The Shifting Role of Cell Division During an Evolutionary Transition to Multicellular-Level Individuality

Abstract

During the transitions from unicellularity to multicellularity, cells transitioned from functioning as wholes to functioning as parts of wholes. In the colonial freshwater green flagellates known as volvocine algae, living "intermediate form" species give ample evidence concerning how cells gradually lost autonomy and began functioning as dedicated parts. This dissertation concerns how and why the role of cell division changed in unicellular to colonial volvocine algae. We review a recent book on levels of selection and apply a proposed three-stage transition to the example of volvocine algae. We found that, in contrast to the previous description of "stage 1", the concept of group reproduction is potentially applicable to very early-branching colonial volvocine algae. This possibility indicates that the role of cell division could have shifted (to function in group reproduction) earlier than was previously thought (Appendix A). We show that, given some reasonable assumptions, cell- and colony-level fitness are equivalent in undifferentiated colonial volvocines (Appendix B). In spite of this, our models show that cell division number could evolve in response to specifically colony-level factors. Cell division number could be regulated indirectly via allocation to growth (Appendix B) or directly via regulation of the growth-to-first division transition (Appendix C). The extent to which group factors matter in the outcome of selection on cell division number is a matter of degree and is quantifiable (Appendix B). Colony cell number could be a genuine group-level adaptation, even in the simplest volvocine algae (Appendix B and C). Because a size-dependent growth trajectory is a substantial group-level cost of higher division numbers, our analysis highlights the potential importance of understanding how colony size affects cell growth (Appendix C). We also present data on cell-type allocation in Volvox (Appendix D). The Volvox colony is clearly the level of function for cell divisions and cell fate acquisition. However, this work indicates that the precision with which Volvox development attains these colony-level goals may be low compared to more complex multicellular organisms.