Cooperation and conflict in the evolution of individuality. IV. Conflict mediation and evolvability in Volvox carteri.

The continued well being of evolutionary individuals (units of selection and evolution) depends upon their evolvability, that is their capacity to generate and evolve adaptations at their level of organization, as well as their longer term capacity for diversifying into more complex evolutionary forms. During a transition from a lower- to higher-level individual, such as the transition between unicellular and multicellular organisms, the evolvability of the lower-level (cells) must be restricted, while the evolvability of the new higher-level unit (multicellular organism) must be enhanced. For these reasons, understanding the factors leading to an evolutionary transition should help us to understand the factors underlying the emergence of evolvability of a new evolutionary unit. Cooperation among lower-level units is fundamental to the origin of new functions in the higher-level unit. Cooperation can produce a new more complex evolutionary unit, with the requisite properties of heritable fitness variations, because cooperation trades fitness from a lower-level (the costs of cooperation) to the higher-level (the benefits for the group). For this reason, the evolution of cooperative interactions helps us to understand the origin of new and higher-levels of fitness and organization. As cooperation creates a new level of fitness, it also creates the opportunity for conflict between levels of selection, as deleterious mutants with differing effects at the two levels arise and spread. This conflict can interfere with the evolvability of the higher-level unit, since the lower and higher-levels of selection will often "disagree" on what adaptations are most beneficial to their respective interests. Mediation of this conflict is essential to the emergence of the new evolutionary unit and to its continued evolvability. As an example, we consider the transition from unicellular to multicellular organisms and study the evolution of an early-sequestered germ-line in terms of its role in mediating conflict between the two levels of selection, the cell and the cell group. We apply our theoretical framework to the evolution of germ/soma differentiation in the green algal group Volvocales. In the most complex member of the group, Volvox carteri, the potential conflicts among lower-level cells as to the "right" to reproduce the higher-level individual (i.e. the colony) have been mediated by restricting immortality and totipotency to the germ-line. However, this mediation, and the evolution of an early segregated germ-line, was achieved by suppressing mitotic and differentiation capabilities in all post-embryonic cells. By handicapping the soma in this way, individuality is ensured, but the solution has affected the long-term evolvability of this lineage. We think that although conflict mediation is pivotal to the emergence of individuality at the higher-level, the way in which the mediation is achieved can greatly affect the longer-term evolvability of the lineage.