Abstract
Stephen Jay Gould argued that replaying the “tape of life” would result in a radically different evolutionary outcome. Some biologists and philosophers, however, have pointed to convergent evolution as evidence for robust replicability in macroevolution. These authors interpret homoplasy, or the independent origination of similar biological forms, as evidence for the power of natural selection to guide form toward certain morphological attractors, notwithstanding the diversionary tendencies of drift and the constraints of phylogenetic inertia. In this paper, I consider the implications of homoplasy for the debate over the nature of macroevolution. I argue that once the concepts of contingency and convergence are fleshed out, it becomes clear that many instances of homoplasy fail to negate Gould’s overarching thesis, and may in fact support a Gouldian view of life. My argument rests on the distinction between parallelism and convergence, which I defend against a recent challenge from developmental biology. I conclude that despite the difficulties in defining and identifying parallelism, the concept remains useful and relevant to the contingency controversy insofar as it underscores the common developmental origins of iterated evolution.
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Notes
Gould invokes this thought experiment in an attempt to answer the following question: is the clumpy distribution of organismic form in an otherwise vast and uncharted ‘morphospace’ the result of predictable optimizing processes, or is it the contingent upshot of quirky, unpredictable events which took place early in the history of life? (2002, 347). Contrary to the Panglossian view that selection has produced the best of all possible functional worlds, Gould interpreted the constellation of actual forms as a “subset of workable, but basically fortuitous, survivals among a much larger set that could have functioned just as well, but either never arose, or lost their opportunities, by historical happenstance” (1160–1161).
Although Gould framed the RCT in exceedingly broad terms (e.g., as applying to “every interesting event of life’s history”), the crux of the debate turns on the counterfactual resilience of the large-scale morphological contours of animal life (Gould 1989, 209). I will therefore not consider whether the same framework can be applied to different levels of biological organization, or to other important investigative questions.
By “effectively random,” I simply mean for reasons unrelated to adaptation, fitness, or natural selection.
The phenotypic effects of mutations in developmentally ‘upstream’ components are rarely linear or modular; in many cases damage to the phenotype includes not only the structures that are directly implicated by the mutation, but ‘collateral’ traits as well (Thattai and van Oudenaarden 2001).
First, although Gould never abandoned the idea that there are important philosophical lessons to be drawn from the Cambrian fauna, it has become increasingly clear over the years that a number of these ‘bizarre’ taxa are less phylogenetically problematic than they initially appeared to be, many turning out to be stem groups of otherwise familiar phyla (Budd 2001; see also Conway Morris and Gould 1998). Note, however, that even if this turns out to be the case, it does little to advance the opposing robust repeatability thesis, since as a selectionist account of Cambrian survivorship the latter requires that alternative body plans arose in the Cambrian and were actively eliminated by selection (see further discussion below). Second, contrary to the refractory development thesis, there is a surprising degree of developmental robustness due to canalization, buffering, and dominance mechanisms all of which tolerate genetic perturbation (Wagner and Schwenk 2000); it bears mentioning, however, that at least some of the observed canalization may be due to stabilizing selection on entrenched developmental pathways (Gibson and Wagner 2000).
The RCT and the RRT represent opposing ends of what is surely a continuum of views on the balance of chance and necessity in the history of life. In structuring the discussion along these antithetical positions, the aim is not to foster the conclusion that biologists have coalesced into two competing factions for purposes of the contingency controversy; rather, it is to set up the dialectical space necessary to evaluate in tandem a key concept (contingency) and a central data set (convergence), both of which take center stage in the debate between Gould and some of his staunchest critics. Where I refer to the ‘contingency debate,’ I mean the well-publicized clash (e.g. Conway Morris and Gould 1998) of these rather extreme views of life.
The probability that complex functional-morphological regularities could be underwritten by stochastic processes, such as drift, mutation or recombination, is astronomically small (Sober 2005). Apart from natural selection, the only mechanistic account of the evolution of biological complexity is due to structuralism, a school of theoretical biology that attributes independent similarity not to the supremacy of selection, but to non-functional laws of complexity (e.g. Goodwin 2001). Even if it were true that biological systems could achieve a certain degree of order “for free” (i.e. in the absence of selection), structuralist theories would still fall short of the mark when it comes explaining the origins of complex adaptive functions, or the exquisite match between organisms and the ecological design problems they need to solve.
For example, consider the impressive suite of convergent ‘saber-toothed lion’ morphology shared by placental and marsupial mammals. If the saber-toothed outcome depends on the existence of mammalian or (even more generally) vertebrate cranial structure, and if the evolutionary proliferation of either the mammalian or vertebrate musculoskeletal configuration is highly contingent because it depends on non-replicable antecedent events that occurred in the Triassic and Cambrian (respectively), then this outcome will fail to support the RRT.
The botanist H.C. Watson criticized Darwin for focusing almost exclusively on the pattern of divergence and underestimating the evolutionary importance of convergence. In a letter to Watson dated January 1860, Darwin replied as follows: “With respect to ‘convergence’ I daresay, it has occurred, but I should think on a very limited scale, owing to the strong principle of inheritance” (Burkhardt et al. 1993, 18).
An example of systematic homoplasy relates to lamnid sharks and tunas, which share not only a distinct body shape, but also a derived muscular architecture and a fine-tuned force-transmission system (Donley et al. 2004).
Note, however, that among large groups of taxa with small numbers of traits, a certain degree of convergence is to be expected even in the absence of adaptation or constraint (Stayton 2008). By contrast, convergence on complex characters with large numbers of variables is much more rare and likely to be the result of adaptation.
The subject of macroevolutionary contingency is also discussed in Sterelny and Griffiths (1999).
Note that chaotic systems may be characterized as metaphysically deterministic, even if their tendency to magnify arbitrarily small differences in initial conditions makes predicting their behavior impossible in principle. Any two deterministic systems with metaphysically identical initial conditions cannot give rise to disparate outcomes, even if they are truly chaotic and regardless of any epistemic difficulties we might have in specifying their initial values with absolute precision.
We need not limit the definition of radical contingency to situations in which arbitrarily smaller changes in boundary conditions will always lead to greater differences in outcome, as might be expected for truly chaotic systems.
Notwithstanding the dichotomous nature of the debate between Gould and some of his critics, macroevolutionary contingency will admit of degrees, depending on (1) the overall proportion of initial conditions on which the outcome is sensitively dependent, (2) the smallness of the perturbations in initial conditions that tend to yield a disparate outcome, (3) the extent of outcome disparity, and (4) the degree of subsequent developmental entrenchment following the initial period of radically contingent dynamics. Unfortunately, this account of contingency is full of ambiguities that make it difficult to operationalize and hence to test. Two problems stand out in particular: what sort of a change in initial conditions should constitute a ‘marginal’ one, and what kind of similarity metrics should be used to assess outcome disparity? Defining and measuring body plans has proved extremely difficult if not intractable, leading some authors to question the methodological viability of Gould’s thesis. These difficulties, which cut equally against the RRT, are akin to those that confound attempts to quantify the ‘degree’ of convergence over which there is little consensus (see e.g. Stayton 2008). Furthermore, as the above points suggest, the vindication of the RCT (or RRT) turns, like many evolutionary theses, on the outcome of a relative significance dispute. In adjudicating between competing views of life, it is not sufficient that we identify some pockets of radically contingent or robustly replicable dynamics, since these overarching theses require that the patterns they describe dominate the history of life. Any thoroughgoing account of the relationship between contingency and convergence requires that these daunting conceptual and methodological hurdles be overcome.
That being said, given his theoretical emphasis on mass extinction, Gould would probably view radical contingency as characterizing later periods of animal evolution as well, even if such dynamics are not ubiquitous throughout the Phanerozoic range. Gould was particularly interested in the patterns of faunal turnover in the wake of mass extinctions that punctuate the fossil record. He believed that survivorship patterns during pulses of catastrophic extinction were generated either by truly random sampling of the biota, or (more frequently) by the episodic imposition of different rules governing clade survivorship (2002, 1314). In either scenario, mass extinction does not amount to a mere intensification of the ordinary ‘background’ mechanisms of extinction (cf. Jablonksi 2002). When previously dominant taxa are removed by mass extinction, otherwise improbable lineages can radiate into the emptied eco-space, as did the mammals after the sudden extermination of Dinosauria. And if Gould’s ‘decimation-diversification’ hypothesis (1989, 216) is correct, then the shape of life may be highly (if not radically) contingent on these clade-level bouts of non-Darwinian sampling, since post-mass extinction diversification would be confined to the body plans of surviving higher taxa due to internal constraints (as described in Section 1). Over deep time, mass extinctions whittle down the breadth of morphospace occupation, leaving increasingly large and unbridgeable morphological gaps between the remaining groups.
Here I am following Amundson’s (1994) helpful distinction between internal and external constraints on the evolution of form. Broadly speaking, internal constraint refers to “biases on the production of variant phenotypes, or limitations on phenotypic variability, caused by the structure, character, composition or dynamics of the developmental system” (Wagner 1988, 46). External constraint, on the other hand, refers to limitations imposed by the optimizing agency of natural selection working to solve ecological design problems within the confines of the chemico-physical laws.
Anolis ecomorphs vary predictably in features such as limb-length, skull dimensions, and other traits relating to predator escape and foraging ability. For instance, species occupying open habitats tend to have long legs for increased sprinting ability, while those inhabiting branches have shorter appendages that increase their maneuverability in this specialized adaptive zone. Despite their considerable morphological disparities, all within-island populations of lizards are phylogenetically closer to one another than to any inter-island population.
To date little is known about the developmental biology of Anolis lizards, and specific genes associated with changes in hind-limb development, skull morphology, skin pigmentation, and other traits that comprise the various ecomorphologies have yet to be identified. Nevertheless, researchers believe that key developmental homologs exist and will ultimately form a crucial part of any synthetic explanation of anole radiations (Sanger et al. 2008).
Pearce (in press) rightfully criticizes my earlier work on this point.
For example, the amino acid polymorphism Mc1r, which is associated with pigmentation gain in various mammal clades ranging from beach mice to wooly mammoths, is bound up with various non-homologous gene networks that are equally necessary for production of the trait in each group. Even if an important sequence such as Mc1r is shared, the proximate developmental pathways of any given homoplasy may be largely non-homologous.
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Acknowledgement
I am grateful to John Beatty, Alex Rosenberg, V. Louise Roth and several anonymous referees for helpful comments on an earlier draft of this manuscript.
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Powell, R. Convergent evolution and the limits of natural selection. Euro Jnl Phil Sci 2, 355–373 (2012). https://doi.org/10.1007/s13194-012-0047-9
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DOI: https://doi.org/10.1007/s13194-012-0047-9