Abstract
There is surprisingly little philosophical work on conceptually spelling out the difference between the traits on which natural selection may be said to act (e.g. “having a high running speed”) and mere circumstantial traits (e.g. “happening to be in the path of a forest fire”). I label this issue the “selectable traits problem” and, in this paper, I propose a solution for it. I first show that, contrary to our first intuition, simply equating selectable traits with heritable ones is not an adequate solution. I then go on to argue that two recent philosophical solutions to this problem—due to Peter Godfrey-Smith and Pierrick Bourrat—are unconvincing because they cannot accommodate frequency-dependent selection. The way out of this difficulty is, I argue, to accept that extrinsic properties dependent on relations between intrinsic properties of the population members should also count as selectable traits. I then show that my proposal is legitimized by more than the simple accommodation of frequency-dependent selection.
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Notes
Obviously, these “individual members” of the population might be biological entities at various levels of biological organization, potentially ranging from genes to species.
Of course, some theorists prefer a stricter notion of natural selection, as will be discussed shortly.
An anonymous reviewer raised this issue.
The chance element involved in the distribution of the causes of variance of reproductive success is plastically highlighted by other biologists. According to Waples (2002, p. 1030), Hedgecock’s explanation implies that “the vast majority of families produce no offspring that survive to adulthood because their larvae do not end up in the right place at the right time to survive the critical phase(s).” Similarly, according to Árnason et al. (2023, p. 2), Hedgecock’s hypothesis consists in that “by chance, a random individual hits the jackpot of favorable environmental conditions that result in a very large reproductive output”.
Whether Hedgecock’s explanation for the observed genetic variation patterns is correct is not the issue here. His explanation has, for example, been challenged by Nunney (1996), but Nunney’s objection has in turn been challenged by Hedrick (2005). I am less interested in the empirical correctness of Hedgecock’s explanation than in the fact that he uses an implicit distinction between selectable and circumstantial traits in his explanation. Let me add that a brief philosophical take on Hedgecock’s hypothesis can be found in Gildenhuys (2009).
A similar explanation is provided by Turner et al. (2006, p. 3070) with respect to the Rio Grande silvery minnow, where “the distance to the nearest downstream dam and the magnitude of river flows where spawning occurred” are seen as the main factors determining the variance in reproductive success.
This is why Sober’s (2020) strategy of distinguishing between expected fitnesses of individuals and of traits remains unconvincing: it fails to establish which traits are admissible.
Endler (1986, p. 33) states that “Natural selection […] is a process, resulting from heritable biological differences among individuals.” But “heritable biological differences” is not the same as “heritable differences”: though it is not clear what is meant by the specification that the differences are “biological,” it would be hard to claim that, for Endler, heritability alone establishes a trait’s selectability, which is the position I am assessing here. Among philosophers, Hodge (1987, p. 251) and Millstein (2002, p. 37, 2021) claim that “heritable physical differences” between biological entities are the relevant ones for selection, but, again, they do not claim that heritability alone establishes whether a trait is potentially relevant for selection. Sterelny (2011) seems closer to a position of this sort when he argues that the intrinsicness of traits is not important in itself, but as a source of heritability.
I borrow Brandon’s (1990) terms for this distinction. Other terms are used in the literature to convey the same distinction. For example, Jacquard (1983) also uses “genetic heritability” for the latter notion, but labels the former notion as “biometric heritability,” while Bourrat (2022) uses the terms “variance approach” and “regression approach” to heritability.
Note that I focus here on what is usually called “narrow genetic heritability” (Jacqard, 1983; Falconer and McKay, 1996) in quantitative genetics. Another genetic notion, “broad genetic heritability,” denotes the fraction of the total phenotypic variance that results from genetic variance (additive or not). But I leave the broad notion out of this discussion because, as per the admission of many biologists, it plays only a little role in evolutionary biology (Jacqard, 1983; Falconer and McKay, 1996; Rice, 2004). It should, however, be noted that when it comes to seeing them as solutions to STP, narrow and broad genetic heritability exhibit the same main drawbacks.
Let me add that Bourrat (2022) proposes a new notion of heritability, one that could potentially avoid the limitations of the two notions discussed here. But the notion of “relative intrinsicness” that his account is based on seems to me to be underdetermined for the time being (indeed, it is not clear if “relative intrinsicness” refers to a quantitative property possessed by individuals or to a binary—yes or no—property of a population). But if this account of heritability were fully and convincingly specified and if it were also advanced as a solution to STP, it could potentially constitute an alternative to the solution I propose here.
Another potential problem is that, depending on various factors (genetic, environmental), the same trait might be transmitted—in the informal sense—by some parents to their offspring, but not by others. If one were to equate the selectability of traits with their transmissibility in this informal sense, one would potentially be led to conclude that the same trait is selectable for a part of the focal population (the part for which the trait is transmitted) and not selectable for the other part.
Let me note that Godfrey-Smith does not make the direct claim that intrinsic properties are the ones on which selection may be said to act, while extrinsic ones are not. Such a claim was not necessary for the conventionalist approach of his 2009 book. However, his suggestion may be and, indeed, has been so interpreted (Bourrat, 2015, 2017). Here, it is not necessarily Godfrey-Smith that I am criticizing, but the possible or actual attempts to follow Godfrey-Smith’s suggestion by equating selectable traits with intrinsic ones.
Technically, colors are not intrinsic properties because they depend on the wavelengths of ambient light (and, depending on how we interpret them, potentially also on an external visual perception). But our red and brown colors could be reduced to their underlying surface molecular structure, and these would indeed constitute intrinsic properties (see Brandon, 1990). Here, I take them as intrinsic properties in this latter sense.
One might suggest that a type might evolve a characteristic that gives it an advantage in populations where it is common, even if it is otherwise a disadvantage to be common. If the newly evolved characteristic were intrinsic (or extrinsic caused by an intrinsic one), the hypothetical scenario would pose less problems for Godfrey-Smith’s solution. This is theoretically possible, though no empirical case of this sort immediately comes to mind. But this does not change the fact that the bulk of frequency-dependent selection cases (which present no evolved characteristics of the type hypothesized here) clashes with Godfrey-Smith’s solution to STP. And this is enough for my purposes in this paper.
An anonymous reviewer raised this point.
Of course, things are different if the local densities vary because of one or more intrinsic properties of individuals. But, as pointed out above, this possibility is covered by Godfrey-Smith’s solution to STP.
Another anonymous reviewer raised this issue.
Vallentyne (1997) understands intrinsic properties as those properties that an object would have even if we were to remove all other distinct objects from its world at the focal time t (for a similar view, see Yablo, 1999; for discussion, see Marshall & Weatherson, 2018). This gives more precision to the meaning of Godfrey-Smith’s “independence” from the existence and arrangement of other objects, insofar as it shows that this independence is relativized to the time t when the putative intrinsic property is instantiated.
Including abilities among intrinsic traits is akin to Godfrey-Smith’s inclusion of preferences among intrinsic traits. But, one could retort, could we then not speak of “the ability to be in the path of a forest fire” or “the ability to be struck by lightning” and claim that these too are intrinsic? I believe this would constitute an abuse of the notion of “ability.” Indeed, “abilities” are usually seen by philosophers as related to actions performed by agents and this is what distinguishes them from other powers, dispositions or affordances of things and living beings (see Maier, 2020 for discussion).
As already alluded to above, Bourrat also admits that differences in survival and reproductive success that are caused by differences in intrinsic-variable properties or by differences in extrinsic properties should also be attributed to natural selection if these latter differences are themselves “causally determined” by differences in intrinsic-invariable properties (Bourrat 2017, p. 33; see also Bourrat 2015, p. 315).
Of course, this class might contain only one element, i.e. the target individual.
These relations that “supervene on the intrinsic properties of their relata” are called “internal relations” by Langton and Lewis (1998, p. 343).
Here is a relevant quotation from Millikan (1984, p. 22): “It is not directly because my father and mother had two legs that I have two legs. Mutilated parents can produce normal children; wooden legs are not inherited. Rather, (…) my genes (tokens) were reproductions of earlier gene tokens harbored by our respective parents, and similar genes produced similar products. It is this sort of consideration that will later complicate the definition of ‘reproductively established family’ causing us to divide these into first-order and higher-order families. Only in the case of first-order families are the members ‘reproductions’ of one another in the sense of ‘reproduction’ we have defined. People and hearts, etc., are members of higher-order reproductively established families”.
We can express this in terms of Price’s (1970) equation. We can write each individual’s trait and reproductive success values as a function of the population mean and of that individual’s deviation from the mean: \(z_{i} = z_{p} + \Delta z_{ip}\) and \(w_{i} = w_{p} + \Delta w_{ip}\) (where \(z_{i}\) and \(w_{i}\) are the trait and reproductive success of the ith individual, \(z_{p}\) and \(w_{p}\) are the average trait and reproductive success in the population). By replacing these equations into Price’s equation (and assuming that individuals breed truly and that generations do not overlap), we can write the population change in z (\(\Delta z_{p}\)) that is due to selection as \(\Delta z_{p} = Cov(\Delta z_{ip} ,\Delta w_{ip} )/w_{p}\).
One could rightfully argue that individual height is a primitive property, while the individual difference with respect to average population height is a second-order property that supervenes on the primitive one. Does this constitute a knock-down argument against the claim that a property like \(\Delta z_{ip}\) may also be seen as relevant for selection in directional selection? Not unless it is coupled with the claim that only primitive properties possess causal powers, and this latter claim raises too great metaphysical issues to be considered the default option.
References
Antonovics, J., Ellstrand, N. C., & Brandon, R. (1988). Genetic variation and environmental variation: Expectations and experiments. In L. D. Gottlieb & S. K. Jain (Eds.), Plant evolutionary biology (pp. 275–303). Chapman & Hall.
Árnason, E., Koskela, J., Halldórsdóttir, K., & Eldon, B. (2023). Sweepstakes reproductive success via pervasive and recurrent selective sweeps. eLife, 12, e80781. https://doi.org/10.7554/eLife.80781
Avital, E., & Jablonka, E. (2001). Animal traditions: Behavioural inheritance in evolution. Cambridge University Press.
Ayala, F., & Campbell, C. (1974). Frequency-dependent selection. Annual Review of Ecology and Systematics, 5, 115–138. https://doi.org/10.1146/annurev.es.05.110174.000555
Baraghith, K. (2020). Investigating populations in generalized Darwinism. Biology & Philosophy, 35(1), 19. https://doi.org/10.1007/s10539-020-9735-6
Birch, J. (2016). Hamilton’s two conceptions of social fitness. Philosophy of Science, 83(5), 848–860. https://doi.org/10.1093/bjps/axt016
Bourrat, P. (2015). Distinguishing natural selection from other evolutionary processes in the evolution of altruism. Biological Theory, 10(4), 311–321. https://doi.org/10.1007/s13752-015-0210-6
Bourrat, P. (2017). Explaining drift from a deterministic setting. Biological Theory, 12(1), 27–38. https://doi.org/10.1007/s13752-016-0254-2
Bourrat, P. (2022). Unifying heritability in evolutionary theory. Studies in History and Philosophy of Science, 91, 201–210. https://doi.org/10.1016/j.shpsa.2021.10.019
Brandon, R. N. (1978). Adaptation and evolutionary theory. Studies in History and Philosophy of Science, 9(3), 181–206. https://doi.org/10.1016/0039-3681(78)90005-5
Brandon, R. N. (1990). Adaptation and environment. Princeton University Press.
Damuth, J. (1985). Selection among ‘species’: A formulation in terms of natural functional units. Evolution, 39(5), 1132–1146. https://doi.org/10.1111/j.1558-5646.1985.tb00453.x
Endler, J. A. (1986). Natural selection in the wild. Princeton University Press.
Falconer, D. S., & Mackay, T. F. (1996). Introduction to quantitative genetics (4th ed.). Longman.
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford University Press.
Futuyma, D. J. (2005). Evolution. Sinauer Associates.
Gildenhuys, P. (2009). An explication of the causal dimension of drift. British Journal for the Philosophy of Science, 60(3), 521–555. https://doi.org/10.1093/bjps/axp019
Godfrey-Smith, P. (2009). Darwinian populations and natural selection. Oxford University Press.
Griffiths, P. E., & Gray, R. D. (2001). Darwinism and developmental systems. In S. Oyama, P. E. Griffiths, & R. D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 195–218). MIT Press.
Hedgecock, D. (1994). Does variance in reproductive success limit effective population sizes of marine organisms? In A. Beaumont (Ed.), Genetics and evolution of aquatic organisms (pp. 122–134). Chapman & Hall.
Hedgecock, D., & Pudovkin, A. I. (2011). Sweepstakes reproductive success in highly fecund marine fish and shellfish: A review and commentary. Bulletin of Marine Science, 87(9), 971–1002. https://doi.org/10.5343/bms.2010.1051
Hedrick, P. (2005). Large variance in reproductive success and the Ne/N ratio. Evolution, 59(7), 1596–1599. https://doi.org/10.1111/j.0014-3820.2005.tb01809.x
Hodge, M. J. S. (1987). Natural selection as a causal, empirical, and probabilistic theory. In K. Gigerenzer, L. Krüger, & M. S. Morgan (Eds.), The probabilistic revolution (pp. 233–270). MIT Press.
Jacquard, A. (1983). Heritability: One word, three concepts. Biometrics, 39(2), 465–477.
Jeler, C. (2017). Multi-level selection and the issue of environmental homogeneity. Biology & Philosophy, 32(5), 651–681. https://doi.org/10.1007/s10539-017-9578-y
Joshi, A., & Mueller, L. D. (1988). Evolution of higher feeding rate in Drosophila due to density-dependent natural selection. Evolution, 42(5), 1090–1093. https://doi.org/10.2307/2408924
Langton, R. C., & Lewis, D. (1998). Defining ‘intrinsic.’ Philosophy and Phenomenological Research, 63(2), 333–345.
MacBride, F. (2020). Relations. In E. N. Zalta (Ed.) The Stanford encyclopedia of philosophy (Winter 2020 Edition), https://plato.stanford.edu/archives/win2020/entries/relations/
Maier, J. (2020). Abilities. In E. N. Zalta & U. Nodelman (Eds.) The Stanford encyclopedia of philosophy (Fall 2022 Edition), https://plato.stanford.edu/archives/fall2022/entries/abilities/
Mameli, M. (2004). Nongenetic selection and nongenetic inheritance. The British Journal for the Philosophy of Science, 55(1), 35–71. https://doi.org/10.1093/bjps/55.1.35
Marshall, D., & Weatherson, B. (2018). Intrinsic vs. extrinsic properties. In E. N. Zalta (Ed.) The Stanford encyclopedia of philosophy (Spring 2018 Edition), https://plato.stanford.edu/archives/spr2018/entries/intrinsic-extrinsic/.
Matthen, M. (2010). What is drift? A response to Millstein, Skipper, and Dietrich. Philosophy and Theory in Biology, 2, e102. https://doi.org/10.3998/ptb.6959004.0002.002
Matthewson, J. (2015). Defining paradigm Darwinian populations. Philosophy of Science, 82(2), 178–197. https://doi.org/10.1086/680665
Michod, R. E. (1999). Darwinian dynamics evolutionary transitions in fitness and individuality. Princeton University Press.
Millikan, R. (1984). Language, thought, and other biological categories. MIT Press.
Mills, S. K., & Beatty, J. H. (1979). The propensity interpretation of fitness. Philosophy of Science, 46(2), 263–286. https://doi.org/10.1086/288865
Millstein, R. L. (2002). Are random drift and natural selection conceptually distinct? Biology & Philosophy, 17(1), 33–53. https://doi.org/10.1023/A:1012990800358
Millstein, R. L. (2006). Natural selection as a population-level causal process. The British Journal for the Philosophy of Science, 57(4), 627–653. https://doi.org/10.1093/bjps/axl025
Millstein, R. L. (2010). The concepts of population and metapopulation in evolutionary biology and ecology. In M. A. Bell, D. J. Futuyma, W. F. Eanes, & J. S. Levinton (Eds.), Evolution since Darwin: The first 150 years (pp. 61–85). Sinauer.
Millstein, R. L., Skipper, R. A., Jr., & Dietrich, M. R. (2009). (Mis)interpreting mathematical models of drift: Drift as a physical process. Philosophy and Theory in Biology, 1, 1–13. https://doi.org/10.3998/ptb.6959004.0001.002
Millstein, R. L. (2021). Genetic drift. In Edward N. Zalta (Ed.), The Stanford encyclopedia of philosophy (Spring 2021 Edition), https://plato.stanford.edu/archives/win2020/entries/relations/
Morsky, B., & Bauch, C. T. (2019). The impact of truncation selection and diffusion on cooperation in spatial games. Journal of Theoretical Biology, 466, 64–83. https://doi.org/10.1016/j.jtbi.2019.01.023
Nunney, L. (1996). The influence of variation in female fecundity on effective population size. Biological Journal of the Linnean Society, 59(4), 411–425. https://doi.org/10.1111/j.1095-8312.1996.tb01474.x
Price, G. R. (1970). Selection and covariance. Nature, 227(5257), 520–521. https://doi.org/10.1038/227520a0
Rice, S. H. (2004). Evolutionary theory: Mathematical and conceptual foundations. Sinauer Associates.
Ridley, M. (2004). Evolution (3rd edition). Balckwell Publishing.
Scriven, M. (1959). Explanation and prediction in evolutionary theory. Science, 130(3374), 477–482. https://doi.org/10.1126/science.130.3374.477
Sober, E. (2020). Fitness and the twins. Philosophy, Theory, and Practice in Biology, 12(1), 1–13. https://doi.org/10.3998/ptpbio.16039257.0012.001
Sober, E. (1984). The nature of selection evolutionary theory in philosophical focus. University of Chicago Press.
Sterelny, K. (2003). Last will and testament: Stephen Jay Gould’s the structure of evolutionary theory. Philosophy of Science, 70(2), 255–263. https://doi.org/10.1086/375466
Sterelny, K. (2011). Darwinian spaces: Peter Godfrey-Smith on selection and evolution. Biology & Philosophy, 26(4), 489–500. https://doi.org/10.1007/s10539-010-9244-0
Sterelny, K., Smith, K., & Dickison, M. (1996). The extended replicator. Biology & Philosophy, 11(3), 377–403. https://doi.org/10.1007/BF00128788
Turner, T. F., Osborne, M. J., Moyer, G. R., Benavides, M. A., & Alò, D. (2006). Life history and environmental variation interact to determine effective population to census size ratio. Proceedings of the Royal Society B, 273(1605), 3065–3073. https://doi.org/10.1098/rspb.2006.3677
Vallentyne, P. (1997). Intrinsic properties defined. Philosophical Studies, 88(2), 209–219. https://doi.org/10.1023/A:1004250930900
Wagner, G. P. (2010). The measurement theory of fitness. Evolution, 64(5), 1358–1376. https://doi.org/10.1111/j.1558-5646.2009.00909.x
Waples, R. S. (2002). Evaluating the effect of stage-specific survivorship on the Ne/N ratio. Molecular Ecology, 11(6), 1029–1037. https://doi.org/10.1046/j.1365-294x.2002.01504.x
Yablo, S. (1999). Intrinsicness. Philosophical Topics, 26(1–2), 479–505. https://doi.org/10.5840/philtopics1999261/234
Acknowledgements
This work was supported by a grant of the Ministry of Research, Innovation and Digitization, CNCS—UEFISCDI, project number PN-III-P1-1.1-TE-2021-1122, within PNCDI III. I am grateful to Andreea Eşanu, Mihai Cernea and three anonymous reviewers for their comments on earlier drafts of this paper. I presented this paper at the 2022 PSA Conference in Pittsburgh and I would like to thank the audience (and especially Pierrick Bourrat) for questions and suggestions.
Funding
This work was supported by a grant of the Ministry of Research, Innovation and Digitization, CNCS—UEFISCDI, project number PN-III-P1-1.1-TE-2021-1122, within PNCDI III.
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Jeler, C. How should we distinguish between selectable and circumstantial traits?. HPLS 46, 6 (2024). https://doi.org/10.1007/s40656-023-00604-4
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DOI: https://doi.org/10.1007/s40656-023-00604-4