The basic problem in an evolutionary transition is to understand how a group of individuals becomes a new kind of individual, possessing the property of heritable variation in fitness at the new level of organization. During an evolutionary transition, for example, from single cells to multicellular organisms, the new higher-level evolutionary unit (multicellular organism) gains its emergent properties by virtue of the interactions among lower-level units (cells). We see the formation of cooperative interactions among lower-level units as a necessary step in evolutionary transitions; only cooperation transfers fitness from lower levels (costs to group members) to higher levels (benefits to the group). As cooperation creates new levels of fitness, it creates the opportunity for conflict between levels as deleterious mutants arise and spread within the group. Fundamental to the emergence of a new higher-level unit is the mediation of conflict among lower-level units in favor of the higher-level unit. The acquisition of heritable variation in fitness at the new level, via conflict mediation, requires the reorganization of the basic components of fitness (survival and reproduction) and life-properties (such as immortality and totipotency) as well as the co-option of lower-level processes for new functions at the higher level. The way in which the conflicts associated with the transition in individuality have been mediated, and fitness and general life-traits have been re-organized, can influence the potential for further evolution (i.e., evolvability) of the newly emerged evolutionary individual. We use the volvocalean green algal group as a model-system to understand evolutionary transitions in individuality and to apply and test the theoretical principles presented above. Lastly, we discuss how the different notions of individuality stem from the basic properties of fitness in a multilevel selection context.

Organisms are constantly subjected to factors that can alter the cellular redox balance and result in the formation of a series of highly reactive molecules known as reactive oxygen species (ROS). As ROS can be damaging to biological structures, cells evolved a series of mechanisms (e.g. cell-cycle arrest, programmed cell death) to respond to high levels of ROS (i.e. oxidative stress). Recently, we presented evidence that in a facultatively sexual lineage--the multicellular green alga Volvox carteri--sex is an additional response to increased levels of stress, and probably ROS and DNA damage. Here we show that, in V. carteri, (i) sex is triggered by an approximately twofold increase in the level of cellular ROS (induced either by the natural sex-inducing stress, namely heat, or by blocking the mitochondrial electron transport chain with antimycin A), and (ii) ROS are responsible for the activation of sex genes. As most types of stress result in the overproduction of ROS, we believe that our findings will prove to extend to other facultatively sexual lineages, which could be indicative of the ancestral role of sex as an adaptive response to stress and ROS-induced DNA damage.

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SUMMARYThe evolution of multicellular organisms is the premier example of the integration of lower levels into a single, higher-level individual. Explaining the evolutionary transition from single cells to multicellular organisms is a major challenge for evolutionary theory. We provide an explicit two locus genetic framework for understanding this transition in terms of the increase of cooperation among cells and the regulation of conflict within the emerging organism. Heritability of fitness and individuality at the new level emerge as a result of the evolution of organismal functions that restrict the opportunity for conflict within and ensure cooperation among cells. Conflict leads, through the evolution of adaptations that reduce it, to greater individuality and harmony for the organism.

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