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Exploring the Status of Population Genetics: The Role of Ecology

  • Thematic Issue Article: The Meaning of "Theory" in Biology
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Abstract

The status of population genetics has become hotly debated among biologists and philosophers of biology. Many seem to view population genetics as relatively unchanged since the Modern Synthesis and have argued that subjects such as development were left out of the Synthesis. Some have called for an extended evolutionary synthesis or for recognizing the insignificance of population genetics. Yet others such as Michael Lynch have defended population genetics, declaring “nothing in evolution makes sense except in the light of population genetics” (a twist on Dobzhansky’s famous slogan that “nothing in biology makes sense except in the light of evolution”). Missing from this discussion is the use of population genetics to shed light on ecology and vice versa, beginning in the 1940s and continuing until the present day. I highlight some of that history through an overview of traditions such as ecological genetics and population biology, followed by a slightly more in-depth look at a contemporary study of the endangered California Tiger Salamander. I argue that population genetics is a powerful and useful tool that continues to be used and modified, even if it isn’t required for all evolutionary explanations or doesn’t incorporate all the causal factors of evolution.

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Notes

  1. Note that Lewontin, in the essay from which this quote is taken and elsewhere, is quick to point out the limitations of population genetics. Also, although the “auto mechanics” comment is a bit cryptic, it can be reasonably interpreted as meaning “that which gets things going.” Judging by Lewontin’s practice, if not always his stated views, Lewontin is a supporter of population genetics, albeit not as staunch as some.

  2. Okasha (2008) is even more explicit: “The basic structure of population-genetic theory has changed little since the days of Fisher, Haldane and Wright.”

  3. Lloyd (1988) articulates a confirmatory relationship between population genetics and ecology. Nothing I say here is meant to overturn her claims; instead, I mean only to describe an additional sort of relationship.

  4. That is, I will be leaving out discussion of, and citations to, much good work. To cover it all is a book(s) length project.

  5. Here it might be objected that neither of these is considered to be “real” ecology by ecologists. Personally, I have little taste for intra-disciplinary disputes about what counts as “real x” (for example, philosophers are often quick to dismiss other work because it does not count as “real philosophy”) and I tend to see them as more turf-protecting than substantive. Here I will just note that my claim is not that all aspects of ecology have been incorporated into population genetics, but rather just that some aspects have been. Moreover, I suspect that many population geneticists might not recognize these areas as “real” population genetics either. It would not be surprising if blended fields were not fully embraced by those at the core of each of the fields involved in the blend.

  6. For more, see, e.g., Kingsland (1985), Collins (1986), and Odenbaugh (2006).

  7. Here it might be objected that population genetics tracks only genotypes, not phenotypes. Below, however, we shall see some cases where population genetics models have in fact been used to track changes in phenotype frequencies over time. Of course, one of the criticisms made by proponents of EvoDevo still holds, namely that population genetics ignores the processes through which phenotypes develop out of genotypes.

  8. For elaboration of this point, see “The Origins of the Neutralist-Selectionist Debates,” a transcript of a discussion involving John Beatty, James Crow, Michael Dietrich, and Richard Lewontin (http://authors.library.caltech.edu/5456/1/hrst.mit.edu/hrs/evolution/public/transcripts/origins_transcript.html).

  9. The distinction between “ecological genetics” as involving ecological fieldwork and “population biology” as involving mathematical modeling that I am drawing here is not a strong one, i.e., I am not confident that those terms are consistently used in that way by contemporary biologists. But it appears that originally the terms had those connotations.

  10. Levins (1966) shows how different population biology models “all converge in supporting the theorem that environmental uncertainty leads to increased niche breadth” (pp. 426–427). One of the models is a “simple genetic model with one locus and two alleles” and draws on insights from R.A. Fisher (p. 425).

  11. Other work in this vein, and from around the same time period, includes that of León (1974) and Slatkin and Maynard Smith (1979).

  12. I agree with Roughgarden that the textbook is very clear, as well as being better than most in laying out key concepts and assumptions!

  13. Shaffer is now at the University of California, Los Angeles.

  14. Fitzpatrick and Shaffer elaborate, “The cues used by amphibians to emerge from their underground retreats in a Mediterranean climate are poorly understood. It is probably determined in part by physiological clocks and in part by how individuals experience the weather and other seasonal stimuli in their subterranean terrestrial habitat, rather than by the pond in which they will breed. Nonrandom fertilization seems unlikely to be affected much by the pond environment, although spermatophores may spend several minutes in the open water prior to internal fertilization…. Other factors are more likely to have strong environment dependence. For example, visual or olfactory mate choice systems may be disrupted in the turbid, eutrophic water of artificial ponds, potentially explaining why there is a deficit of DLX3 heterozygotes only in the less turbid vernal pools. Alternatively, components of the physical or biotic environment may cause stronger viability selection on embryos and young larvae in vernal pools. The habitat-dependent heterozygote excess at HOXD8 could arise because cattle ponds may present immunological challenges that would be unusual in cleaner vernal pools, leading to balancing selection or heterosis in gene regions involved in pathogen response” (Fitzpatrick and Shaffer 2004, p. 1290). Although one referee of this paper suggested that Fitzpatrick and Shaffer’s explanation amounts to “hand waving,” I think it is an example of how knowledge of organisms in their habitats can help to overcome some of the problems with HWE analysis. Of course, such explanations are defeasible, as Fitzpatrick and Shaffer readily acknowledge.

  15. Note that my claim is not that the Shaffer Lab is the only, or even the first, to perform such studies. For example, the Collins Lab at ASU performed similar studies of a species of salamander native to Arizona, raising many similar ethical and policy issues (Jones et al. 1995; Maienschein et al. 1998; Storfer et al. 2004). Rather, my claim is that the Shaffer Lab studies are illustrative of many such excellent studies.

  16. Although Fitzpatrick and Shaffer certainly go beyond a one-locus, two-allele model!.

  17. Their BAPS software, looking for significant allele frequency differences, identified 15 different populations.

  18. As Wilson and Rannala explain, “The method requires fewer assumptions than estimators of long-term gene flow and can be legitimately applied to nonstationary populations that are far from genetic equilibrium. Moreover, the newly proposed method relaxes a key assumption of previous nonequilibrium methods for assigning individuals to populations and identifying migrants—namely that genotypes are in Hardy–Weinberg equilibrium within populations. We allow arbitrary genotype frequency distributions within populations by incorporating a separate inbreeding coefficient for each population. The joint probability distribution of inbreeding coefficients is estimated from the data” (2003, p. 1178).

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Acknowledgments

Thanks to Jim Collins, Lisa Gannett, Elihu Gerson, Jim Griesemer, Jon Hodge, Jay Odenbaugh, Alirio Rosales, and Rob Skipper for extremely helpful comments, and to Massimo Pigliucci and an anonymous referee for raising a number of concerns that I have attempted to address here. Thanks also to the Konrad Lorenz Institute for Evolution and Cognition Research, Werner Callebaut, Massimo Pigliucci, and Kim Sterelny for the invitation to the workshop.

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    Roberta L. Millstein

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Millstein, R.L. Exploring the Status of Population Genetics: The Role of Ecology. Biol Theory 7, 346–357 (2013). https://doi.org/10.1007/s13752-012-0056-0

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