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Evolutionary transitions in heritability and individuality

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Abstract

With a few exceptions, the literature on evolutionary transitions in individuality (ETIs) has mostly focused on the relationships between lower-level (particle-level) and higher-level (collective-level) selection, leaving aside the question of the relationship between particle-level and collective-level inheritance. Yet, without an account of this relationship, our hope to fully understand the evolutionary mechanisms underlying ETIs is impeded. To that effect, I present a highly idealized model to study the relationship between particle-level and collective-level heritability both when a collective-level trait is a linear function and when it is a nonlinear function of a particle-level trait. I first show that when a collective trait is a linear function of a particle-level trait, collective-level heritability is a by-product of particle-level heritability. It is equal to particle-level heritability, whether the particles interact randomly or not to form collectives. Second, I show that one effect of population structure is the reduction in variance in offspring collective-level character for a given parental collective. I propose that this reduction in variance is one dimension of individuality. Third, I show that even in the simple case of a nonlinear collective-level character, collective-level heritability is not only weak but also highly dependent on the frequency of the different types of particles in the global population. Finally, I show that population structure, because one of its effects is to reduce the variance in offspring collective-level character, allows not only for an increase in collective-level character but renders it less context dependent. This in turn permits a stable collective-level response to selection. The upshot is that population structure is a driver for ETIs. These results are particularly significant in that the relationship between population structure and collective-level heritability has, to my knowledge, not been previously explored in the context of ETIs.

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Notes

  1. For a recent update of the view developed in Maynard Smith and Szathmary (1995), see Szathmary (2015).

  2. Note that because I am interested in the evolutionary origins of individuality, by ‘individual’ I will mean throughout ‘evolutionary’ or ‘Darwinian individual.’ For other definitions of individuality and organismality, see Pepper and Herron (2008), Gilbert et al. (2012), Lidgard and Nyhart (2017a), Godfrey-Smith (2013). Note also that there is some tension with the view that a unit of selection can be equated with Darwinian individuality. In fact, one might consider that individuality ‘emerges’ at one level when not one but a large number of traits at that level exhibit differences in fitness and heritability, while Lewontin’s conditions are trait specific. I will put these problems to the side here and consider the two as synonymous.

  3. Note that the conditions require nevertheless to be slightly amended to fit the specificities of different levels of organization in the context of ETIs. For attempts to amend them, see for instance De Monte and Rainey (2014), Bourrat (2014), Bourrat (2015a), Griesemer (2000).

  4. The notion of context dependence is notoriously ambiguous (Godfrey-Smith 1992; Lloyd 1988, p. 69; Sober and Wilson 1994, p. 539). By ‘context dependence’ in this article, I will mean ‘independent from the particle-type frequencies in the global population.’

  5. For a similar approach to mine, in which the authors analyze the heritability of ‘heterozygosity’ in the context of diploid sexual species in which variation in the environment is not considered, see Nietlisbach et al. (2016).

  6. Recall that I assume that all particles produce the same number of offspring at each generation in an infinitely large population, so that I keep both selection (i.e., difference in fitness associated with differences in phenotype) and drift out of the picture here.

  7. For the difference between the binomial and hypergeometric distributions, see Wroughton and Cole (2013).

  8. For a model based on the ‘wrinkly spreader’ strain of Pseudomonas fluorescens (see Rainey and Rainey 2003; Hammerschmidt et al. 2014), in which a fitness trade-off between collective viability and fecundity is considered, see Rainey and Kerr (2010). The sort of trade-off I have in mind here is slightly different as it concerns fidelity of transmission and fertility.

  9. The notion of allele used here is similar to the one presented in Lu and Bourrat (2018), that is following an evolutionary conception of the gene, not a molecular one.

  10. Thanks to Jonathan Hodge for pointing out this reference to me.

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Acknowledgements

I am thankful to Matthew Herron, Michael Bentley, and two anonymous reviewers who provided useful feedback on previous versions of this manuscript. I am also thankful to the Theory and Method in Biosciences group at the University of Sydney and more particularly Stefan Gawronski who proofread the final manuscript. This research was supported by a Macquarie University Research Fellowship and a Large Grant from the John Templeton Foundation (Grant ID 60811).

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  1. Department of Philosophy, Macquarie University, North Ryde, NSW, 2109, Australia

    Pierrick Bourrat

  2. Department of Philosophy and Charles Perkins Centre, The University of Sydney, Camperdown, NSW, 2006, Australia

    Pierrick Bourrat

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Bourrat, P. Evolutionary transitions in heritability and individuality. Theory Biosci. 138, 305–323 (2019). https://doi.org/10.1007/s12064-019-00294-2

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