Convergent occurrence of the developmental hourglass in plant and animal embryogenesis?

Abstract

Background: The remarkable similarity of animal embryos at particular stages of development led to the proposal of a developmental hourglass. In this model, early events in development are less conserved across species but lead to a highly conserved 'phylotypic period'. Beyond this stage, the model suggests that development once again becomes less conserved, leading to the diversity of forms. Recent comparative studies of gene expression in animal groups have provided strong support for the hourglass model. How and why might such an hourglass pattern be generated? More importantly, how might early acting events in development evolve while still maintaining a later conserved stage?

Scope: The discovery that an hourglass pattern may also exist in the embryogenesis of plants provides comparative data that may help us explain this phenomenon. Whether the developmental hourglass occurs in plants, and what this means for our understanding of embryogenesis in plants and animals is discussed. Models by which conserved early-acting genes might change their functional role in the evolution of gene networks, how networks buffer these changes, and how that might constrain, or confer diversity, of the body plan are also discused.

Conclusions: Evidence of a morphological and molecular hourglass in plant and animal embryogenesis suggests convergent evolution. This convergence is likely due to developmental constraints imposed upon embryogenesis by the need to produce a viable embryo with an established body plan, controlled by the architecture of the underlying gene regulatory networks. As the body plan is largely laid down during the middle phases of embryo development in plants and animals, then it is perhaps not surprising this stage represents the narrow waist of the hourglass where the gene regulatory networks are the oldest and most robust and integrated, limiting species diversity and constraining morphological space.

Keywords: Embryogenesis; comparative transcriptomic analysis; convergent evolution; developmental hourglass; developmental networks; gene expression.

Fig. 1.

Comparison of the morphological and transcriptome hourglass model between flowering plants and animals. In both panels, embryogenesis proceeds from the bottom to the top (early, mid and late stages), and the width represents the morphological and transcriptome diversity. Left: the hourglass model in flowering plants predicts that the mid-embryonic stage (globular to torpedo) is the most conserved stage. Plant embryogenesis begins with the formation of the zygote, followed by several rounds of mitotic divisions to produce a cluster of cells, the globular embryo. The embryo passes from the globular stage through a transition stage to the heart stage, and finally reaches the torpedo stage, in which all the tissue types and organs have been established. Late-stage embryos lack morphological conservation (dark green area) but exhibit transcriptional variation (light green area). Right: the hourglass model in animals predicts that the morphological ‘phylotypic period’ around the mid-embryonic stages is the most conserved. Animal embryogenesis begins with the formation of the zygote followed by several rounds of mitotic divisions to produce a cluster of cells in which the main axes of the adult morphology are established, and the broad domains of the body plan defined. The subsequent middle period of embryogenesis is also known as the ‘phylotypic period’ as species in common phyla share morphological similarities despite differences in the early stages. In the last stage of embryo development, the limbs, organs, eyes and other structures form, resulting in the final structures of the adult or larvae. By the end of development, the differing growth and patterning trajectories of different species lead to increased divergence and diversity in adult body plans.

Fig. 2.

The two major hypotheses about how developmental processes are conserved. In both models, embryogenesis proceeds from the bottom to the top (early, mid and late stages), and the width represents the phylogenetic diversity of developmental processes, which are deduced from morphological similarities. Left: the funnel-like model predicts conservation at the earliest embryonic stage. During embryogenesis, diversity increases additively and progressively, leading to the diversity of forms. Right: the hourglass model predicts conservation of the ‘phylotypic period’. During embryogenesis, early events in development are less conserved across species but lead to a highly conserved ‘phylotypic period’. Beyond this stage, the model suggests that development once again becomes less conserved, leading to the diversity of forms.