| Abstract |
Animal embryogenesis is a multi-faceted phenomenon through which a single-celled zygote is transformed into a multi-cellular organism with a complex morphology and the ability to feed as well as locomote. Embryos of species that constitute the bulk of animal phylogeny rely on maternally-supplied energy sources to fuel their early development until they hatch into a feeding form. Although animal embryogenesis has been studied extensively across species from the point of view of morphogenesis and gene expression, a large-scale systematic comparison from the perspective of energy metabolism has been missing. In this work, I address a broad question by sampling different nodes of the phylogenetic tree: how much energy do different clades spend on their early development, and at what rate do they usually do this? The main species included in this work are: an insect − Drosophila melanogaster, a fish − Danio rerio, a cnidarian sea anemone − Nematostella vectensis, a marine segmented worm − Platynereis dumerilii, and an echinoderm sea star − Patiria miniata. Using isothermal calorimetry to measure the energy dissipation rate as a readout for overall metabolic activity, I demonstrate that animal embryogenesis is fuelled by a continuously changing rate of energy expenditure, which lies on different orders of magnitude for different species. Combining these data with quantitative measures of developmental dynamics such as cell number and size acquired through imaging reveals common features underlying the observed trends of heat dissipation rates. First, the volume-specific heat dissipation rate tends to increase continuously in the absence of volumetric growth of the embryo. This means that the splitting of a unit-volume of embryonic tissue into more and more cells simply by reductive divisions leads to a continuous increase in its energy dissipation rate. The onset of growth, on the other hand, is associated with a lowering of volume-specific dissipation rate. Next, the overall embryonic energy dissipation rate depends on the number of cells in the embryo at any given time, and can be theoretically described as a function of the number of cells, N. This mathematical relationship indicates that the increase in the energy dissipation rate is initially dominated by the total surface or plasma membrane coverage of the embryo (N^1/3). In some cases, it later switches to a scaling with a term directly proportional to the number of cells (N) around the time of the maternal-to-zygotic transition at a characteristic species-specific cell number (N∗). A gradient of surface-associated mitochondrial activation underlies the early surface-scaling observed in the mathematical model, and leads to the activation of more and more mitochondria at the whole-embryo level with successive rounds of reductive divisions. This gradient may contribute to the establishment of species-specific values of N∗ and provide insights into the timing of the maternal-to-zygotic transition in different species. In summary, common features of energy expenditure do exist even in distantly related species − they are combined together by different developmental modes to give rise to species-specific patterns of embryonic energy expenditure. This suggests that energy metabolism might constitute an ancient constraint in the evolution of developmental modes. |