Mitotic topologies and mechanics of Neoproterozoic algae and animal embryos

Abstract

Cell division is a key biological process in growth, morphogenesis, and reproduction. Despite our improved understanding of the genetics and dynamics of cell division in all major groups of living organisms, paleontological evidence for cell division is largely restricted to silicified (and some carbonaceous) algae and vascular plants where three-dimensional observation is possible. Animal cell division has been documented in the fossil record to a lesser extent; however, such knowledge is highly desirable in the recently revitalized field of evolutionary developmental biology. Two fundamentally different mitotic cell division topologies are preserved in late Neoproterozoic Doushantuo phosphorites (ca. 550–600 million years old) in South China. Doushantuo algal cells (∼20 μm in diameter) are successively cleaved by mitotic division planes that are offset but not deformed by subsequent cytokinesis. Mitotic division planes in successively cleaving Doushantuo animal embryos (several hundred microns in diameter) are also offset. However, in sharp contrast to Doushantuo algae, Doushantuo animal blastomeres repeatedly shift to mechanically stable configurations by disturbing preexisting division planes. This divergence reflects the underlying cytological and developmental differences between algae and animals. Specifically, the presence/absence of rigid cell walls and different cytokinetic mechanisms, coupled with mechanics at mitotic offsets, contribute to the diverging mitotic topologies in Doushantuo algae and animal embryos. These findings not only confirm previous interpretation of Doushantuo fossils but also provide direct paleontological evidence of cell movement in the development of these early animal fossils.