Levels of selection in biofilms: Ellen Clarke on individuality

Pseudomonas biofilm. From Spiers et al. 2013.

Pseudomonas biofilm. From Spiers et al. 2013.

The question of what constitutes a biological individual is intimately entangled with questions about levels of selection. Many authors implicitly or explicitly treat individuals as units of evolution or some variation on this theme. A recent appreciation for the complexity of bacterial biofilms has led to comparisons with multicellular organisms. A recent paper by Ellen Clarke bucks this trend by claiming that multispecies biofilms are not evolutionary individuals.

The recent paper starts off by describing biofilms and specifying that the central claim (that they are not evolutionary individuals) applies only to multispecies biofilms. Clarke spends some time describing some of the complex features of biofilms; I don’t think she can fairly be accused of failing to appreciate this point:

Biofilms are not homogeneous lumps of slime, but delicate and spatially heterogeneous structures with complex and variable three dimensional architectures that are occasionally visible to the naked eye. They are organised according to oxygen and nutrient gradients into different regions which specialise for diverse tasks. Biofilm microbes use intercellular signals to coordinate colony behaviours and regulate gene expression…Lateral transfer provides an extra route by which traits can be passed between cells, in addition to the normal vertical process of inheritance from a parent cell. [references removed]

She also emphasizes the potential advantages of living in a biofilm:

Biofilm life enables microbes to live in conditions where they cannot survive alone. It provides defence against predators, against host immune defences and unpredictable environmental changes. It allows access to resources that individual cells cannot effectively obtain on their own, via metabolic divisions of labour. [references removed]

Clarke has long advocated the individuals as units of selection view*, specifically that individuals are those units that possess Lewontin’s conditions for evolution by natural selection:

1. Different individuals in a population have different morphologies, physiologies, and behaviors (phenotypic variation).
2. Different phenotypes have different rates of survival and reproduction in different environments (differential fitness).
3. There is a correlation between parents and offspring in the contribution of each to future generations (fitness is heritable).

So for Clarke, the central question is

Are biofilms selected mostly as wholes? Or are biofilm parts mostly selected independently of one another?

She considers several arguments in favor of treating biofilms as individuals: that they exhibit heritability, that they possess adaptations, and that their members engage in fitness-affecting interactions. To have heritability in Lewontin’s sense, biofilms “…need to form lineages in which fitness-affecting novelties get transmitted from parents to offspring,” and she concludes that there is no good evidence that they do. While she admits that biofilms often have features that look like adaptations, “Things can appear designed when they are not”; in other words, these features may have arisen non-adaptively or as a byproduct of cell-level adaptation. Fitness affecting interactions, she says, mostly “…take place across spatial scales that are much smaller than an entire biofilm,” making group structure poorly defined and preventing group selection.

Mainly due to the first objection, lack of heritability, she concludes that

…there is little utility in treating wild biofilms as if they can function as evolutionary individuals. In other words, I doubt that wild biofilms generally evolve by group selection, where whole biofilms are taken as groups.

But her view is actually a bit more nuanced than that:

…I am not convinced that multispecies biofilms do meet Lewontin’s conditions—or at least, not much. Evolutionary individuality is continuous—living objects can manifest more or less of the properties that are essential to the evolutionary process.

This is key, and it’s something that most recent treatments agree on: individuality is too complicated to treat as a dichotomy. From a Major Transitions perspective, this is bound to be true: if higher (more inclusive) units in the hierarchy of life evolved from lower ones without huge saltations, they must have passed through stages with intermediate degrees of individuality. This doesn’t mean that the individual is not a useful concept any more than gradual speciation invalidates species. And lots of taxa appear to have been in these ‘intermediate’ states for an awfully long time, blissfully unaware of the problems they cause philosophers of biology.

*More recently, she has suggested that individuals be recognized by the possession of “individuating mechanisms” — traits that increase the capacity for among-unit selection or decrease the capacity for within-unit selection (see “Pathways to pluralism: Beckett Sterner on biological individuality, part 1“). But this refinement is absent from her most recent paper. Whether this is because of a change of heart or just an artifact of a very long review process I don’t know.


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