Life history tradeoffs, division of labor and evolutionary transitions in individuality

Abstract

Reproductive division of labor has been proposed to play a key role for evolutionary transitions in individuality (ETIs). This chapter provides a guide to a theoretical model that addresses the role of a tradeoff between life-history traits in selecting for a reproductive division of labor during the transition from unicellular to multicellular organisms. In particular, it focuses on the five keys assumptions of the model, namely (1) fitness is viability times fecundity; (2) collective traits are linear functions of their cellular counterparts; (3) there is a tradeoff between cell viability and fecundity; (4) cell contribution to the collective is optimal; and (5) there is an initial reproductive cost in large collectives. Thereafter the chapter contrasts two interpretations of the model in the context of ETIs. Originally, the model was interpreted as showing that during the transition to multicellularity the fitness of the lower-level (the cells) is 'transferred' to the higher level (the collective). Despite its apparent intuitiveness, fitness transfer may obscure actual mechanisms in metaphorical language. Thus, an alternative and more conservative interpretation of the model that focuses on cell traits and the evolutionary constraints that links them is advocated. In addition, it allows for pursuing subsequent questions, such as the evolution of development.

Individuality through ecology: Rethinking the evolution of complex life from an externalist perspective

“…Grappling with the latter and recognizing that natural selection at the lower level cannot be invoked to explain the emergence of Darwinian properties at the higher level-doing so would assume that which requires explanation as the cause of its own evolution-led to development of the "ecological scaffolding" framework, which emphasizes the role of external factors in major evolutionary transitions (Figure 1 A E to D E ). This conceptual framework, which has both experimental [19][20][21] and theoretical [2,4,22] support, emphasizes that higher-level Darwinian properties can be exogenously imposed by specific ecological conditions.…”

“…They do so by developing properties that make the ecological scaffold unnecessary for their maintenance. In the case of the evolution of multicellularity, the evolution of an extracellular matrix maintaining the cells together in the absence of a scaffold represents an example of endogenization (see [2][3][4]).…”

“…Once it reaches a peak, the population is at evolutionary equilibrium. In many cases, the relationship between phenotypic variation and long-term reproductive output involves a landscape with more than one peak (of differing heights), prompting questions about crossing fitness valleys from one local peak to the other (see [4] and Figure 2, for uses of the metaphor).Fitness transfer: a proposed mechanism for the evolution of a new level of individuality. In the case of the evolution of multicellularity, cells can be considered as transferring their fitness to the multicellular entities that progressively gain individuality (see [7]).…”

“…Once it reaches a peak, the population is at evolutionary equilibrium. In many cases, the relationship between phenotypic variation and long-term reproductive output involves a landscape with more than one peak (of differing heights), prompting questions about crossing fitness valleys from one local peak to the other (see [4] and Figure 2, for uses of the metaphor).…”

The Effect of Bottleneck Size on Evolution in Nested Darwinian Populations

“…This tradeoff between improving patch (group) fitness and decreasing cell growth rate has been interpreted through the lens of fitness decoupling (Michod and Roze, 1999;Michod and Nedelcu, 2003;Okasha, 2005Okasha, , 2008Rainey and De Monte, 2014;Hammerschmidt et al, 2014), alluding to the fact that after an ETI, the fitness of the higher level construct (the patch) is no longer a simple function of the fitness of the individual components (the cells). However, the underlying assumptions of the notion of fitness decoupling and related terms such as "fitness transfer" or "export of fitness" have been called into question (Doulcier et al, 2022). In particular, it has been shown that properly measured, that is, measured over the same set of events, the fitness of cells and patches are always equal (Shelton and Michod, 2014;Bourrat, 2015b,a;Black et al, 2020).…”