Major evolutionary transitions in individuality

Abstract

The evolution of life on earth has been driven by a small number of major evolutionary transitions. These transitions have been characterized by individuals that could previously replicate independently, cooperating to form a new, more complex life form. For example, archaea and eubacteria formed eukaryotic cells, and cells formed multicellular organisms. However, not all cooperative groups are en route to major transitions. How can we explain why major evolutionary transitions have or haven't taken place on different branches of the tree of life? We break down major transitions into two steps: the formation of a cooperative group and the transformation of that group into an integrated entity. We show how these steps require cooperation, division of labor, communication, mutual dependence, and negligible within-group conflict. We find that certain ecological conditions and the ways in which groups form have played recurrent roles in driving multiple transitions. In contrast, we find that other factors have played relatively minor roles at many key points, such as within-group kin discrimination and mechanisms to actively repress competition. More generally, by identifying the small number of factors that have driven major transitions, we provide a simpler and more unified description of how life on earth has evolved.

Keywords: altruism; conflict; cooperation; division of labor; signaling.

Fig. 1.

A major evolutionary transition involves two steps: first, the formation of a cooperative group; second, the transition to a new level of organism, with division of labor, interdependence, and coordination of the parts. Although the first step is well-understood, the second is not. We follow Bourke, except that he divides transitions into three steps, distinguishing between maintenance and transformation (1).

Fig. 2.

The hypothetical level of cooperative helping in a symbiont plotted against the relatedness between the symbionts infecting a host. If the hosts sanction uncooperative symbionts, then a high level of cooperation is predicted, relatively independent of relatedness. If the hosts do not carry out sanctions, then the level of cooperation is predicted to depend strongly upon relatedness between symbionts (23).

Fig. 3.

The relationship between the proportion of resources invested into a trait (A) and the fitness return from that trait. We assume that a proportion of resources X is put intro trait A, and the remaining proportion 1 − X into trait B.

Fig. 4.

The individual and the group. The hypothetical level of a cooperative trait, such as the amount of an extracellular factor produced by bacterial cells, plotted against the extent of conflict between interacting individuals. The different lines show the optimal strategy from the perspective of an individual’s inclusive fitness (blue line) and group fitness (red line). Natural selection will lead to the evolutionarily stable strategy (ESS), which will be the strategy that maximizes inclusive fitness (i.e., the blue line), irrespective of the consequences at the group level. We would expect natural selection to lead to maximization of group fitness, and thus think of the group as a fitness-maximizing individual, only in extreme cases where there is no within-group conflict.

Fig. 5.

The way in which groups form is a major determinant of when major transitions have taken place, because it determines relatedness and the potential for within-group conflict. Within-species transitions have taken place only when offspring stay to help their parents (subsocial), and reproduction is either asexual or sexual with lifetime monogamy. Between-species transitions seem to involve similarly restrictive group formation, such as vertical transmission leading to clonal symbionts whose interests are aligned with their hosts. Different colored circles represent either genetically distinct individuals (within-species) or individuals of different species. Larger circles represent hosts with smaller circles representing their symbionts. The images, from left to right show: obligately multicellular human (image courtesy of Stu West), facultatively multicellular Chlamydomonas algae (image courtesy of Will Ratcliff), obligately eusocial Atta ants (image courtesy of Wikimedia commons/Arpingstone), facultatively eusocial Stenogastrine hover wasp (image courtesy of Wikimedia commons/David Baracchi), mitochondrion (image courtesy of Wikimedia commons/Louisa Howard), Hamiltonella defensa symbiont in black bean aphids (image courtesy of Christoph Vorburger), facultatively multicellular Dictyostelium slime mould (image courtesy of Wikimedia commons/Bruno in Columbus), cooperatively breeding superb fairy wren (image courtesy of Wikimedia commons/JJ Harrison), Legume-Rhizobia mutualism (image courtesy of Dave Whitinger, All Things Plants). Negligible conflict is not sufficient for a major transition—the algae, wasp, and symbiont examples have not made a major transition because there is not mutual dependence (see also Table 1).