Internal conflicts and the measurement of evolutionary individuality

In biology, individuals can be identified at various levels of organization, ranging from the molecular and cellular—e.g., viruses and protists—to the organismal and societal—e.g., termites and termite colonies. This nested biological hierarchy results from evolutionary transitions in individuality, in which lower-lying entities (particles) come together to form higher-level entities (collectives). These collectives are then taken to be individuals in their own right, capable of being the units on which selection acts and where adaptations may reside. Challenges arise, however, when we recognize the possibility for internal conflict, for example from selfish genetic elements within organisms. Here we develop a quantitative approach to biological individuality, in which collectives qualify as individuals to the extent that their particles possess a unity of purpose—i.e., that they possess aligned fitness interests. We propose a mathematical framework that measures the degree of individuality exhibited by organisms and other biological collectives in the presence of internal conflicts. This framework not only helps pinpoint where in the hierarchy biological individuality sits, but also identifies the level at which adaptation may reside. We develop two metrics: fitness unity, which measures the threat posed by internal conflicts to a collective individual’s status as an optimizing agent; and trait unity, which measures differences in optimal strategies among its particles. Finally, we consider cases where internal conflicts become so disruptive to individualized biological collectives so that it no longer makes sense to think of them as individuals, but instead as compromises of multiple competing particles.