Evolution of mitotic spindle behavior during the first asymmetric embryonic division of nematodes

Abstract

Asymmetric cell division is essential to generate cellular diversity. In many animal cells, the cleavage plane lies perpendicular to the mitotic spindle, and it is the spindle positioning that dictates the size of the daughter cells. Although some properties of spindle positioning are conserved between distantly related model species and different cell types, little is known of the evolutionary robustness of the mechanisms underlying this event. We recorded the first embryonic division of 42 species of nematodes closely related to Caenorhabditis elegans, which is an excellent model system to study the biophysical properties of asymmetric spindle positioning. Our recordings, corresponding to 128 strains from 27 Caenorhabditis and 15 non-Caenorhabditis species (accessible at http://www.ens-lyon.fr/LBMC/NematodeCell/videos/), constitute a powerful collection of subcellular phenotypes to study the evolution of various cellular processes across species. In the present work, we analyzed our collection to the study of asymmetric spindle positioning. Although all the strains underwent an asymmetric first cell division, they exhibited large intra- and inter-species variations in the degree of cell asymmetry and in several parameters controlling spindle movement, including spindle oscillation, elongation, and displacement. Notably, these parameters changed frequently during evolution with no apparent directionality in the species phylogeny, with the exception of spindle transverse oscillations, which were an evolutionary innovation at the base of the Caenorhabditis genus. These changes were also unrelated to evolutionary variations in embryo size. Importantly, spindle elongation, displacement, and oscillation each evolved independently. This finding contrasts starkly with expectations based on C. elegans studies and reveals previously unrecognized evolutionary changes in spindle mechanics. Collectively, these data demonstrate that, while the essential process of asymmetric cell division has been conserved over the course of nematode evolution, the underlying spindle movement parameters can combine in various ways. Like other developmental processes, asymmetric cell division is subject to system drift.

Organelle size scaling over embryonic development

“…In addition to developmental spindle scaling, correlations between embryo, cell, and spindle sizes have been characterized across a wide variety of different species (Crowder et al, 2015;Farhadifar et al, 2015;Valfort, Launay, Semon, & Delattre, 2018). X. laevis spindles are larger than Xenopus tropicalis spindles (Brown et al, 2007).…”

Age structure landscapes emerge from the equilibrium between aging and rejuvenation in bacterial populations

“…Despite these conflicting results on bacterial aging, diverse studies have suggested asymmetric damage partitioning as a common mechanism of cell maintenance. Besides bacteria and yeast, the physiological asymmetry between daughter cells has been observed in diatoms 12 , nematodes 21 , stem cells 22 – 24 , and others. Thus, the identification of a deterministic divisional asymmetry in bacteria, leading to aging and rejuvenation in clonal populations, could further characterize aging at the cellular level as a ubiquitous process in living organisms.…”

Biophysical factors in the regulation of asymmetric division of stem cells

“…As the cell cycle progresses, unbalanced cortical forces shift the spindle towards a posterior location. However, other Caenorhabditis species with similar cellular shapes show anterior or posterior nuclear positions of the spindle at the onset of mitosis (Valfort et al ., ).…”