Expansion and the hierarchical structure of levels of selection

Evolutionary success comes to the selfish—or so most biologists are taught. Those organisms that reproduce most will of course be better represented in future generations. Current theory has had great success using this fact to understand much of evolution, but it hits a wall when it comes to understanding how primitively solitary organisms can aggregate together to form new wholes. Current theory predicts that the evolution of new wholes is undermined by the selfishness of the parts; if the parts keep reproducing an emergent whole can’t originate. Yet every animal is a living contradiction of current theory. During development animal cells divide in the same way their solitary ancestors reproduced, while concurrently the whole animal reproduces itself.

It’s not that our theories are wrong; it is just that what we traditionally call evolutionary success is overly myopic. In the formulation I am developing, one that is explicitly hierarchical in structure, I consider three general ways for frequencies of units to increase over time and so be considered successful: (1) Differential persistence of units. (2) Differential multiplication of units. (3) Differential expansion of units. Any combination of these can occur. Only the first two aspects of selection are incorporated into current theory. Expansive fitness looks, from the higher level, like growth. But from the lower level, it appears as the differential multiplication of parts. For example, a coral colony grows when its constituent zooids increase in number. Once one adopts a hierarchical framework, one can incorporate the notion of expansive fitness, a key concept that has been missing. Expansion allows us to translate units of fitness at one level into units at another. Population growth at one level is expansion at the next level up. You can see expansion in action during animal development: through cell division, the animal grows. The important role of differential expansion in evolution has barely been recognized even though it may be the most common mode of multilevel selection.

The practical and conceptual consequences of incorporating expansion into our theories of natural selection promises to be profound. The immediate payoff of is the ability to understand how selection can act and interact simultaneously at different levels; something that is not accommodated by standard theory, where lower levels of selection must directly oppose or be turned off for higher levels to be effective. What we still don’t understand, and what I will focus on in my theoretical and empirical research, is the effect of interacting levels of selection on the origin and evolution of adaptations.

Adaptations are always the products of natural selection, but they are thought to most often arise when selection is dominated by differential multiplication. However, when selection occurs at multiple levels, oftentimes parts and wholes both multiply independently and the selective cause of adaptations can be murky. Is it possible to decompose the evolution of an adaptation into the separate contributions from multiple levels of selection? It is, but it requires an understanding of how the various parts in the whole interact with each other and how they are structured developmentally. Given that knowledge, the correlation between parts and the multiplication component of fitness at multiple levels can be made precise. New theoretical work is needed to understand this problem.

One promising empirical application of my work is the examination of the origin and early evolution of development during transitions in individuality, where primitively solitary organisms aggregate into new wholes. How can development evolve from previously independent parts? Are there any processes of development that increase the efficacy of multilevel selection? I am interested in testing predictions about how development evolves between and among metazoans that have varying degrees of clonal growth (thus varying degrees of the expansive component of fitness). For example, we could predict systematic differences in developmental processes between animals with either a significant component of expansive fitness or in animals where expansion is absent. These predictions would allow us to identify the types of innovations in developmental processes needed for the origin of the bilaterian animal phyla (in which expansion plays a minor role) during the Cambrian explosion.

At the macroevolutionary scale, theoretical work on multilevel adaptations allows me to ask a previously taboo question in a precise and falsifiable way: can adaptations occur at the community level? Here I am interested in testing the new theory on empirical data, focusing on the evolution of one of the oceans most important biomes, reefs. Thus, for example, by identifying the patterns of differential expansion, origination and extinction across levels I can determine at what levels natural selection acts in and among reef communities. In reef communities, there are three putative levels: expansion and collapse of reef communities at the highest level, origination and extinction of reef genera at an intermediate level, and the expansion of reef genera are at the lowest level. When reefs are globally widespread they are observed to be more similar to each other. Is this pattern the byproduct of organismal selection or a result of selection acting on communities directly? Setting up the problem using multilevel selection theory with expansion will allow me to estimate the contribution (if any) of selection at each level in patterning reef evolution and assess the potential for community-level adaptation.

An additional empirical application is in human cultural evolution, where changes in cultural traits are potentially controlled by organismal-level selection, selection at the level of human groups, or they can be non-adaptive. It is possible to identify the level and strength (including no selection) by the covariance of traits with demographic processes at both the organismal and group levels.