The group covariance effect and fitness trade-offs during evolutionary transitions in individuality

Abstract

Transforming our understanding of life is the realization that evolution occurs not only among individuals within populations but also through the integration of groups of preexisting individuals into a new higher-level individual, that is, through evolutionary transitions in individuality. During evolutionary transitions (such as during the origin of gene networks, bacteria-like cells, eukaryotic cells, multicellular organisms, and societies), fitness must be reorganized; specifically, it must be transferred from the lower-to the higher-level units and partitioned among the lowerlevel units that specialize in the fitness components of the new higher-level individual. This paper studies the role of fitness trade-offs in fitness reorganization, the evolution of cooperation, and the conversion of a group into a new individual during the origin of multicellular life. Specifically, this study shows that the fitness of the group is augmented over the average fitness of its members according to a covariance effect. This covariance effect appears to be one of the first emergent properties of the group and a general aspect of groups with multiplicative properties that are themselves averages of properties of lower-level units. The covariance effect allows groups to break through the constraints that govern their members, and this effect likely applies to group dynamics in other fields.T ransforming our understanding of life is the realization that evolution occurs not only among individuals within populations but also through the integration of groups of preexisting individuals into a new higher-level individual, that is, through evolutionary transitions in individuality (1-5). These evolutionary individuals constitute the familiar hierarchy of life: gene networks, bacteria-like cells, eukaryotic cells, multicellular organisms, and certain societies of organisms such as social insects. How does a group become an individual? This is the central question motivating this study. The premier example of the process of individuation of groups is the evolution of multicellular individuals from unicellular and colonial ancestors. The hypothesis explored here is that specialization of reproductive and vegetative viability-enhancing functions, termed germ-soma specialization, is a major factor in the conversion of cell groups into true multicellular individuals. Once cells specialize in fitness components, they cannot survive and reproduce on their own, and the group becomes indivisible and, hence, an individual.The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). As embodied in current theory, trade-offs between these fitness components drive the evolution of diverse life-history traits in extant organisms (6, 7). Fitness trade-offs gain special significance during the transition from unicellular to multicellular life for several related reasons: (i) fitness trade-offs often create a covariance effect at the group level so that group fitnes...

Lifetime monogamy and the evolution of eusociality

“…R. Soc. B (2009) reproduction (Michod 2005(Michod , 2006. This process, which is reminiscent of the synergistic benefits of increasing colony size in insect societies (Bourke 1999; see also figure 1) results in a significant increase in the heritability of fitness at the collective level (Michod & Roze 1997) and is connected to the emergence of a totipotent germ line and a majority of cells that have been terminally determined to serve somatic functions.…”

Behavioral Responses in Structured Populations Pave the Way to Group Optimality

“…We then apply our framework to the problem of when natural selection can lead to maximization of fitness at the group level, or group optimality. Our focus on group optimality is motivated in part by the fact that group optimality is intimately related to evolutionary transitions in individuality (ETIs), that is, groups becoming new, higher-level individuals (Maynard Smith and Szathmáry 1995;Michod 2005Michod , 2006. We show that behavioral responses significantly increase the conditions under which group optimality is evolutionarily stable.…”

Evolution of Individuality: A Case Study in the Volvocine Green Algae

“…Due to the ubiquity and importance of germ-soma division of labor (Simpson 2012), some multicellular groups without this trait have been considered to lack individuality (Godfrey-Smith 2009). Reproductive division of labor simultaneously increases group-level fitness and decouples the group-level fitness from the average of lower-level fitnesses (Michod 2006;Michod et al 2006;Hanschen et al 2015). While the evolution of division of labor is an especially clear example of how fitness decoupling may occur, it is not the only means.…”

“…Another criterion is reproductive division of labor (Weismann 1885;Buss 1987), in which lowerlevel units specialize on the basic fitness components of the group (Maynard Smith and Szathmáry 1995;Michod 2005Michod , 2006Michod , 2007. Reproductive division of labor promotes cooperation and inhibits conflict amongst lower-level entities.…”