BIOELECTRIC COUPLING AS THE MECHANISM OF THE TRANSITION FROM COLONY TO ORGANISM: CONVERGENCE OF SOLUTIONS AND THE LIMITS OF THE CLAIM

This paper proposes a hypothesis according to which the key factor in the transformation of a cell colony into an integrated organism was the bioelectric coupling of cells. Existing theories explain the mechanical aggregation of unicellular organisms into colonies but do not answer how a colony of autonomous cells becomes a single whole under common regulation. Relative to the previous version, two defects have been corrected. First, the mechanism has been reformulated in terms of function rather than structure. The previous version named gap junctions as the mechanism, yet connexins arose de novo in early chordate evolution; other animals use innexins, plants plasmodesmata, fungi septal pores, and these structures are not homologous. The argument from the repeated independent origin of multicellularity thereby lost its force, since the named structure appeared hundreds of millions of years after multicellularity had arisen in plants, fungi and most animals. In the present version what is held to be common is not the structure but the function — direct electrical and cytoplasmic continuity between neighbouring cells. The convergent emergence of four structurally unrelated solutions to one problem is advanced as independent evidence of its necessity, stronger than the previous appeal to the convergence of multicellularity itself. Second, the case of experimentally evolved multicellularity in yeast is examined: sixty days of selection produced reproduction by multicellular propagules, a juvenile phase, apoptosis and division of labour — without any electrical coupling. The previous formulation was refuted by this. The claim is narrowed: coupling is held to be necessary not for multicellularity as such, but for organismal integration with coordinated morphogenesis, in which the position and fate of a cell are determined by the state of the system as a whole. The yeast clusters thereby become not a counterexample but a control case — a system that has the one without the other. A limitation is named separately: the notion of coordinated morphogenesis is stated qualitatively and has not been operationalized.