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Stranger in a strange land: an optimal-environments account of evolutionary mismatch

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Abstract

In evolutionary medicine, researchers characterize some outcomes as evolutionary mismatch. Mismatch problems arise as the result of organisms living in environments to which they are poorly adapted, typically as the result of some rapid environmental change. Depression, anxiety, obesity, myopia, insomnia, breast cancer, dental problems, and numerous other negative health outcomes have all been characterized as mismatch problems. The exact nature of evolutionary mismatch itself is unclear, however. This leads to a lack of clarity about the sorts of problems that evolutionary mismatch can actually explain. Resolving this challenge is important not only for the evolutionary health literature, but also because the notion of evolutionary mismatch involves central concepts in evolutionary biology: fitness, evolution in changing environments, and so forth. In this paper, I examine two characterizations of mismatch currently in the literature. I propose that we conceptualize mismatch as a relation between an optimal environment and an actual environment. Given an organism and its particular physiology, the optimal environment is the environment in which the organism’s fitness is maximized: in other words, the optimal environment is that in which the organism’s fitness is as high as it can possibly be. The actual environment is the environment in which the organism actually finds itself. To the extent that there is a discordance between the organism’s actual and optimal environments, there is an evolutionary mismatch. In the paper, I show that this account of mismatch gives us the right result when other accounts fail, and provides useful targets for investigation.

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Fig. 1

Notes

  1. 1.

    In the philosophical literature to date, the only detailed attempts of which I am aware are Lloyd et al. (2011) and Cofnas (2016). Garson (2015) discusses a certain kind of mismatch but does not give a general characterization.

  2. 2.

    Credit for coining the term is typically given to Bowlby (1982), cf. Barr (1999), Tooby and Cosmides (2005), Gluckman and Hanson (2006) and Taylor (2015). A related term is ‘ancestral environment’, preferred by Lloyd et al. (2011) but treated as roughly equivalent to EEA. I am using the established EEA terminology for brevity, and I think that even mismatch theorists who eschew the particular terminology will recognize its theoretical analogues in their own accounts. The EEA is really a cluster of related concepts and gets used in various ways—Lloyd et al. (2011), for example, describe traits rather than populations as having ‘ancestral environments’—but all I need at the moment is for the reader to understand roughly what the EEA is. Those already familiar with the term should take my use of EEA as a gesture at the phenomenon of interest rather than a commitment to the particular claims of Tooby and Cosmides’s evolutionary psychology. Thanks to an anonymous reviewer for this point.

  3. 3.

    See, e.g., Lindeberg (2010, p. 30). As I said in footnote 2, for the sake of brevity I am eliding the full set of views here: some theorists prefer to think of each trait or mechanism as having a specific EEA.

  4. 4.

    See, e.g., Nesse and Williams (1994), Trevathan (1999), Tooby and Cosmides (2005), Gluckman and Hanson (2006), Keller and Nesse (2006), Gluckman et al. (2009), Lindeberg (2010), Lieberman (2013) and Aktipis et al. (2015).

  5. 5.

    Whether we are being given a story about fitness outcomes or health outcomes can sometimes be a bit fuzzy. More on this in Sect. 6.2.

  6. 6.

    For more discussion of this example, see Gluckman et al. (2009).

  7. 7.

    For more extensive discussion of this highly simplified example and related hypotheses, see Nesse and Williams (1994), Gluckman et al. (2009), Lindeberg (2010) and Lieberman (2013). By contrast, Tideman et al. (2016) found that myopia had a stronger association with serum vitamin D levels than with time spent outdoors, indicating that low vitamin D may be implicated in myopia. Pan et al. (2017) suggest that the evidence supporting the vitamin D hypothesis is still insufficiently strong, however, and argue that the current state of the evidence favors time spent outdoors as a more likely protective factor than higher serum vitamin D. I use the simplified example above in part because it is more popular in the evolutionary health literature.

  8. 8.

    See, e.g., Buller (2006).

  9. 9.

    Garson (2015) gives a sketch of evolutionary mismatch as well, but I take the scope of the account to be a particular kind of mismatch. Thus, I will treat it here as subsumed under Cofnas (2016), due in part to the latter’s use of the former. My thanks to Justin Garson for calling my attention to his work here.

  10. 10.

    The paper is available at the website of The Evolution Institute at https://new.evolution-institute.org/wp-content/uploads/2015/08/Mismatch-Sept-24-2011.pdf.

  11. 11.

    This general adaptationism has been criticized in, e.g., Valles (2012) and Cournoyea (2013), and I will not engage with that worry here.

  12. 12.

    The discussion here is inspired by discussion in Sih et al. (2010) and Sih (2013) of evolutionary mismatch caused by novel predators.

  13. 13.

    See e.g. Ravelli et al. (1998) for more discussion of this incident and the specific results. See Hales and Barker (2013) for further discussion of the so-called “thrifty phenotype hypothesis”.

  14. 14.

    I use ‘physiology’ to refer collectively to an organism’s heritable traits (including phenotypic plasticity), rather than merely to genotype or merely to phenotype.

  15. 15.

    My view does not depend on a particular analysis of evolutionary/reproductive fitness, and the reader should feel free to insert her preferred account. Although I assume a concept of fitness linked in some way to reproductive success, I see no reason that a concept like that developed in Bouchard (2011) could not work here.

  16. 16.

    To be clear, my use of the term ‘optimal environment’ is not intended to refer to optimization in the sense of optimal foraging strategies or other optimality models as discussed in e.g. Orzack and Sober (1994). If anything, the reader should take this sense of ‘optimal environment’ to be similar to, if not quite identical with, that invoked by Gluckman and Hanson (2006, pp. 17–19, 33) and Levins (1968, p. 14): an environment in which fitness is maximized.

  17. 17.

    As mentioned above, Eaton and Konner (1985) and Konner and Eaton (2010) can be consulted for estimates of dietary vitamin C in the diets of early humans.

  18. 18.

    As noted in footnote 16, I realize that ‘optimal’ can be a loaded concept, and so I would like to stress that my use of the term is not intended to imply any theoretical commitments other than what I have explicitly stated here.

  19. 19.

    Cf. Nesse and Williams (1994), Editorial (2009) and Lindeberg (2010).

  20. 20.

    Cf. Gluckman et al. (2005, 2011), Gluckman and Hanson (2006), Keller and Miller (2006), Jasienska (2013) and Cofnas (2016).

  21. 21.

    Thanks to an anonymous reviewer for drawing my attention to this point.

  22. 22.

    My use of the term is inspired by Maner and Kenrick (2010)’s discussion of social anxiety.

  23. 23.

    I am grateful to an anonymous reviewer for these helpful points.

  24. 24.

    It may be the case that fitness is not actually maximized in this case because certain facts of human physiology make this impossible, or it relies on the wrong fitness concept. I suspect the former is actually true. Nevertheless, I think the case worth discussing for the benefit of those who think otherwise.

  25. 25.

    Thanks to an anonymous reviewer for suggesting this response.

  26. 26.

    Thanks to an anonymous reviewer for this point.

  27. 27.

    See Jachmann et al. (1995) and Owens and Owens (2009) for some discussion of this.

  28. 28.

    Absolute fitness, as opposed to relative fitness.

  29. 29.

    Credit for this specific objection goes to Andrew Sih of UC Davis. Several other concerns raised in this section emerged as a result of our conversation, but not all were directly expressed the way I have raised them here. Any failures of clarity or plausibility are my own.

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Acknowledgements

Special thanks to Roberta Millstein (University of California, Davis) for extensive feedback on previous drafts of this article. For excellent discussion and feedback on the project: thanks to James Griesemer, Tina Rulli, Zoe Drayson, and Andrew Sih, all of UC Davis, to Sean Valles of Michigan State, to Justin Garson of Hunter College, to Alan Love and Max Dresow of the University of Minnesota, to Jonathan Tsou of Iowa State University, and to Thomas Stewart and Devin Gouvêa of the University of Chicago. Thanks also to the members of the Griesemer-Millstein Philosophy of Biology Lab at UC Davis. Last but certainly not least, thanks to five anonymous reviewers whose comments strengthened this paper.

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Correspondence to Rick Morris.

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Morris, R. Stranger in a strange land: an optimal-environments account of evolutionary mismatch. Synthese (2018). https://doi.org/10.1007/s11229-018-01915-x

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Keywords

  • Evolutionary mismatch
  • Developmental mismatch
  • Evolution
  • Biology
  • Mismatch
  • Adaptation
  • Environment