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Regulatory Evolution and Theoretical Arguments in Evolutionary Biology

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Abstract

The cis-regulatory hypothesis is one of the most important claims of evolutionary developmental biology. In this paper I examine the theoretical argument for cis-regulatory evolution and its role within evolutionary theorizing. I show that, although the argument has some weaknesses, it acts as a useful example for the importance of current scientific debates for science education.

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Notes

  1. See Stern (2000), from where I borrow the title for this section.

  2. It is not the place here to examine Evo-devo in detail. For an excellent introduction, see Carroll (2005b). For more on the history and philosophy of Evo-devo, see Amundson (2005), Sansom and Brandon (2007) and Laubichler and Maienschein (2007). Although I am here discussing the cis-regulatory hypothesis, not all Evo-devo researchers focus primarily on the genetic level (see for example Müller 2007; Müller and Newman 2005; Newman and Müller 2000). See also Love (2008) for viewing Evo-devo as based on a non-reductive epistemology.

  3. The distinction between structural and regulatory mutations is not identical with the distinction between structural and regulatory genes. A mutation is either structural or regulatory, but not all genes are either regulatory or structural. Many proteins (e.g. histones) have both structural and regulatory functions. Note also that there are mutations that are structural (involve aminoacid substitutions) but nevertheless alter regulation (e.g. genes that code for transcription factors).

  4. The idea that morphological evolution proceeds through changes in the timing of developmental processes rather than the creation of new developmental pathways -what has been called heterochrony—is not new (cf. Gould 1977). Recent discoveries in gene regulation enabled the application of this idea to the level of genes.

  5. However, it now seems that 80% of proteins are different between chimps and humans (Glazko et al. 2005).

  6. For discussion of empirical cases the interested reader should consult, apart from Carroll's writings, Wray (2006) and Carroll et al. (2008), and references therein. Stern and Orgogozo (2008) is another detailed discussion of the debate and relevant case studies.

  7. The use of form here should not be taken to imply that research in Evo-devo does not focus on the functions of morphological structures and the evolutionary origin of those functions (cf. Love 2006, 2003). Strictly speaking, we should not equate the distinction between morphology and physiology with the distinction of form versus function.

  8. It has been discovered that there exist redundant copies of crucial components of developmental processes. This genetic redundancy means that certain mutations can be tolerated even if they are pleiotropic (cf. Kafri et al. 2009, as well as Brigandt (2011) for more on genetic redundancy and its connection to evolvability, i.e. the capacity of an organism for adaptive evolution).

  9. Gerhart and Kirschner further discuss the properties of the developmental system that result in specific phenotypic variation (cf. Gerhart and Kirschner 2007; Kirschner and Gerhart 2005). The key point is that a small number of regulatory changes is enough to generate phenotypic variation that does not disrupt the organism and can in principle be selected. In this sense, development 'facilitates' the generation of phenotypic variation.

  10. Craig (2009) suggests that a biological justification for the distinction between physiological and morphological evolution can be found in the mode of paralog divergence of Hox genes (paralogs are genes that arose by gene duplication and evolved new functions). However, there is no evidence that paralog divergence of Hox genes proceeds primarily by cis-regulatory evolution rather than coding sequence evolution (cf. Fares et al. 2003; Chiu et al. 2001). So, even if we succeed in making the distinction the way Craig suggests, this is irrelevant for the theoretical argument discussed here.

  11. However, recent findings suggest that Carroll may be right after all. Liao et al. (2010) have compared the evolution of what they called ‘morphogenes’ and ‘physiogenes’ (genes, changes in which affect morphology and physiology, respectively) and have found that morphogenes are more pleiotropic and less tissue-specific and that coding sequence evolution is faster in physiogenes, whereas gene expression evolves faster in morphogenes. However, there seems to be no difference concerning the respective rates of cis-regulatory evolution. This can be explained if morphogenes require fewer cis-regulatory changes, for a given amount of change in gene expression (cf. Monteiro and Podlaha 2009). If this is true, then there exist a biological reason why morphological evolution proceeds differently from physiological evolution.

  12. Of course, Carroll’s papers include empirical evidence for cis-regulatory evolution. However, the general claim that morphological evolution proceeds mainly through changes in cis-regulation, is not possible without the theoretical argument. The empirical evidence only results in the claim that cis-regulatory evolution is one of the many ways morphological evolution can proceed.

  13. Recall Darwin's claim that natural selection is ‘the most important, but not the exclusive means of modification' (Darwin 1872: 4). Darwin argues that although there are many other means of modification (e.g. sexual selection, the law of use and disuse, or laws of correlation of growth), natural selection is the most frequent and powerful factor in evolution.

  14. It has been argued that selection and drift cannot be conceptually distinguished, and so it does not make sense to argue which is more significant (cf. Beatty (1984) as well as Millstein (2002) for a different view). Could this be the case with the regulatory versus structural evolution debate? I think not. The various alternative mechanisms mentioned earlier (regulatory or structural mutations, gene duplications etc.) are all types of mutations; the question then is which type of mutation is the most prevalent. So, apart from any practical difficulties to measure relative significance, there does not seem to be a conceptual problem in distinguishing regulatory from other types of evolutionary change.

  15. See Wimsatt (2007) and Odenbaugh (2005) for similar points about the heuristic use of models in biology.

  16. For example, see the discussion on NOS (‘nature of science') in Kampourakis and McComas (2010).

  17. For an exception see Silverman (1992), which contains a useful general discussion with many case studies. See also Kipnis (2001), Paraskevopoulou and Koliopoulos (2010), and Braga et al. (2010), which discuss the importance of specific controversies from the history of science for science teaching.

  18. I borrow the phrase from Gould and Lewontin (1979: 585).

  19. What about the intelligent design versus evolution controversy? Should this be part of science education, as proponents of intelligent design have argued? It is clear from the discussion in this section that the answer is negative. Even if we accept that theories which employ supernatural explanations are in principle comparable with scientific ones, the important point here is that this controversy is not part of current scientific discussions, where ID is not considered as an alternative theory to evolution. So, the main reason in favour of the inclusion of scientific controversies in science education (i.e. that they illustrate the dynamics of science) rules out the ID versus evolution controversy (see Scott and Branch 2003 for more on this topic).

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Acknowledgments

I would like to thank Samir Okasha, Ingo Brigandt, as well as two anonymous referees for this journal for their helpful comments and criticism that greatly improved this paper.

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    Stavros Ioannidis

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Ioannidis, S. Regulatory Evolution and Theoretical Arguments in Evolutionary Biology. Sci & Educ 22, 279–292 (2013). https://doi.org/10.1007/s11191-011-9378-8

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