Why did eukaryotes evolve only once? Genetic and energetic aspects of conflict and conflict mediation

Abstract

According to multi-level theory, evolutionary transitions require mediating conflicts between lower-level units in favour of the higher-level unit. By this view, the origin of eukaryotes and the origin of multicellularity would seem largely equivalent. Yet, eukaryotes evolved only once in the history of life, whereas multicellular eukaryotes have evolved many times. Examining conflicts between evolutionary units and mechanisms that mediate these conflicts can illuminate these differences. Energy-converting endosymbionts that allow eukaryotes to transcend surface-to-volume constraints also can allocate energy into their own selfish replication. This principal conflict in the origin of eukaryotes can be mediated by genetic or energetic mechanisms. Genome transfer diminishes the heritable variation of the symbiont, but requires the de novo evolution of the protein-import apparatus and was opposed by selection for selfish symbionts. By contrast, metabolic signalling is a shared primitive feature of all cells. Redox state of the cytosol is an emergent feature that cannot be subverted by an individual symbiont. Hypothetical scenarios illustrate how metabolic regulation may have mediated the conflicts inherent at different stages in the origin of eukaryotes. Aspects of metabolic regulation may have subsequently been coopted from within-cell to between-cell pathways, allowing multicellularity to emerge repeatedly.

Keywords: endosymbiosis; genome transfer; levels of selection; major transitions; mitochondria; redox signalling.

Figure 1.

Levels-of-selection analyses usually focus on particles nested within a collective (a), for example, individuals within a society, or cells within an organism. In the case of proto-mitochondria within a proto-eukaryote, much of the collective is not contained within the particles, as emphasized in (b) with the cytosol shaded. The cytosol can be viewed as an emergent feature of the collective. The host genome appears as the unique particle.

Figure 2.

Evolutionary history of mitochondria. If the character states of all modern mitochondria were known, then features of the last common ancestor could be accurately reconstructed. Nevertheless, the last common ancestor may be very distinct from the first proto-mitochondrion (i.e. extensive evolution occurred in the mitochondrial stem group). Modern out-groups are also highly derived.

Figure 3.

Stoichiometric mediation of conflict. In the initial endosymbiosis (a), the proto-eukaryote takes up substrate and uses an unspecified molecule, X, as a terminal electron acceptor. The proto-mitochondrion takes up the reduced form of this electron carrier, XH, and oxidizes it, excreting X. Both partners obtain energy in this fashion. The proto-mitochondrion replicates and the host increases in size (b), eventually dividing (c). This simple life cycle continues with conflicts mediated by stoichiometry.

Figure 4.

Regulation of energetically selfish proto-mitochondria by metabolic demand and stochastic processes. If the proto-eukaryote exerts strong metabolic demand because of rapid growth and replication (a), then normal proto-mitochondria (unfilled circles) will perceive a high ADP/ATP ratio and their rates of growth and division will match those of variant proto-mitochondria (filled circles). If metabolic demand of the proto-eukaryote falters and it undergoes whole-cell fusion and whole-genome recombination (b), stochastic processes may still produce a daughter cell with all normal proto-mitochondria.