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Phenotype-first hypotheses, spandrels and early metazoan evolution

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Abstract

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.

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Notes

  1. The distinction between the differences actually present among the individuals in a population and potential or propensity to vary, represented by the possible routes the ball could have followed, corresponds to Wagner’s and Altenberg’s distinction between variation and variability (1996).

  2. There is also the distinct, but related notion of evolvability as used in quantitative genetics, which focuses on the evolutionary potential of populations (Hansen & Pélabon, 2021).

  3. But even here, Newman maintains that genetic accommodation may not have been in every case required. “Some [anatomical distinctions among metazoan body plans]—even the clade-defining ones—may not have initially been genetically determined, but relatively arbitrary ‘frozen accidents,’ alternative morphotypes within evolving populations of organisms for which body plans were still plastic” (Newman, 2016, p. 150).

  4. This said, Love and Lugar flag Mark Webster’s argument to the effect that the fossil record does not unequivocally support the claim that greater initial variation is typically followed by less intraspecific variation in Cambrian lineages (Love & Lugar, 2013, p. 454; Webster, 2007).

  5. In this way, just as the morphologies of the primitive metazoans were responsive to environmental stimuli in a relatively unconstrained way, Gould and Lewontin suggest that the “good design” of modern-day sponges and corals is a function of how their relatively contained liquid tissue form is tuned by the aquatic environments in which they find themselves. The fact that such marine organisms “are well adapted to the flow regimes in which they live” need not be explained by natural selection, but “may be purely phenotypic in origin, largely induced by the current itself” (Gould & Lewontin, 1979, p. 592).

  6. I return to this point in Sect. 3.3.

  7. Alasdair Houston documents a narrow and broad use of the term “spandrel” in biology (2009, p. 227). Where Gould and Lewontin characterize a spandrel as the “necessary byproduct” of an adaptation (Gould, 1997, p. 10, p. 754), George Williams adopts the less restricted view that a spandrel is a “structure arising as an incidental consequence of some evolutionary change” (1992, p. 78). This conception of spandrel as “accident” has also been endorsed by Dennett (1995, pp. 279–280). In the present case I employ the broad use of the term. Thus, in characterizing liquid tissue as a “spandrel,” I am not implying that it is a “necessary byproduct” of a certain mechanism of cellular cohesion, but merely an “accident” or “incidental consequence” of that mechanism relative to its selected effects.

  8. To be clear, while this interpretation is compatible with Newman’s plasticity-first account of early metazoan evolution, he makes no appeal to a “spandrel” or “side-effect” to disentangle the adaptive and incidental products of the toolkit genes. Thus, I cannot be sure if this interpretation would ultimately be met with his endorsement.

  9. I’m speaking loosely here. While, as a general rule, spatially and temporally proximal causal relationships tend to be more invariant, as Woodward points out, proximal causal relationships can lack invariance or be “sensitive” to interference and distal relationships can be relatively invariant (Woodward, 2010, pp. 294–295).

  10. Except for the Labridae fish family.

  11. This posit is a simplifying assumption. In fact, the decoupling is likely just another biomechanical side-effect of a different selected effect of a mutation.

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I am grateful for the especially insightful feedback I received from the two reviewers of this journal.

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The author is grateful to Stetson University for providing financial support for this project in the form of a sabbatical leave.

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Rust, J. Phenotype-first hypotheses, spandrels and early metazoan evolution. HPLS 44, 48 (2022). https://doi.org/10.1007/s40656-022-00531-w

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