Searching for evo‐devo's Holy Grail: the nature of developmental variation

When Evolution & Development initiated its “Highlights and Comments” section in 2007, the plan was to draw attention to selected important articles in much the same way that Nature does through its “News and Views” section, but with a broader remit in two respects. Highlights (as they will be referred to from here on) were intended to cover a wider range of journals than “their own” one—most News and Views articles are on papers published in Nature. And while most Highlights were also expected to be on recently published articles, there was provision for occasional “historical highlights,” drawing attention to older publications that have become of renewed interest in the evo-devo era. The first of these two anticipated features of Highlights— covering articles published in a range of journals—has indeed come to pass, but the second—the appearance of occasional “historical highlights”—has not. Here, I try to make good that omission, but not by focusing solely on a notable work from the past. Rather, I focus on one such publication— Haldane’s (1932) book The Causes of Evolution—but also one important recent article (Sanger et al. 2011) and try to relate these to each other. As my title suggests, this endeavor concerns our quest to understand the nature of developmental variation, and thereby to understand whether the structure of such variation plays a role in determining the direction of evolutionary change. In contrast to his contemporary, R.A. Fisher (1930), who can reasonably be labeled a pan-selectionist, J.B.S. Haldane (1932) was a pluralist in relation to the factors that determine the direction of evolution. This is apparent from his title, which refers to the “Causes,” not the “Cause,” of evolution, and it becomes even more apparent from some sections of the text, especially toward the end of Chapter 5 (What is Fitness? ). At this point in the book, Haldane makes the following statement: “To sum up, it would seem that natural selection is the main cause of evolutionary change in species as a whole. But the actual steps by which individuals come to differ from their parents are due to causes other than selection, and in consequence evolution can only follow certain paths. These paths are determined by factors which we can only very dimly conjecture. Only a thorough-going study of variation will lighten our darkness” (the italics are mine). Earlier this year, an interesting article that picks up this theme (though without referring to Haldane) was published in Molecular and Developmental Evolution (Sanger et al. 2011). It begins: “If we wish to understand whether development influences the rate or direction of morphological evolution, we must first understand the developmental bases of morphological variation within species” (this time the italics are in the original). Of course, intraspecific variation includes much more than just the differences between parents and their offspring—for example, it also includes sexual dimorphism and variation in developmental reaction norms at the population level—but the overall message is the same: the direction of evolution involves an interplay between heritable variation and natural selection, rather than being explicable in terms of the latter alone. It is now time to connect this issue with the voluminous literature on the subject of developmental bias, or developmental constraint as many authors call it (e.g., Gould and Lewontin 1979; Maynard Smith et al. 1985; Schwenk 1995; Arthur 2004). There are two key questions: first, is developmental variation structured, so that from any given starting point some variant developmental trajectories are possible while others are not, or at least are less probable (bias present), or is such variation equally available in all directions (bias absent)? Second, if the variation is indeed structured, for example, such that an increase in the value of character X is always associated with an increase in the value of Y, can this structuring be “broken” by natural selection? The possibility of it being broken depends on the existence or otherwise of “variation in the structure of variation. ” Interestingly, in experiments designed to test whether natural selection can “break” developmental structuring in the sizes and pigmentation patterns of butterfly wing eyespots, the answer was “yes” for size (Beldade et al. 2002) but “no” for pigmentation (Allen et al. 2008).