Levels of selection in biofilms: multispecies biofilms are not evolutionary individuals

Abstract

Microbes are generally thought of as unicellular organisms, but we know that many microbes live as parts of biofilms—complex, surface-attached microbial communities numbering millions of cells. Some authors have recently argued in favour of reconceiving biofilms as biological entities in their own right. In particular, some have claimed that multispecies biofilms are evolutionary individuals (Doolittle in Biol Philos 28:351–378, 2013; Ereshefsky and Pedroso in PNAS USA 112(33): 10126–10132 2015). Against this view, I defend the conservative consensus that selection acts primarily upon microbial cells.

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Notes

  1. 1.

    A complication here lies in distinguishing programmed cell death from accidental death caused by competition for resources. Ratcliff et al. argue that they saw the evolution of multicellular yeast floccules on the grounds that they exhibit sterile cells which apoptose in order to enhance the fitness of the group (Ratcliff et al 2012). But a different interpretation is that the cells in question merely starve to death as the surrounding cells obscure their access to scarce resources.

  2. 2.

    Claessen et al are content to judge that some bacteria have lost the ability to survive and divide in a unicellular, planktonic state (Claessen et al 2014). Some authors write that a species will only be considered multicellular if its life cycle includes a multicellular stage necessarily (Fisher et al 2013). A problem with this view is that it makes a presupposition about what counts as a life cycle. From the point of view of view of a cell, the life cycle is complete once the cell has divided. If you argue that cells in a filament dont complete division, then you are assuming that physical attachment is enough to make two cells into one life. Although Anabaena always form chains, any cell separated from a chain will still divide. We can simplify matters if we rule that spore formation, but not cell fission, qualifies as completion of the life cycle. But this only makes it obvious that some circularity lies in defining multicellularity according to a life cycle.

  3. 3.

    Although these papers were based on research carried out only on single-species biofilms, others make use of analogous ‘life cycle stages’ in multispecies settings (Singer et al 2010; Rendueles and Ghigo 2012).

  4. 4.

    A different use of the term ‘individual’ occurs when bacterial cells are claimed to be individuals - as in phenotypically different from one another (Davidson & Surette 2008; Ackermann 2013).

  5. 5.

    Cells, especially, cancerous cells, may occasionally attempt to proliferate at the expense of the rest. But they lack any means for passing their traits on to future generations—there is no heritability.

  6. 6.

    It might be noted that analogous processes of shuffling during sexual reproduction are not thought to prevent the traits of sexual organisms from being heritable, even though we know that epistasis is significant. However, if those same epistatic effects were occurring between genes in organisms that had an unlimited number of parents, with no mechanisms for controlling which genes could pair with which and no mechanisms of developmental canalisation, then we might think again.

  7. 7.

    With many thanks to Kim Sterelny for this point.

  8. 8.

    This is not a problem that is specific to the biofilm case: adaptive hypotheses are generally flimsy constructions on which to rest arguments, although the problems are certainly exacerbated in contexts where there is potentially more than one hierarchical level of selection in play (Clarke Forthcoming). Methods are available for subjecting adaptive hypotheses to tests (e.g., Orzack and Sober 2001) but as far as I know these have not been applied to biofilm traits.

  9. 9.

    Note that this falls short of demonstrating that the relevant traits are social adaptations—i.e. were selected in virtue of their benefits to the recipient (Mitri and Foster 2013).

  10. 10.

    Ecologists term this ‘protocooperation’ to indicate that the interaction is not essential.

  11. 11.

    In fact Elias & Banin suggest that multispecies biofilms tend to exhibit one of three spatial architectures: a collection of neighbouring clonal microcolonies; co-aggregation in which cells of two species are mixed throughout the colony (‘interdigitated cellular mosaics’ (Katharios-Lanwermeyer et al. 2014); and finally layered structures, in which different species occupy different layers (Elias and Banin 2012, 997). They note that these structures will have very different consequences for the ability of the different species to interact, especially in high flow conditions where diffusibles may not accumulate. There is some evidence, on the other hand, that the structure may be determined by the type of interactions between cells (Momeni et al 2013). In addition, more specific morphologies have been described for particular co-aggregations, such as ‘corncob-like structures’ and ‘rosettes’ (Katharios-Lanwermeyer et al 2014).

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Acknowledgments

Very many thanks to Marc Ereshefsky and Maureen O’Malley who gave me invaluable feedback on earlier drafts of this paper, in addition to two referees, the young folk at All Souls College, and the audience at Philosophy of Biology in the UK 2014. I also received invaluable feedback and experience from Kevin Foster, Sara Mitri, Isabel Frost and Sarah Hammarlund as well as patient guidance from Kim Sterelny.

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Clarke, E. Levels of selection in biofilms: multispecies biofilms are not evolutionary individuals. Biol Philos 31, 191–212 (2016). https://doi.org/10.1007/s10539-016-9517-3

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Keywords

  • Multicellularity
  • Bacteria
  • Biofilm
  • Individuality
  • Organism
  • Microbiology