The Major Transitions in Evolution Revisited

8. Conflicts among Levels of Selection as Fuel for the Evolution of Individuality

8Conflicts among Levels of Selection as fuel for the Evolution of Individuality Paul B. Rainey and Benjamin Kerr A fundamental feature of contemporary biological life is its hierarchical organization. Consider just one colony of leaf-cutting ants in a South American forest. This colony is composed of multiple individual ants, differentiated for different tasks. However, each ant is also composed of a set of differentiated cells.And each cell houses a diverse array of genes. Although multiple layers of nested organization characterize many living systems, these hierarchical structures were presumably reduced or absent in our most ancient ancestors. How then do biological hierarchies come to be? This question motivates a consideration of the “major transitions in evolution,” which describe the shift from autonomous lower-level entities to differentiated and integrated higher-level entities (Maynard Smith and Szathmáry 1995). At their core, many major transitions involve a hierarchical shift in individuality. Specifically, each transition is characterized by the emergence of individuality at a new level of organization. This occurs as a consequence of subjugation and coordination of lower-level units (Michod 1999). Evolutionary transitions have been variously categorized (Buss 1987; Jablonka and Lamb 2006; Maynard Smith and Szathmáry 1995). An informative distinction concerns the nature of the alliance among the lower-level entities (Queller 2000). The so-named egalitarian transitions are characterized by a fairness in reproduction and mutual dependence: the coming together of disparate entities in a symbiotic association for the benefit of both partners. Examples include the transition from independently replicating nucleic acids to chromosomes, and the transition from prokaryotes to eukaryotes, in which—upon completion—the mitochondrion (once a free-living prokaryote) replicates as part of the host cell. Unlike the egalitarian transitions, the fraternal transitions, such as the transition from single cells to multicellularity, and from multicellular organisms to societies (e.g., eusociality in certain insects), originate with an alliance of entities that at the outset were most likely identical (or highly similar) and where a division of labor arose through epigenesis—a common developmental program expressed differently in different units. Explaining the fraternal transitions poses special challenges because of the need to explain the evolution of the ultimate in self-sacrificial behavior, namely, reproductive altruism: the evolution of entities, such as soma (in a multicellular individual) and sterile workers (in a 142 Paul B. Rainey and Benjamin Kerr eusocial insect colony), that forgo reproduction and serve solely to enhance fitness of the germline. While genetic relatedness (Hamilton 1964a, b) is without doubt a central feature of fraternal transitions (Okasha 2006; Queller 2000)—and conditional sterility a necessary factor (Charlesworth 1980)—the nature of the selective events and mechanistic details underpinning the fraternal transitions remain unclear. Multicellularity In this chapter we focus on the evolutionary transition from single cells to multicellular individuals—a transition that has been important for many taxa. The panoply of plant and animal forms owes a great deal to the multicellular foundations of these groups (Conway Morris 1998). From a genetically diverse range of starting positions, independent unicellular lineages have made the transition to multicellularity (Bonner 2000). The most ancient transitions occurred in the major lineages of large multicellular eukaryotes approximately one billion years ago (Wray 2001). However, multicellularity has also arisen in the ciliates, slime molds, diatoms, certain groups of prokaryotes, and, most recently, the volvocine algae (Bonner 1998; Herron and Michod 2008; Kirk 1998). Although certain benefits of multicellularity seem clear, such as the division of labor, the evolutionary causes and mechanistic details underlying this transition remain unknown. Multicellularity also illustrates the fundamental tension inherent in any major transition, which involves the potential for dissonant interests of entities at different levels in the hierarchy . Although evolutionary transitions involve the exchange of some lower-level autonomy for higher-level functionality, entities at the lower level are not left entirely bereft of individuality (Buss 1987; Michod 1999). From the perspective of multilevel selection theory, natural selection may act simultaneously at different levels within the hierarchy (e.g., genes, cells, multicellular organisms, groups), and selection at one level may oppose selection at another level (Buss 1987; Sober and Wilson 1998). Certain kinds of cancers in vertebrates provide a case in point: Cancer is clearly maladaptive at the level of the organism ; nonetheless, natural selection favors individual cells that become cancerous despite the negative consequences for the higher unit of selection (Frank 2007). With respect to major transitions, this conflict between levels is generally seen as a hurdle to be overcome. However, our...