How Advances in Phylogenetic Methods Change Our Understanding of the Evolutionary Emergence of Land Plants (Embryophyta)

Abstract

The origin and subsequent evolution of land plants have transformed the terrestrial environment, with their emergence leading to profound changes to the Earth's ecosystem, climate and the evolution of life. Embryophyta (land plants) evolved once, so to understand this event we need an accurate phylogeny of their four principal lineages: bryophytes (mosses, hornworts, liverworts) and the more complex vascular tracheophytes (e.g. ferns, conifers and flowering plants). Phylogenetic inference has supported seven different hypotheses of how these four lineages are related, each with different implications for the anatomy, genome and physiology of the ancestral embryophyte. Recent developments in phylogenetics mean that we cannot assume that the first plants to live on land resembled modern bryophytes, and that the ancestral embryophyte may have been more complex than previously thought. Key Concepts Land plants include flowering plants, conifers, cycads, ferns, lycophytes and mosses that contribute a considerable proportion of living biomass. Before land plants, there was a barren, rocky terrestrial environment with a minimal, superficial biological cover. Embryophyta (land plants) evolved once from an aquatic algal ancestor in the green clade Streptophyta. After their emergence, embryophytes led to the development of soils, changes in the global climate and affected the evolution of other groups, including animals and fungi. The early‐diverging topology of the land plants consists of the bryophytes (liverworts, mosses and hornworts) and the tracheophytes. It is generally assumed the biology of bryophytes (e.g. small size, haploid‐dominated life cycle, no vascular tissue) is representative of the ancestral embryophyte, and tracheophytes subsequently acquired their complexity. Studies have supported seven alternative arrangements between the four lineages (liverworts, hornworts, mosses, tracheophytes) of land plants. Despite the development of sophisticated phylogenetic techniques and new sources of data, there has been a continuous debate around the phylogeny of early land plants. Many results do not support a natural grouping of bryophytes, indicating they do not share a single recent ancestor (e.g. they are paraphyletic). This arrangement suggests that the bryophytes emerged sequentially, and the tracheophytes are derived. Recent research shows the topology of sequentially diverging bryophyte lineages and the tracheophytes is the result of model biases. More recent studies support the monophyly of bryophytes by correcting for the model biases, with a grouping of the mosses and liverworts in a clade called Setaphyta . The new topology with an initial split between vascular plants and a natural group of bryophytes has important evolutionary implications. We cannot accept that the ancestral embryophyte resembled a modern bryophyte in biology. The new topology with a more ambiguous relationship to land plants indicates that the ancestral embryophyte could have been more complex than a modern bryophyte.