Pierrick Bourrat’s new paper in Philosophy and Theory in Biology criticizes aspects of the influential ‘export of fitness’ framework developed by Rick Michod and colleagues and extended by Samir Okasha (Bourrat, P. 2015. Levels, time and fitness in evolutionary transitions in individuality. Philos. Theory Biol., 7: e601. doi: 10.3998/ptb.6959004.0007.001). According to this view, an evolutionary transition in individuality, for example from unicellular to multicellular life, involves a transfer of fitness from the lower level units (e.g. cells) to the higher level unit (e.g. nascent multicellular organism). Fitness is defined as the product of viability and fecundity, and the emergence of a division of labor between reproductive (germ) and non-reproductive (somatic) units at the lower level exports fitness to the higher level. Full disclosure: Rick Michod was my Ph.D. co-advisor, and he has had a huge influence on my thinking about this topic.
For the sake of readability, I’ll refer to cells and (multicellular) organisms, though the principles are generally agreed to be similar for (at least) the fraternal transitions in individuality. It just gets a bit cumbersome to keep referring to ‘lower-level units,’ ‘higher-level units,’ and ‘propagules.’
Michod’s framework is largely focused for the potential for conflict among cells and the need to prevent or mediate these conflicts, a need that is generally met by a unicellular bottleneck in Michod’s models. Conflict mediation, though, is not sufficient for the emergence of a higher-level individual; a division of labor between germ and soma is also required. Up to this point, Bourrat seems to have no problem with Michod’s framework. However, Michod claims that germ-soma differentiation results in cells with zero fitness, and this is where Bourrat disagrees:
Michod and colleagues’ model relies on an assumption regarding fitness of the higher-level entity (hereafter the “collective”) that is inconsistent with the claim made about the fitnesses of the lower level entities (hereafter the “particles”). I claim that an ambiguity surrounding the concept of viability (fertility) of the particle/ viability (fertility) of the collective exists in Michod’s and Okasha’s writings and creates the illusion that the fitness of the particle can be nil while the fitness of the collective is high.
The crux of Michod’s claim that specialized cells have zero fitness is that germ cells invest all of their effort into reproduction, resulting in zero viability, and somatic cells invest all of their effort into viability, resulting in zero reproduction. Since zero times anything is zero, the product of viability and reproduction for either cell type is zero. Bourrat objects that Michod is conflating viability and fecundity of cells with viability and fecundity of the multicellular organism:
…the terms ‘viability’ and ‘fertility’ at the collective level do not respectively equate to the terms ‘viability’ and ‘fertility’ at the particle level. In fact, during the phase of development of the multicellular organism – that is, when only the somatic or viability function of the organism is performed – the somatic line has offspring, and to do so the somatic cells need both to survive and reproduce. Similarly, during the phase of reproduction of the multicellular organism the germ cells both survive and reproduce…the viability and fertility of the multicellular organism result from the effort of the cells in those variables. Yet, if the invested effort of a particular line of cells in the viability (fertility) of the multicellular organism is nil, it does not follow that the viability (fertility) of the cell is nil.
This is mostly true, although in Volvox at least, the somatic cells born of the final round of cell division do not have any offspring. I agree with Bourrat that Michod’s claim that differentiated cells have zero fitness is either metaphorical or mistaken, but for different reasons. It is trivially easy to show that germ cells do not have zero fitness: they (usually) have offspring. Even for soma, Michod’s conclusions rely on a particular definition of fitness; the somatic cells resulting from the final round of cell division have zero offspring and zero direct fitness, but if the germ cells, with a relatedness of r = 1 to the somatic cells, reproduce, the inclusive fitness of the somatic cells is nonzero. Michod’s model confounds EFFORT invested in the components of fitness with the components themselves, especially when components are realized in the context of the multicellular group. It is reasonable to assume that viability and fecundity are functions of the effort invested in each, but it is not reasonable to assume that the components are equal to the effort. Furthermore, all cells invest in their own viability; as Bourrat points out, a germ cell with zero viability is useless. I’m not sure if Michod’s view on this has changed; in his 2011 book chapter, he refers to ‘low cell fitness’ rather than ‘zero cell fitness’ (p. 181).
Bourrat takes an entirely different approach to the question of somatic cell fitness. Rather than arguing on the grounds of inclusive fitness, he argues that the claim that somatic cells do not reproduce (and thus have zero fitness) fails when reproduction does not require material overlap (‘formal reproduction,’ in Peter Godfrey-Smith’s terms):
For formal reproduction to happen, relatively to a particular grain of description, the only requirement is the presence of a causal link between the presence/absence of a somatic cell in the parental organism and the overall number of cells produced (number and quality of offspring).
Here I think that Bourrat (and, to be fair, the inclusive fitness account) has missed an important point of Michod’s models. In one important sense, the somatic cells (but not the germ cells) do have zero fitness: they are evolutionary dead ends in that novel mutations that occur in somatic cell lineages will never be passed on to future organismal generations (unless they cause the somatic cells to produce offspring, in which case they are, by definition, no longer somatic cells). The claims about formal reproduction may be right, at least for some concepts of fitness, but Bourrat’s example shows that fitness concepts based on formal reproduction fail what I consider the most important function of fitness: to predict, at least probabilistically, the short-term outcome of selection.
None of this means that Michod’s models are not useful. To be sure, the claim that germ-soma specialized cells have zero fitness is either wrong or metaphorical (Godfrey-Smith makes a similar point). But we need not throw out the baby with the bathwater; the ‘export of fitness’ framework is still (IMO) a useful heuristic for thinking about evolutionary transitions in individuality. The division of labor between reproduction and viability can be usefully conceptualized as cells increasing their effort at one component of fitness at the expense of the other, resulting in cell groups that require both cell types to survive and reproduce. Whether or not such specialization creates a disconnect between cell-level fitness and organism-level fitness is the subject of the remainder of Bourrat’s paper, and one that I will address in a future post.