Phenotype-first hypotheses, spandrels and early metazoan evolution

Against the neo-Darwinian assumption that genetic factors are the principal source of variation upon which natural selection operates, a phenotype-first hypothesis strikes us as revolutionary because development would seem to constitute an independent source of variability. Richard Watson and his co-authors have argued that developmental memory constitutes one such variety of phenotypic variability. While this version of the phenotype-first hypothesis is especially well-suited for the late metazoan context, where animals have a sufficient history of selection from which to draw, appeals to developmental memory seem less plausible in the evolutionary context of the early metazoans. I provide an interpretation of Stuart Newman's account of deep metazoan phylogenesis that suggests that spandrels are, in addition to developmental memory, an important reservoir of phenotypic variability. I conclude by arguing that Gerd Müller's "side-effect hypothesis" is an illuminating generalization of the proposed non-Watsonian version of the phenotype-first hypothesis.