis that hydroactive movement was acquired with the emergence of the gymnosperms. We also conclude that the role of stomata in the earliest land plants was to optimise carbon gain per unit water loss. There remain many other unanswered questions concerning the evolution and especially the origin of stomata. To address these questions, it will be necessary to: find more fossils representing the earliest land plants, revisit the existing early land plant fossil record in the light of novel phylogenomic hypotheses and carry out more functional studies that include both tracheophytes and bryophytes.

Wingtip folds and ripples on saturniid moths create decoy echoes against bat biosonar.

Sensory coevolution has equipped certain moth species with passive acoustic defenses to counter predation by echolocating bats.1,2 Some large silkmoths (Saturniidae) possess curved and twisted biosonar decoys at the tip of elongated hindwing tails.3,4 These are thought to create strong echoes that deflect biosonar-guided bat attacks away from the moth's body to less essential parts of their anatomy. We found that closely related silkmoths lacking such hindwing decoys instead often possess intriguing ripples and folds on the conspicuously lobed tips of their forewings. The striking analogy of twisted shapes displayed far from the body suggests these forewing structures might function as alternative acoustic decoys. Here we reveal that acoustic reflectivity and hence detectability of such wingtips is higher than that of the body at ultrasonic frequencies used by hunting bats. Wingtip reflectivity is higher the more elaborate the structure and the further from the body. Importantly, wingtip reflectivity is often considerably higher than in a well-studied functional hindwing decoy. Such increased reflectivity would misdirect the bat's sonar-guided attack toward the wingtip, resulting in similar fitness benefits to hindwing acoustic decoys. Structurally, folded wingtips present echo-generating surfaces to many directions, and folds and ripples can act as retroreflectors that together create conspicuous targets. Phylogenetically, folds and ripples at wingtips have evolved multiple times independently within silkmoths and always as alternatives to hindwing decoys. We conclude that they function as acoustic wingtip decoys against bat biosonar. VIDEO ABSTRACT.

Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata.

The origin of land plants was accompanied by new adaptations to life on land, including the evolution of stomata-pores on the surface of plants that regulate gas exchange. The genes that underpin the development and function of stomata have been extensively studied in model angiosperms, such as Arabidopsis. However, little is known about stomata in bryophytes, and their evolutionary origins and ancestral function remain poorly understood. Here, we resolve the position of bryophytes in the land plant tree and investigate the evolutionary origins of genes that specify stomatal development and function. Our analyses recover bryophyte monophyly and demonstrate that the guard cell toolkit is more ancient than has been appreciated previously. We show that a range of core guard cell genes, including SPCH/MUTE, SMF, and FAMA, map back to the common ancestor of embryophytes or even earlier. These analyses suggest that the first embryophytes possessed stomata that were more sophisticated than previously envisioned and that the stomata of bryophytes have undergone reductive evolution, including their complete loss from liverworts.