If allometric ontogenies establish channels of positive constraint, then heterochrony supplies a convenient and effective mechanism for evolutionary utilization. By selective acceleration or retardation of single traits, small to large complexes of correlated characters, or even entire phenotypic stages, heterochrony can differentially extend or compress features across ontogenetic trajectories, and can also “mix and match” the characteristics of several stages into a transformed phenotype. (Contrary to a popular impression, for example, the evolutionary power of progenesis does not lie in full “promotion” of a functioning larva to sexual maturity, but rather in the almost invariable, and sometimes adventitiously beneficial, combination of characters that progenesis yields — with some features “left behind” in the early ontogenetic stages appropriate to the truncated age of sexual maturation, and others accelerated to appear in a phenotypically more adult form through correlation with the early achievement of sexual maturity — see Gould, 1977b.)
For these reasons, heterochrony has long been a favored concept among evolutionists searching for mechanisms to accelerate evolutionary rates in complexes of characters — for simple changes in “rate genes” (to use Goldschmidt's old phrase) [Page 1039] may yield extensive consequences for entire organismal phenotypes, as suites of correlated characters change in concert with altered rates of development. Thus, with strongly allometric ontogenies as favored channels, and with heterochrony available as a mechanism to move sets of characters quickly along these channels, organisms often meet both classical criteria — channeling and speed — for utilizing constraint as a positive accelerator of evolutionary change.
For these and other reasons, the subject of heterochrony has generated a long, memorable and voluminous literature (see De Beer, 1930 for the classic 20th century statement; Gould, 1977b, for a historical and then-current summary; and McKinney, 1988, McKinney and McNamara, 1991, and McNamara, 1997, for subsequent views). In a later summary, McKinney (1999) notes that three major themes have marked the fruitful use of heterochrony within macroevolutionary studies in recent years: heterochronoclines (or trends caused by temporal displacements of developmental rates), heterochronic biases within clades, and the origin of novelties.
In summarizing the extensive literature on heterochronoclines, McKinney emphasizes the same point stressed here — heterochrony and allometry as convenient and available mechanisms, whereby selection can accelerate and intensify adaptive change (making positive constraint a “partner,” not an “antagonist,” of selection in many cases). He writes (1999, p. 150): “Heterochronic variation is a very rapid, easy way to produce coadapted suites of traits. It makes sense that simple extrapolations (or truncations) of major environmental parameters (such as water depth, sediment size and temperature) could select for relatively simple extrapolations (or truncations) along the ontogenetic trajectory of a population (= cladogenesis) or species (= anagenesis).”
The frequency of neoteny in salamanders, potentiated by unusual ease in dissociation of sexual maturation from somatic development, represents the classic case of heterochronic biases. In another sensible correlation of positive constraints in heterochrony with adaptive utility, Whiteman (1994) demonstrates that amphibian paedomorphs generally arise when the aquatic habitat of larvae becomes more productive, or more stable, than the terrestrial environment of adults. At a larger scale, and in an intriguing macroevolutionary speculation, McNamara (1997) surveys the known examples of heterochrony among trilobites, and finds that paedomorphosis predominates in Cambrian lineages, while the opposite processes of peramorphosis seems to gain the higher relative frequency in later Paleozoic lines. McNamara wonders if this pattern might not reflect changes in the organization and activity of homeotic genes in times of evolutionary turmoil in and after the Cambrian explosion vs. the relative “calm” of the later Paleozoic evolutionary world.
For the third theme of evolutionary novelties, the classic literature has stressed the role of global paedomorphosis, usually in the progenetic mode (as noted in Gould, 1977b), in shedding the “excess baggage” of adult complexity and reverting to the more labile phenotypes that often characterize juvenile forms — an “escape from specialization” in the classic description. Such [Page 1040] examples of “wiping the slate clean” may explain the origin of some major groups (see Mooi, 1990, on sand dollars among echinoids), but McKinney (1999) rightly points out that an even more powerful, and almost surely more frequent, heterochronic boost to the origin of novelties may lie in the potential for what I previously called the “mix and match” of characters produced by varying modes of heterochrony in different features and complexes within the same organism.
As a poor and parochial surrogate for adequate review of an immense literature, I limit myself to two examples from my own research that have enlightened me about the evolutionary implications of positive constraint in this allometric and heterochronic form.
The two structural themes of internally set channels and ease of
transformation as potentially synergistic with functional causality
by natural selection: increasing shell stability in the Gryphaea
heterochronocline
In quantitative studies of fossil invertebrates, no case has commanded nearly so much attention as the evolution of coiled Jurassic oysters of the genus Gryphaea in the British Isles (see Trueman, 1922 for the classic statement). I collected only the major papers of this debate into a full book (Gould, 1980f), while a volume of equal extent has been published since then, leading to what I regard, with obvious self-serving bias, as a genuine solution in Jones and Gould (1999). I will not discuss earlier errors and struggles (see Gould, 1972, for a compendium), and will simply note a consensus reached by the 1970's — that the complete lower Jurassic sequence from Gryphaea incurva to Gryphaea gigantea features a basic trend in a set of phyletically correlated characters, including substantial increase in body size, decrease in coiling, and increasing relative width of the valves.
These trends, at least in a descriptive sense, certainly seem to embody the heterochronic result of paedomorphosis, as all sustained changes in form led to progressive juvenilization in adult phenotypes of later phylogenetic stages (Fig. 10-1). The strong allometry of increased coiling through ontogeny permits an easy identification of this trend, as larval shells cement briefly to a hard object, with the young organism then breaking free and coiling throughout life on a muddy substrate. Juvenile lower valves (after breaking their initial cementation) therefore begin growth as relatively flat, and then coil progressively throughout life. The phyletic trend to flattening strongly resembles a progressive excursion to earlier and less coiled stages of ontogeny.
But this descriptive consensus remained stymied by a common technical problem in heterochronic studies within paleontology. The causal distinctions within heterochrony can only be specified with reference to the chronological age of specimens, and few fossils record the months and years of their growth in a recoverable manner (see discussion of this dilemma in McKinney and McNamara, 1991; and Jones and Gould, 1999). Without information about the age of specimens, we could not tell whether increasing body size simply [Page 1041] represented a chronological extension of the life cycle (with juvenilization of form then unresolvable in mode of origin), or an increase in rates of growth over an unchanged length of life (with the paedomorphic result then attributable to the heterochronic process of neoteny based on prolongation of rapid juvenile growth rates and attendant retention of characteristic morphologies associated with these rates).
I had the privilege of working with Douglas Jones, who developed the first reliable procedures for inferring ages from growth banding (by matching isotopic cycles, interpreted as seasonal, with morphological banding, Fig. 10-2 — because simple counts of banding, the standard procedure of past sclerochronological study, had never yielded firm results). We were able to break this conceptual logjam by determining the ages
of shells throughout the trend (Jones and Gould, 1999), and resolving the problem, thanks to unusual cooperation from nature (who rarely provides clear answers at one extreme of a potential continuum). The larger adult shells of later phylogenetic stages showed no increase at all in length of life, but died at the same age as adult shells in the earliest stages in the trend (Fig. 10-3). Thus, we could identify the correlated phenotypic trend in size and shape as a genuine case of neoteny
10-1. Paedomorphosis in lower Jurassic Gryphaea. The left sequence (top to bottom) shows ontogenetic stages of the ancestral species drawn at the same size as adults of the phylogenetic series (the right sequence, bottom to top). From Gould, 2000e; adapted from Hallam.
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10-2. Determination of age of individual Gryphaea shells by oxygen isotope profiles across annual growth increments. Solving this problem of sclerochronology allowed us to determine, for the first time, the actual mode of heterochrony in Gryphaea. From Jones and Gould, 1999.
10-3. Increase in shell size (measured as shell height) in the phyletic sequence G. arcuata to G. gigantea. Although the shells augment markedly in size, this increase does not reflect longer periods of growth as descendants are larger at each comparable age, and the average adult descendant dies before reaching the final age of the average adult ancestor. From Gould, 2000e.
(Fig. 10-4), using the allometric channel of Gryphaea's ontogeny to evolve a broader and less coiled adult shell in later stages of the sequence.
When we combine this structural analysis of the evolutionary trend with a well-documented scenario for its adaptive basis, the positive aspect of constraint as an adjunct to selection stands forth in an unusually clear manner. The environmental correlation of flat and cemented Ostrea with clear waters and hard substrates, and of coiled and free-living Gryphaea with muddy substrates,
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10-4. Evidence of neoteny for the same sequence of G. arcuata to G. gigantea as measured by increasing juvenilization of form in the increasing length to height ratio — implying that descendant adults become less coiled and therefore more like the flatter juvenile shells. Our analysis of absolute ages for each shell allowed us to specify this case of paedomorphosis as neotenic. From Gould, 2000c.
establishes a long-enduring, iteratively-evolved pattern demanding functional explanation. The adaptive value of coiling in Gryphaea has long been ascribed with much evidence in support (see Hallam, 1968, p. 119) and little dissent among experts, to the animal's need to keep the shell commisure above the muddy substrate, lest the shell become entombed or clogged, leading to the animal's death.
Coiling represents an excellent morphological means — presumably the best available given the limitations of bivalved molluscan design — for continually raising the commisure above the substrate as the shell grows. But coiling, particularly if intensified in a relatively narrow shell, also entails the negative consequence of increasing instability, for a narrow object, shaped like the rocker of a hobby horse, can easily be tipped over from its presumed upright life position (see Fig. 10-5, with the plane of bilateral symmetry orthogonal to the substrate). In fact, in highly coiled Gryphaea, a shell tipped over onto its side (Fig. 10-6) lies in a position of greater stability than a shell in this presumed, and only viable, life orientation. Some early German paleobiologists, after discovering this fact from hydrodynamic experiments, actually postulated that Gryphaea might have lived in such a side-down position. But Hallam (1968) and others argue convincingly that a shell on its side would soon become clogged with mud, rendering the animal unable to feed. Moreover, once the heavy shell is tipped, the animal cannot right itself — so quick death would seem to follow as an inevitable consequence of such displacement from the bilateral living position.
We therefore assume that stabilization of a shell that must coil to rise above a muddy substrate represents a fundamental functional problem for gryphaeate oysters. (Indeed, the most strongly coiled Gryphaea incurva, the ancestral state of the Jurassic sequence, developed an especially thickened lower valve, presumably to gain stability by ballasting such a non-optimal form.) [Page 1044]
Hallam's persuasive flow tank experiments (1968) identified the morphological changes that could provide greater shell stability in an evolutionary lineage beginning with the problematical G. incurva: namely, larger size, broader shells, and decreased coiling. The evident conclusion now simply follows: if natural selection favored all these traits as conjoined enhancers of essential stability, wouldn't its action be greatly aided by any internal mechanism that happened to bias variation in these directions, or to forge correlations among these jointly beneficial characters?
Fortunately, all the morphological features already exist within the ontogenetic (and strongly allometric) channel of the founding member, G. incurva — for young shells of this ancestral species are relatively broader and less coiled than the adults that will develop from them. If these features can be brought forward by paedomorphosis into later ontogeny, greater stability can be achieved.
10-5. The life position of Gryphaea, with the implied adaptive advantage of coiling in keeping the aperture of the shell above the muddy surface. From flow channel experiments of Hallam, 1968.
10-6. A Gryphaea shell tipped onto its side — an inviable position — is actually more stable than a shell in its life position of Figure 10-5. From Hallam, 1968.
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Heterochrony now seals the case and intensifies the joint benefit. Neoteny often operates through a correlation of juvenile form with rapid growth rates of the young organism. If these rapid rates can be prolonged into later ontogeny, then juvenile form can also be “promoted” to the adult stage — and the adult shell will also increase substantially in size (at any age in common with ancestors). Thus, as an automatic consequence of heterochronic correlations, working within a pre-set allometric channel of ancestral ontogeny, all three adaptive desiderata for greater shell stability can evolve in tandem as consequences of a single focus of selection — that is, for prolongation of rapid juvenile growth rates. By thus linking all the valued characters, and evoking their common expression by one basic developmental change, positive constraints work synergistically with natural selection to produce an apparently complex set of adaptive changes with relative ease and speed.
Ontogenetically channeled allometric constraint as a primary
basis of expressed evolutionary variation: the full geographic and
morphological range of Cerion uva
Since snail shells preserve a complete record of ontogeny in a unitary and rigid structure that generally cannot be modified after initial formation (at least in exterior expression, whereas the shell interior can often be altered through secondary resorption and deposition by appressing soft tissues), this taxon presents unusual opportunities for the study of developmental constraints. Evolution in any character, whether caused by selection or not, must automatically elicit a suite of correlated responses throughout such an integral and integrated structure.
However, the isometric growth model of the logarithmic spiral, so often assumed to apply to the actual growth of most mollusks will greatly limit the expression of such constraints based on “correlations of growth” (Darwin's own phrase), because such a logarithmic shell does not change its shape through ontogeny (D'Arcy Thompson, 1917), and heterochrony therefore loses its power to alter the form of descendants by general retardation or acceleration — for the juvenile shell looks just like a scaled-down adult, and global paedomorphosis, for example, would therefore exert no effect upon form. But when shells grow with pronounced allometry, then positive channels of constraint attain great potential for influencing or directing the evolution of phenotypes (as expressed in a complex, rigid structure, preserving a complete and unaltered record of ontogeny, where any change must elicit a cascade of correlated consequences, and where strong allometries establish a rich playing field for effective heterochrony).
I have used inductive multivariate biometry to identify, and then to judge the extent of influence for groups of ontogenetically correlated characters (“covariance sets” in my terminology) that are both mechanically enforced by allometric growth, and that also exert substantial, often controlling, impact upon patterns of temporal and geographic variation in the phenotypic history of species. These covariance sets usually dominate several major axes of orthogonal variation detected in such techniques as factor and discriminant analysis (see Gould and Woodruff, 1986, for a detailed application; Gould, 1989a, for a general statement; and Gould, 1992b, for an analysis of the infamous “square snails” in the Cerion dimidiatum complex of Cuba, a phenotype that Maynard Smith had declared “impossible” at the 1980 Chicago macroevolution meeting in order to acknowledge that even he, as a strict Darwinian, did not deny a role for constraint in precluding access to certain regions of morphospace. His principle cannot be gainsaid, but his application failed because he assumed a logarithmic spiral model, thus forbidding the square shape that can be attained only by intense allometry; but Cerion's allometry leads precisely to such squareness at the extreme of contrast and sudden transition between allometric phases one and two).
The Structure of Evolutionary Theory Page 166
