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Origins of evolutionary transitions

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Abstract

An ‘evolutionary transition in individuality’ or ‘major transition’ is a transformation in the hierarchical level at which natural selection operates on a population. In this article I give an abstract (i.e. level-neutral and substrate-neutral) articulation of the transition process in order to precisely understand how such processes can happen, especially how they can get started.

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Notes

  1. This is a philosophical strategy, intended to complement, rather than to replace, the more standard strategy of generalising from data.

  2. Note that I am not committed to saying that selection causes transitions – in fact I will deny that selection can bring about the first transitional step. Instead I am using a definition on which a change in the level of selection is what constitutes a transition. I defend this view in Clarke 2013, arguing that only a selectively defined concept is capable of underpinning the successful inferences we achieve regarding the action of natural selection.

  3. Note that the parts of State One and State Two objects may or may not be identical. In other words, a transition can be fraternal or egalitarian (Queller 2000). In real-life cases, the parts are unlikely to ever be genetically identical, and will sometimes be from different species. So there is nothing in this schema which precludes symbiotic or chimeric higher-level organisms.

  4. This is an idealization. Real-life organisms will almost never meet this ideal – that is, there will always be some lower-level conflict, excepting perhaps very tiny organisms.

  5. Note that sometimes we use the term ‘higher-level’ to refer to lower-level properties viewed from a particular scale. For example, water molecules do not exhibit waves but water does. This is different from my use, in which to say that selection is at the higher level is to make a claim about the scale at which variance occurs. This is not a matter of perspective – meiotic drive, for example, either takes place or it does not (Okasha 2006).

  6. This is not to imply that partial steps in a transition cannot take place relatively suddenly, but a whole transition – all the way from no selection at level x to exclusive selection at x – will probably require a multiplicity of steps, and will happen gradually, rather than all at once. This is not because the changes have to be genetic, but only because the elimination of lower-level selection is not a simple thing to accomplish, and usually requires several different complex policing mechanisms working simultaneously. See section 4.

  7. Bourke divides the process of transition itself into three distinct phases – social group origination, maintenance and transformation (Bourke 2011 p 15). I prefer to think of the transition process as smoothly continuous rather than carving it up into discrete segments, but nonetheless agree that there are distinguishable questions to be asked about it.

  8. It is important to be clear that when I say ‘object-level selection’ or ‘lower-level selection’, I always refer to variation in fitness among objects within groups, not to variation in fitness among objects in the global population (Sober 2011).

  9. Buss’ own answer to the problem focuses on the role of germ soma separation in eliminating competition between different cell lineages in a multicellular.

  10. For example, it may be assumed that reproducing clumps of cells are easy to generate, and offer obvious selective advantages, without giving proper consideration to issues such as how reproduction of the whole emerges, or how such clumps can overcome some obvious difficulties, such as the build-up of waste products.

  11. Again, this is idealized – in real-life transitions the start and end points are unlikely to be perfectly exclusive levels of selection.

  12. For example, contextual analysis (Heisler and Damuth 1987; Goodnight et al. 1992; Goodnight 2013); neighbourhood analysis (Nunney 1985; Nowak and May 1992; Godfrey-Smith 2008); inclusive fitness analysis (Hamilton 1964; Gardner, West and Wild 2011).

  13. Taken from Okasha 2006. See also Gardner 2008.

  14. After all, we could use mechanical means to stick together a group of humans, but would not therein consider the group to constitute a super-organism – why not?

  15. Note that this still qualifies as kin selection under the statistical understanding of relatedness as a regression coefficient (Frank 1998).

  16. Although a new mechanism may spread through a population just as a consequence of drift or novel niche occupation. I thank my referee for pointing this out.

  17. Again, I refer here to selection between cells within the organism, rather than globally (Sober 2011).

  18. As my referee pointed out, these simple mechanisms may be exaptations – phenomena that were selected at the lower level for one function, but are subsequently recruited for a different purpose in the higher-level collective.

  19. Such feedback processes have now been modelled, for example in Garcia and De Monte 2013; Powers et al. 2011; Fleming 2012.

  20. I deny that stickiness, on its own, can bestow one hundred per cent higher-level individuality on an aggregate of cells (contrast Newman 2003). It is merely a first step. My argument is that a whole transition – all the way to the capacity for selection being held exclusively at the higher level – requires a multiplicity of such steps, and in this sense should be viewed as gradual, rather than happening all at once.

  21. Bouchard 2008.

  22. In any case, even paradigm reproduction would be insufficient in the case where offspring production is exactly coincident with the death of the parent, so that the replication event fails to make any positive increase in the overall population number.

  23. Coral colonies, for example, do not fission as a programmed developmental event, like starfish do. It just occurs when the group is large and there is a storm.

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Acknowledgements

This article emerged out of long and fruitful discussions with Silvia De Monte and Paul B Rainey, which followed the hugely fecund meeting of perspectives that was ‘Individuals and Groups’ in Almora. In addition to them, I give many thanks to Stuart Newman, my anonymous referees and especially to Vidyanand Nanjundiah.

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  1. All Souls College, 27 High Street, Oxford, OX1 4AL, UK

    Ellen Clarke

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Correspondence to Ellen Clarke.

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[Clarke E 2014 Origins of evolutionary transitions. J. Biosci. 39 1–14] DOI 10.1007/s12038-013-9375-y

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Clarke, E. Origins of evolutionary transitions. J Biosci 39, 303–317 (2014). https://doi.org/10.1007/s12038-013-9375-y

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