Evolutionary modiﬁcations of ontogeny: heterochrony and...

q 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3103-0002/$1.00

Paleobiology, 31(3), 2005, pp. 354–372

Evolutionary modifications of ontogeny: heterochronyand beyond

Mark Webster and Miriam Leah Zelditch

Abstract.—Consideration of the ways in which ontogenetic development may be modified to givemorphological novelty provides a conceptual framework that can greatly assist in formulating andtesting hypotheses of patterns and constraints in evolution. Previous attempts to identify distinctmodes of ontogenetic modification have been inconsistent or ambiguous in definition, and incom-prehensive in description of interspecific morphological differences. This has resulted in a situationwhereby almost all morphological evolution is attributed to heterochrony, and the remainder iscommonly either assigned to vague or potentially overly inclusive alternative classes, or overlookedaltogether.

The present paper recognizes six distinct modes of ontogenetic change, each a unique modifi-cation to morphological development: (1) rate modification, (2) timing modification, (3) heterotopy,(4) heterotypy, (5) heterometry, and (6) allometric repatterning. Heterochrony, modeled in terms ofshape/time/size ontogenetic parameters, relates to parallelism between ontogenetic and phylo-genetic shape change and results from a rate or timing modification to the ancestral trajectory ofontogenetic shape change. Loss of a particular morphological feature may be described in termsof timing modification (extreme postdisplacement) or heterometry, depending on the temporal de-velopment of the feature in the ancestor. Testing hypotheses of the operation of each mode entailsexamining the morphological development of the ancestor and descendant by using trajectory-based studies of ontogenetically dynamic features and non-trajectory-based studies of ontogenet-ically static features.

The modes identified here unite cases based on commonalities of observed modification to theprocess of morphological development at the structural scale. They may be heterogeneous or par-tially overlapping with regard to changes to genetic and cellular processes guiding development,which therefore require separate treatment and terminology. Consideration of the modes outlinedhere will provide a balanced framework within which questions of evolutionary change and con-straint within phylogenetic lineages can be addressed more meaningfully.

Mark Webster. Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue,Chicago, Illinois 60637. E-mail: [email protected]

Miriam L. Zelditch. Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109-1079

Accepted: 3 November 2004

Introduction

Ontogeny holds a pivotal place in evolu-tionary biology. Modification of ontogeneticdevelopment (‘‘developmental reprogram-ming’’ [Arthur 2000]) forms a critical link be-tween mutation and selection at any life stage.Comparative studies of ontogeny provideunique windows into evolutionary mecha-nisms, permitting recognition of constraintson morphological evolution and of the proxi-mal processes responsible for evolutionarychange, as well as helping to elucidate phylo-genetic patterns (see Wagner et al. 2000). Notsurprisingly, several attempts have been madeto recognize the modes by which ontogenycan be modified (e.g., Zimmermann 1959;Takhtajan 1972; Gould 1977, 2000; Alberch etal. 1979; McNamara 1986a; Atchley 1987; Re-

gier and Vlahos 1988; Raff and Wray 1989;Wray and McClay 1989; McKinney and Mc-Namara 1991; Sattler 1992; Alberch and Blan-co 1996; Raff 1996; Zelditch and Fink 1996;Reilly et al. 1997; Rice 1997; Klingenberg 1998;Lovejoy et al. 1999; Arthur 2000; Li and John-ston 2000; Sundberg 2000; Smith 2001). In thispaper we present a novel consideration ofmodes of evolution because those previouslyproposed offer incomplete and sometimesconfusing characterizations of ontogeneticmodifications. Confusion arises partly fromapplication of the same terminology for casesof developmental reprogramming identifiedby using morphological and non-morpholog-ical criteria despite evidence that these may bebiologically incommensurate. Additional con-fusion results from poorly defined evidentia-

355MODIFICATIONS OF ONTOGENY

ry criteria demarcating the modes to the pointthat a heterogeneous array of changes can beinterpreted as a single type. Moreover, the fail-ure to entertain a full range of competing hy-potheses means that cases failing to meet theevidentiary criteria of a well-defined mode areassigned to poorly conceived or nonspecifiedmodes, or even ignored. Such conceptual andsemantic confusion has resulted in a strongbias in favor of recognition of some modes ofchange (particularly heterochrony), in theconfounding of heterochrony with other kindsof modification to development, and in a ten-dency to oversimplify the evolution of ontog-eny.

Some workers contend that attempts to re-solve the confusion will only further compli-cate an already excessively verbose literature(e.g., Klingenberg 1998; McKinney 1999).However, we are concerned that the presentframework, if left unrefined, will lead to in-adequate summaries of developmental repro-gramming and a misleading impression of therelative contribution of some of the modes toevolution. We think that the need for a com-prehensive consideration of modes of devel-opmental reprogramming, with explicit cri-teria by which the various modes can be iden-tified and the increased investigative rigorthat this brings, far outweighs the understand-able reluctance to stir once again the alreadymuddied terminological waters of this re-search field.

The present paper aims to reduce confusionabout heterochrony and to expand and refinethe range of hypotheses considered beyondheterochrony. These aims are interrelated, asclearly articulating distinctions among con-cepts and specifying their contrasts helps toreduce confusion. We therefore present a com-prehensive summary of natural modes of evo-lutionary modification of ontogeny relevant tomorphologists.

The Confusion about Heterochrony

Much of the confusion surrounding heter-ochrony can be traced to the application of in-consistent criteria for recognizing the phe-nomenon. Heterochrony has been defined aschanges in developmental rate or the relativetime of appearance of features that ‘‘produce

parallels between the stages of ontogeny andphylogeny’’ (Gould 1977: p. 2). Gould (1977)and Alberch et al. (1979) considered heteroch-rony in terms of morphological criteria (spe-cifically, the decoupling of organismal shape orsize from developmental time) and expressedthe concept in terms of the types of data avail-able to morphologists. Heterochrony was de-tected when, for a given age, the descendanthas a shape typical of the ancestor at a morejuvenile age (paedomorphosis) or at a moremature age (peramorphosis; this could be ahypothetical extrapolation beyond the termi-nal morphology of the ancestor), or retains an-cestral shape but differs in size (dwarfism orgigantism). A nomenclature is in place de-scribing the various ways in which a paedo-morphic or peramorphic descendant can re-sult from an increase (acceleration) or de-crease (neoteny) in the rate at which the tra-jectory of shape change is followed, or from anearly (predisplacement) or late (postdisplace-ment) onset of the trajectory of shape change,or from the early (progenesis) or late (hyper-morphosis) termination of the trajectory ofshape change (Gould 1977; Alberch et al.1979). As well as a nomenclature, there is a for-mal analytic scheme for detecting which ofthese modes of heterochrony occurs in a par-ticular case (Alberch et al. 1979). The fact thatthe evolutionary and ontogenetic vectors ofshape change coincide under this definition ofheterochrony suggests a channeling or con-straint in the direction of morphological evo-lution, which may be significant in terms of re-lating such change to underlying developmen-tal processes.

Heterochrony has been recast in a moremechanistic context, as changes in relative rateor timing of developmental processes (e.g.,Raff and Wray 1989). Application of this con-cept requires direct knowledge of those pro-cesses. This was a significant change in em-phasis: any developmental process has a tem-poral aspect to its operation and thus becomessusceptible to heterochronic modificationwhether or not the process is directly con-cerned with morphological development. Thetwo concepts are not commensurate: casesmeeting the criteria of one definition mightnot meet those of the other (e.g., Raff and

356 MARK WEBSTER AND MIRIAM L. ZELDITCH

Wray 1989; Alberch and Blanco 1996; Raff1996). McKinney and McNamara (1991; alsoMcNamara 1995, 1997) later defined heteroch-rony as ‘‘change in timing or rate of develop-mental events, relative to the same events inthe ancestor.’’ This third definition removesall constraint of morphological parallelism be-tween ontogeny and phylogeny and does notrequire mechanistic knowledge of the process:the only requirement is that an event (howeverdefined) occurs at a different time or that de-velopment proceeds at a different rate in thedescendant relative to the ancestor. When aclass signified by a term is so broadly encom-passing and heterogeneous (‘‘serves too manymasters’’ [Wake 1996]) it can generate confu-sion because its theoretical implications de-pend specifically on which meaning is intend-ed, but the language is presently too impreciseto allow us to specify that meaning.

Not only does heterochrony have variousmeanings, but the criteria for applying it todata are inconsistent as well. For example, toapply Gould’s (1977) definition to data (as for-malized by Alberch et al. 1979) we need anaxis of ontogenetic shape change common toall species under comparison. Hypotheses ofthe operation of heterochrony in this sense canbe accepted only once it is demonstrated thatall interspecific differences are explicable interms of rate or timing differences along thatshared trajectory of ontogenetic shape change.If the trajectory of shape change was not con-served, then parallelism between ontogenyand phylogeny was lost and spatial ratherthan (or in addition to) temporal aspects ofontogeny must have been evolutionarily mod-ified. Modifications to spatial aspects of de-velopment lie within the realm of ‘‘non-het-erochrony’’ (see Alberch 1985). However, cri-teria by which shape is summarized, and bywhich hypotheses of shared trajectories ofshape change are tested, differ among work-ers (see also ‘‘Dimensionality Bias,’’ below).

To exemplify the difficulty of testing the hy-pothesis of heterochrony in light of inconsis-tencies in approach, consider an exampledrawn from a comparison between the pira-nha species Pygopristis denticulata and Pygo-centrus nattereri (Zelditch et al. 2003a) (Fig. 1).The ontogenies of shape for the two species

can be quantified in two ways: (1) the onto-genetic change in geometric shape (estimatedby multivariate regression of geometric shapeon geometric scale; Fig. 1A,B), or (2) the allo-metric coefficients of size measurements (alsoestimated by multivariate regression on bodysize; Fig. 1C,D). Interspecific comparison ofpatterns of shape change involves calculationof the vector correlation between the two on-togenies. On purely intuitive grounds wemight reject the hypothesis of a shared trajec-tory of ontogenetic shape change betweenthese piranha species given the relativelyweak correlation between their trajectories ob-tained from the geometric data (0.332). How-ever, we might find it equally reasonable onintuitive grounds to accept that these speciesare very similar in light of the high correlationbetween their trajectories obtained from thetraditional size data (0.995).

That such a difference in magnitude of cor-relation (and in potential inference about theunderlying biological process) is caused bydifferences in approach to measurement isdisturbing. However, the difference is less-ened when the correlations are subjected tostatistical testing (using a resampling proce-dure detailed in Zelditch et al. 2003b): bothdata sets then reveal significant differences be-tween the ontogenies. The striking contrast inthe correlations estimated from the two datasets results from the different scales on whichthe correlations are estimated. To compare thevalues we need to calibrate them, taking intoaccount the values we would expect betweenrandom vectors. For the geometric data, 1000random permutations of the ontogenetic vec-tor of each species yield average correlationsfor the two species of 0.0125 and 0.0047 (for P.denticulata and P. nattereri, respectively), with95% confidence intervals ranging from 20.322to 0.257 and 20.265 to 0.257. These are the val-ues we would expect from independent vec-tors. In contrast, random permutations of thetraditional morphometric data yield an aver-age correlation of 0.9870 and 0.9921 for P. den-ticulata and P. nattereri, respectively, with 95%confidence intervals ranging from 0.9841 to0.9920 and 0.9891 to 0.9946. The correlationsexpected from independent vectors for tradi-tional morphometric data are strong. Thus, for


FIGURE 1. Ontogenetic trajectories of shape change in two species of piranha, each depicted by using geometricshape data and traditional morphometric measurements. Locations of 16 landmarks selected to summarize shapeof each specimen are shown in top figure (see Zelditch et al. 2003a for details). Differences in the relative positionof homologous landmarks between conspecific specimens of different sizes (developmental ages) can be used toquantify patterns of ontogenetic shape change. A, Ontogeny of geometric shape for Pygopristis denticulata shownas a deformation using the thin-plate spline (Bookstein 1991; see Webster et al. 2001 for a nonmathematical sum-mary). B, Ontogeny of geometric shape for Pygocentrus nattereri shown as a deformation using the thin-plate spline.C, Allometric coefficients for traditional length (inter-landmark distance) measurements of Pygopristis denticulata.Values .1.0 indicate positive allometry (relative to standard body length) during ontogeny; values ,1.0 indicatenegative allometry. D, Allometric coefficients for traditional length measurements of Pygocentrus nattereri. Regres-sion of the full set of partial warps (including the uniform component) from the geometric data, or of the full setof allometric coefficients from the traditional morphometric data, against a measure of geometric scale (centroidsize; see Fig. 3) gives the trajectory of ontogenetic shape change for a species. The degree to which two speciesshare similar patterns of ontogenetic shape change is given by the vector correlation between their respective tra-jectories (the dot product of the ontogenetic vectors, normalized to unit length). The inverse cosine of the vectorcorrelation is the angle between the ontogenies. Ontogenies identical in their patterns of shape change have anangle of 08 between them; larger angles indicate differences in allometric patterning.


both data sets, the interspecific correlation isonly marginally higher than one expectedfrom two random vectors.

Without taking into account the very highcorrelations that can be produced solely bychance when analyzing traditional morpho-metric data, it is difficult to appreciate themagnitude of the difference between the on-togenies. Recognizing that these species arevery different in their trajectories of shapechange is clearly important in light of the def-inition of heterochrony given by Gould (1977)and implicit in its formalization by Alberch etal. (1979). Of course, were we to use the broaddefinition that equates heterochrony to anychange in the slope or intercept of allometriccoefficients (McKinney and McNamara 1991)we would necessarily accept the hypothesis ofheterochronic evolution. We would infer thatP. nattereri is neotenic relative to P. denticulatain those measurements in which it displayslower allometric coefficients (e.g., in postcra-nial depth and posterior lengths), and is ac-celerated in development in those measure-ments in which it displays higher allometriccoefficients (e.g., anterior head depth andlengths). If we followed an alternative conven-tion favored by many workers (e.g., Shea 1985;Wayne 1986), we would infer neoteny or ac-celeration from contrasting changes in posi-tively and negatively allometric coefficients:neoteny predicts that positively allometric co-efficients are decreased whereas negatively al-lometric coefficients are increased. Under amore process-based definition of heterochro-ny (e.g., Raff and Wray 1989) we would haveto conclude that these data are immaterial be-cause they contain no direct information aboutprocess: any attempt to draw a conclusionabout the nature of the change in ontogenywould be regarded as suspect.

Heterochrony in one guise or another hasfrequently been documented in empirical casestudies (indeed, it ‘‘explains everything’’ [Mc-Namara 1997: p. 46]). However, the inconsis-tencies and ambiguities associated with theconcept of heterochrony and its evidentiarycriteria, which almost certainly account forsome of its apparent prevalence, have rarelybeen stressed except in the context of quitemathematical technical issues (e.g., Klingen-

berg 1998; Godfrey and Sutherland 1995,1996). One methodological issue (hereintermed ‘‘dimensionality bias’’) is critical to theidentification of modes of developmental re-programming in general and to the testing ofhypotheses of heterochrony in particular, andyet has been almost entirely overlooked. Thenature and significance of dimensionality biasare therefore now discussed.

Dimensionality Bias: MethodologicallyDetermined Biological Conclusions

The mode(s) of evolutionary changes in de-velopment that can be detected in a particularcase can be limited by the complexity withwhich morphological features are described.When complex morphologies are reduced tosingle dimensions, the variety of modifica-tions that could be discerned is drastically re-duced. We therefore term this ‘‘dimensionali-ty bias.’’

Whether shape data are interpreted as such,or instead reduced to a collection of individ-ual size measurements that are interpretedseparately, is the primary cause of dimension-ality bias. This bias has its greatest effect onthe ability to recognize changes in ontogeneticallometries, and therefore on the ability to re-ject a hypothesis of heterochrony which, fol-lowing the definition of Gould (1977), requiresthat the ancestral pattern of ontogenetic shapechange be conserved in the descendant. If thepattern of shape change itself is evolutionarilymodified, then ancestor and descendant donot share a common ‘‘axis of shape change,’’and their ontogenetic trajectories cannot beplotted on the same shape/size/time plot (Al-berch et al. 1979; Alberch 1985), irrespective ofthe rate at which the taxa progress along theirrespective trajectories or when progressionsalong those trajectories are initiated or ter-minated. However, the degree to which taxaare determined to share the same trajectory ofontogenetic shape change depends on thecomplexity with which shape is summarized.

Shape is inherently multidimensional, andtrajectories of shape change must therefore bequantified by utilizing multidimensional vec-tors (e.g., O’Keefe et al. 1999; Zelditch et al.2000; Webster et al. 2001; Roopnarine 2001;Nehm 2001; also piranha example above and


trilobite example below). Reducing the de-scription of shape to a collection of univariatesize measurements, regressing each indepen-dently against time, and comparing the re-sulting bivariate regression parameters can-not test a hypothesis of heterochrony (nor doc-ument it). ‘‘Heterochrony’’ detected in such away is an artifact of the geometric constraintimposed on the data: one-dimensional dataare constrained in that taxa can differ only in(1) the point at which progress along that di-mension starts or stops, or (2) the rate of pro-gress along that dimension. Any interspecificdifference in such bivariate regression param-eters can be interpreted only in terms of a dif-ference in rate and/or timing, and detection of‘‘heterochrony’’ is methodologically guaran-teed for each measure of size in which the taxadiffer at a given age. (Note that the only evo-lutionarily conserved aspect of ontogeny im-plied by detection of ‘‘heterochrony’’ usingthis methodology is a homologous lengthmeasurement on ancestor and descendant.)

Restricting the morphological coverage tomore localized regions to test for conservedpatterns of shape change on a local scale canproduce a similar bias in favor of interpretingany interspecific differences as heterochrony,in that this often decreases the number ofshape variables and thus the dimensionalityof the analysis. There is no rule dictating howmany dimensions an analysis must includebefore hypotheses of constraint in shapechange (local or otherwise) can be consideredadequately tested. However, when the numberof inferred ‘‘local heterochronies’’ required toexplain the data in terms of modification totemporal aspects of ontogeny alone approach-es the number of variables by which shape issummarized, the data may be more parsimo-niously explained by an alternative hypothe-sis (such as allometric repatterning, discussedbelow).

Dimensionality bias is not unique to themodes of evolutionary change recognizedherein. Rather, dimensionality bias pervadingall previous concepts and classifications ofmodes of evolution has been overlooked, ig-nored, or hidden. Acknowledging the exis-tence of a dimensionality bias does not auto-matically render recognition of modes of evo-

lutionary change futile. Studies using thesame methodology are subject to the same po-tential biases, and their results are directlycomparable. When comparing modes of evo-lutionary change between studies it is there-fore critical to consider dimensionality bias:do observed similarities/differences in evo-lutionary mode result from biological realityor methodological approach? This is especial-ly important when compiling cases to assessthe relative contribution of various modes toevolution (e.g., McNamara 1988).

Beyond Heterochrony

Most workers acknowledge that some evo-lutionary modifications to ontogeny lie be-yond the realm of changes in developmentalrate or timing, and that the nomenclaturalscheme of progenesis, hypermorphosis, pre-and postdisplacement, and neoteny and ac-celeration is incomplete in its description ofevolutionary phenomena (e.g., Alberch 1985;Gould 2000). Various non-heterochronicmodes of developmental reprogramminghave been proposed (see below), but each ispotentially subject to the same problems asthe concept of heterochrony. The problemsplaguing heterochrony are in most immediatedanger of being repeated by the concept ofheterotopy (a change in the topology of de-velopment; Haeckel 1875; Gould 1977; Wrayand McClay 1989; Zelditch and Fink 1996; Liand Johnston 2000). Some workers have con-sidered heterotopy as a modification to spatialaspects of morphological development (e.g.,Zelditch and Fink 1996; Webster et al. 2001).Others have regarded heterotopy as any spa-tial dissociation in development. This is ex-emplified by a statement by Raff (1996: p. 335)who included under heterotopy ‘‘such diverseevents as shifts of gene expression from onecell type or group of cells to another, homeoticchanges, production of serial homologues,production of repeated structures, changes oflocation of structures relative to the body axisor some other frame of reference, and changesin relative proportions of structures.’’ Incom-mensurability of meaning across these scalesis inevitable. The ambiguity in precise defini-tion means that any modification to ontogenyfailing to meet the criterion of heterochrony is


likely to be considered a case of heterotopy,which could devolve into a virtually meaning-less concept (a wastebasket for cases of ‘‘non-heterochrony’’).

To forestall that possibility, we present herea complete consideration of modes of modifi-cation of morphological development (i.e.,modification to the dynamics of morphologi-cal change, and to the distribution of morpho-logical features on the organism). A consid-eration of modes of modification to moreproximal developmental processes mightseem preferable, but a morphological ap-proach has merit in that: (1) morphology rep-resents one direct link between the organismand the surrounding environment and is sub-ject to selective pressures; (2) shared modifi-cations of morphological development may re-flect shared changes in life history; (3) thetypes of observed changes in morphologicaldevelopment can constrain hypotheses re-garding causes at more proximal (mechanis-tic) levels; and (4) it is applicable to specimen-based studies, including paleontological ex-amples.

For each mode recognized here we includea diagnosis that offers unambiguous criteriafor its recognition. Hypotheses of the opera-tion of each mode of modification thereforebecome rigorously testable. We recognize dis-tinct modes of ontogenetic modification ratherthan a continuum with ‘‘pure heterochrony’’and ‘‘pure heterotopy’’ as end-members (con-tra the view taken by Zelditch and Fink[1996]).

Modes of Modification toMorphological Development

Several modes of evolutionary change of on-togeny have been proposed in previous stud-ies, including heterotopy, heterometry, heter-otypy, homeosis, heteroposy, heteromorphy,heteroplasy, novelty, and deviation, in addi-tion to heterochrony (e.g., Zimmermann 1959;Takhtajan 1972; Gould 1977; Regier and Vla-hos 1988; Sattler 1992; Wake 1996; Zelditchand Fink 1996; Gellon and McGinnis 1998; Ar-thur 2000; Li and Johnston 2000; Sundberg2000). These terms refer to modification of on-togenetic parameters such as location (heter-otopy), number (heterometry), type (hetero-

typy, homeosis), and amount/abundance(heteroposy), as opposed to temporal param-eters. Others (heteromorphy, novelty, and de-viation) are defined in terms of what they arenot (i.e., wastebasket classes for cases failingto meet other criteria). Some workers have al-luded to the existence of additional ontoge-netic parameters that may be evolutionarilymodified but did not explicitly identify them(e.g., Atchley 1987; Sattler 1992). This leads touncertainty as to the number of discrete non-heterochronic modes of ontogenetic modifi-cation, with proposals ranging from one(‘‘novelty’’ [Gould 1977]) to a potentially in-finite number (Sattler 1992).

Our characterization of modes (Table 1)achieves comprehensiveness of descriptionwithout recourse to wastebasket classes or un-specified ‘‘phantom parameters.’’ The defini-tions are intended to be more restrictive andrigorous, and therefore of more utility in em-pirical studies. Testing hypotheses of the op-eration of each mode of change entails exam-ining the morphological development of theancestor and descendant by using trajectory-based studies of ontogenetically dynamic fea-tures (i.e., aspects of morphology whichchange during ontogeny; Fig. 1) and non-tra-jectory-based studies of ontogenetically staticfeatures (i.e., aspects of morphology whichcan be considered ‘‘fixed’’ or unchanging dur-ing ontogeny). Although discussed in evolu-tionary terms, the modes also account for her-itable morphological traits differentiatingsubspecies, populations, or dimorphs. Hy-potheses of modification at any taxonomic lev-el must be framed within a defendable phy-logenetic context (Fink 1982, 1988; Jaecks andCarlson 2001).

A comprehensive reexamination of empiri-cal studies in light of the modes recognizedhere is beyond the scope of this paper. Nev-ertheless, it is important to demonstrate theapplicability of the scheme, and so examplesof each of the modes are here cited. In manycases, additional data are required for ade-quate testing of alternative hypotheses as a re-sult of our expanded and refined framework.

Rate Modification: Modification of the Rate ofMorphological Development Relative to Time.This can be detected by plotting the magni-


TABLE 1. Modes of evolutionary modification of morphological ontogeny recognized herein. Dynamic aspects ofmorphological development (i.e., relating to features that change during ontogeny) are susceptible to modificationthrough rate or timing modifications and/or allometric repatterning (depending on whether or not patterns ofshape change are assessed). Static aspects of morphological development (i.e., relating to features that are consid-ered ‘‘fixed’’ or unchanging during ontogeny) are susceptible to heterotopy, heterotypy, or heterometry. See textfor details.

Ontogeneticbehavior oftrait

Aspect of morphologyinvestigated Potential modes of evolutionary modification

Dynamic changes in type, num-ber, location, or size of struc-ture during ontogeny

No modificationRate modificationTiming modification (including deletion)

Dynamic

Ontogenetic shape change

No modificationRate modification (5 rate heterochrony)Timing modification (5 event heterochrony)Rate modification 1 allometric repatterningTiming modification 1 allometric repatterningAllometric repatterning

Location of structure (fixedthrough ontogeny)

No modificationHeterotopy

Static Type of structure (fixed throughontogeny)

No modificationHeterotypy

Number of structure (fixedthrough ontogeny)

No modificationHeterometry (including deletion)

tude of change away from the condition ob-served at the youngest stage against time. Achange in rate is evident as a difference inslope between the regression lines of the an-cestor and descendant when the relationshipbetween development and time is linear, or bychanges in the parameters of a nonlineargrowth model when the relationship is non-linear (see Zelditch et al. 2003b). The aspect ofmorphology under consideration may beshape, size, or the location, number, or type ofparticular elements, but must obviously beontogenetically dynamic if ancestor and de-scendant differ in terms of their rate of change(Table 1). Evolutionary change in the rate atwhich morphological differentiation isachieved during ontogeny represents a ratemodification even when species follow differ-ent ontogenies of shape and so cannot be com-pared by using the Alberch et al. (1979) model(e.g., Zelditch et al. 2003b). Parameters sum-marizing size and net shape change are sug-gested below. For shape data, a rate modifi-cation may be further qualified as a rate het-erochrony (sensu Gould 1977 and Alberch etal. 1979) when the ancestral trajectory ofshape change is conserved in the descendant(because parallelism between ontogeny andphylogeny is then retained, and only temporal

parameters have been modified). An in-creased or decreased rate of shape changethen results in peramorphosis (acceleration)or paedomorphosis (neoteny), respectively.Morphological parameters such as size are of-ten used as a proxy for time (developmentalage), but detection of a rate modification withsuch data does not provide the informationneeded to determine which parameter (mor-phological change or size) has been decoupledfrom the ancestral relationship to time.

Timing Modification: Modification of the Rela-tive Sequence and/or Temporal Spacing of Events inMorphological Development. Examples ofevents would include the appearance of par-ticular anatomical structures or relationshipbetween structures, or discrete ‘‘kinks’’ in thetrajectory of ontogenetic shape change (onto-genetic changes in allometric patterning; per-haps marking entry into a different phase ofdevelopment, including termination ofgrowth if appropriate) (Table 1). The eventsmust be conserved between ancestor and de-scendant: only their relationship to ontoge-netic time is modified (Alberch and Blanco1996). The ontogenetic trajectory can be mod-eled as a linear series of events, arranged ac-cording to the order in which they occur dur-ing ontogeny (Fig. 2). The parameter of inter-


FIGURE 2. Detecting timing modification. In each case,species A is ancestral to species B. A, Timing modifi-cation involving a change in rank order of events. Event4 has been temporally displaced in species B. Note thatno reference to absolute ontogenetic time need be madeto detect the change. B, Timing modification without achange in rank order of events. Event 4 has been tem-porally displaced in species B but to a lesser extent thanin Figure 2A. Absolute ontogenetic time must be knownto detect such a change.

est is the temporal spacing between theseevents during ontogeny. A given event mayoccur earlier or later in the descendant ontog-eny, and can be considered to have been pre-displaced or postdisplaced, respectively, rel-ative to other events. For shape data, a timingmodification may be further qualified as anevent heterochrony (sensu Gould 1977 and Al-berch et al. 1979) when the ancestral trajectoryof shape change is conserved in the descen-dant (because morphological parallelism be-tween ontogeny and phylogeny is then re-tained, and only temporal parameters have

been modified). A later or earlier terminationof an otherwise conserved trajectory of shapechange then results in peramorphosis (hyper-morphosis) or paedomorphosis (progenesis)in the descendant, respectively. Conversely, alater or earlier initiation of an otherwise con-served trajectory of shape change results inpaedomorphosis (postdisplacement) or pera-morphosis (predisplacement) in the descen-dant, respectively.

Timing modification is most evident whenthe temporal order of events is modified in thedescendant relative to the ancestor (Fig. 2A).This can be detected in the absence of absolutetemporal information (Smith 2001) and sug-gests developmental modularity, with non-contingency among the switched events.However, modification to the temporal spac-ing between events can occur without dis-placing one event temporally beyond another,conserving the rank order of events (Fig. 2B).It is then conceivable that constraint is oper-ating: later events may be contingent uponearlier events. Detection of this more subtletiming modification does require absolutetemporal information. (There seems little rea-son to assume that timing modifications re-sulting in a switch in rank order of develop-mental events are always fundamentally dif-ferent from those that modify timing of eventswithout altering their rank order. ThusSmith’s [2001] concept of ‘‘sequence heteroch-rony,’’ which she defined as an evolutionaryswitch in rank order of developmental events,is subsumed within the revised concept oftiming modification.) Timing modificationcannot be inferred from comparison of the rel-ative timing of one event alone in the ancestorand descendant, as any differences detectedcould result from rate modification. The cri-terion that one event is evolutionarily dis-placed differentially relative to another eventis evidence for a timing rather than a ratemodification.

Examples of Rate and Timing Modifications.Many empirical studies have found supportfor ‘‘heterochrony,’’ but rarely do these ade-quately test for evolutionary conservation ofthe ancestral pattern of ontogenetic shapechange. The ‘‘shape data’’ in these studies areoften one-dimensional size axes and thus are


subject to the extreme form of the dimension-ality bias discussed above. Modified rate ofseptal insertion relative to shell size in Car-boniferous ammonoids (Stephen et al. 2002),change in the timing of proximale formationrelative to thecal size in bourgueticrinid cri-noids (Kjaer and Thomsen 1999), change inthe timing of fusion of the scapula and cora-coid relative to attainment of maturity in croc-odilians (Brochu 1995), and modified rates ofcranidial widening, ocular lobe shortening, orglabellar elongation relative to cranidiallength in trilobites (Nedin and Jenkins 1999)therefore support hypotheses of rate or timingmodification but not of heterochrony. Similar-ly, Alberch and Blanco (1996) and Smith (1997,2001) documented several morphological‘‘event heterochronies’’ in vertebrate evolu-tion, but pending investigation of the degreeto which patterns of shape change were evo-lutionarily conserved these examples are bestqualified as timing modifications.

Several studies assess temporal aspects ofmorphological development (often using sizeas a proxy for age) and include considerationof patterns of shape change, and can thereforepotentially detect heterochrony. Rate modifi-cation coupled with allometric repatterning(see below) of body form has been document-ed in piranhas (Zelditch et al. 2000, 2003a) andbetween the rodents Mus musculus domesticusand Sigmodon fulviventer (Zelditch et al.2003b). The trilobite Aulacopleura konincki ex-hibited several morphs differentiated by thenumber of thoracic segments in maturity(Hughes and Chapman 1995). This differenceresulted from delayed termination of segmentrelease from the transitory pygidium into thethorax (and of segment generation at the pos-terior of the transitory pygidium) relative tomorphological development: a timing modi-fication. However, Hughes and Chapman(1995; Hughes et al. 1999) found that the var-ious morphs showed no significant differencein overall mature body proportions despitethe differing number of thoracic segments. Inmorphs with more thoracic segments in ma-turity, each segment was therefore relativelyshorter (longitudinally) than in the morphswith fewer segments. As the pattern of onto-genetic shape change followed by each seg-

ment was modified between morphs, this rep-resented a case of a timing modification withallometric repatterning. Similarly, the loss ofproximale formation in Democrinus maximuswith modification of shape of the basals (Kjaerand Thomsen 1999) represented a rate or tim-ing modification with allometric repatterning.

A case of event heterochrony was recentlydocumented in marginellid gastropods(Nehm 2001). His study demonstrates thatevolutionary conservation of the ancestral tra-jectory of shape change can be detected by us-ing multidimensional morphometric tech-niques. The rigorous criteria by which heter-ochrony is defined (above) can be met by em-pirical data.

Several studies document rate or timingmodification in dynamic aspects of ontogenyother than shape. Evolutionary decrease inthickness (including loss) of the secondary fi-brous shell layer in thecideide brachiopods(Jaecks and Carlson 2001) represented a tim-ing modification, in that the ontogenetic inter-val over which the secondary layer was de-posited was shortened (assuming a constantrate of shell deposition). The decrease in sizeof thecideide brachiopods documented bythese authors represented either a rate or atiming modification (pending age data). Fur-ther examples of rate modification are docu-mented in the trilobite genus Nephrolenellus be-low.

Heterotopy: Modification of the Location of aParticular Morphological Feature. The result isa ‘‘topological shuffling’’ of features such thatnovel proximity relationships are establishedbetween features. Heterotopy can be consid-ered ‘‘morphological ectopy without replace-ment,’’ in contrast to heterotypy (below). Itdiffers from heterometry (below) in that het-erotopy does not affect the number of ele-ments. (This definition of heterotopy is morerestricted than previous definitions [e.g., Raff1996; Zelditch and Fink 1996], which incor-porate cases that are now classified as heter-otypy, heterometry, and allometric repattern-ing.) Heterotopy should be applicable only tomorphological features that are consideredfixed in location once formed (Table 1). If astructure undergoes migration during ontog-eny, then an evolutionary difference in its lo-


cation may alternatively be interpretable interms of temporal modification of the migra-tory path, and/or in terms of repatterning ofthe migratory path.

Examples. The classic case of heterotopy,used by Haeckel in his original formulation ofthe concept, is the shift in germ layer (from theectoderm or endoderm into the mesoderm)from which reproductive organs differentiate,which must have occurred at some point inthe evolution of triploblasts from diploblasts.Heterotopy has also been documented inplants (reviewed in Li and Johnston 2000),typically involving a change in the site of ini-tiation of organ primordia.

Heterotypy: Modification of the Type of Morpho-logical Structure at a Given Location. A mor-phological structure of one type is found inthe descendant in place of one of a differenttype found in the ancestor. Heterotypy shouldbe applicable only to morphological featuresthat are considered fixed in type once formed.Heterotypy can be considered ‘‘morphologi-cal ectopy with replacement’’ or a ‘‘change intype,’’ in contrast to heterotopy (Table 1). Incontrast to heterometry (below), heterotypyinvolves a decrease in number of one type ofstructure for every increase in number of an-other. Heterotypy therefore excludes cases of‘‘homeosis’’ involving a net change in the totalnumber of features.

Examples. Homeotic replacement of onetype of appendage by another in arthropodsrepresents heterotypy. The famous Antenna-pedia and bithorax mutants of Drosophila rep-resent examples of (non-evolutionary) hetero-typic change (Lewis 1978). In Antennapediamutant flies, walking legs develop on the headin place of antennae. In bithorax mutants,wings develop in place of halteres. Similar ho-meotic changes in plants, such as transfor-mation of stamens into petals or petalodia,represent heterotypy (reviewed in Li andJohnston 2000). However, not all documentedcases of homeotic change in arthropods rep-resent heterotypy. Many cases involve devel-opment of appendages on previously non-ap-pendicular segments or loss of appendagesfrom a segment altogether, and so representheterometry in the revised scheme (see be-low). Sundberg (2000) interpreted many as-

pects of trilobite evolution in terms of home-otic change. However, his criterion for home-otic change (‘‘distribution changes of charac-ters among body segments’’) is rather liberallyapplied, and not consistently differentiatedfrom his concept of ‘‘heterochronic’’ change.In our classification, his cases of homeosis arebetter described in terms of rate modification,heterometry, or allometric repatterning (seebelow).

Deposition of an acicular calcitic shell layerin thecideide brachiopods (Jaecks and Carlson2001) represented heterotypy. The acicularlayer was discretely different from other shellmicrostructures, and its deposition was notcontingent upon first depositing the typical fi-brous shell layer (e.g., on the ventral valve ofThecidea radiata). Description of the introduc-tion of the acicular layer in terms of pera-morphic extrapolation of shell microstructureontogeny (going ‘‘beyond’’ the secondary lay-er microstructure) is therefore unsatisfactory.Similarly, the transformation of walking leg tomaxilliped during the ontogeny of Porcellioscaber (Abzhanov and Kaufman 1999) repre-sents a novel heterotypic change introduced ata relatively late ontogenetic stage of this iso-pod (assuming that this transformation wasnot present in the ontogeny of its ancestor).

Heterometry: Modification of the Number of aParticular Morphological Feature. Ancestorand descendant differ in the number of a par-ticular type of feature, without ectopic re-placement, and not reached through trunca-tion or prolongation of the ancestral ontoge-netic trajectory. Heterometry should be appli-cable only to morphological features that areconsidered fixed in number through ontoge-ny. Supernumerary features may develop innovel locations (without replacing existingstructures). Reduction in the number of a typeof feature is simple deletion (loss) and doesnot involve replacement by a different struc-ture.

Heterometry differs from heterotopy in thatheterotopy relates to change in the location ofa given morphological feature on the organ-ism, with no increase or decrease in the num-ber of that feature. Heterometry differs fromheterotypy in that heterotypy relates to a dis-crete change in type of feature at a given site


on the organism (there is no net change in thetotal number of features). Heterometry de-scribes increase or decrease in the total num-ber of features. The requirement that thechange in number cannot be describedthrough truncation or prolongation of the an-cestral ontogenetic trajectory (i.e., the numberis ontogenetically fixed rather than dynamic)serves to differentiate heterometry from rateor timing modification (Table 1). In the case ofcomplete absence of an ancestral morpholog-ical feature from the descendant, knowledgeof the temporal dynamics of the feature in theancestor is therefore critical for distinguishing(deletive) heterometry from (extreme) timingmodification.

The term heterometry was used by Arthur(2000) to describe ‘‘change in amount’’ (simi-lar to Regier and Vlahos’s [1988] ‘‘heteropo-sy’’: a change in the abundance of a develop-mental process). His example of a heterome-tric change was the production of a higherconcentration of BICOID caused by an in-creased rate of transcription in the nurse cells.This would not be classed as heterometry inthe present scheme, as the example is con-cerned with amount of gene product ratherthan morphology (and so belongs at a moreproximal process level).

Examples. Results of the experimental ma-nipulation of the eyeless gene in Drosophila,whereby supernumerary compound eyes de-velop on the antennae, legs, and wings of theinsect (Halder et al. 1995), represent a (non-evolutionary) case of heterometry. Develop-ment or loss of axial nodes on the glabellaand/or thorax of some trilobites (see also casestudy below), described as homeotic changeby Sundberg (2000), represented heterometryas the nodes were added or deleted ratherthan being replaced by another structure. Sim-ilarly, cases of appendage loss or the devel-opment of appendages on typically non-ap-pendicular segments in arthropods (e.g.,Akam et al. 1994; Carroll 1994; Gellon andMcGinnis 1998; Kettle et al. 1999) are de-scribed as heterometry rather than heterotypyin the revised classification.

Allometric Repatterning: Modification of thePattern of Ontogenetic Shape Change. Ancestorand descendant differ in the trajectory of on-

togenetic shape change followed by a struc-ture or the organism (Fig. 1). The parameterof interest is the pattern of shape change fol-lowed by a structure or individual over a spec-ified ontogenetic interval, and is necessarilyontogenetically dynamic (Table 1). The dis-tinction between allometric repatterning andrate or event heterochrony lies in their differ-ent impacts on ratios among allometric coef-ficients: in the case of heterochrony these ra-tios are conserved between ancestor and de-scendant, but in the case of allometric repat-terning they are modified (subject todimensionality bias; see above) and parallel-ism between ontogenetic and phylogeneticshape change is lost. Heterochrony and allo-metric repatterning are therefore mutually ex-clusive categories when assessed for the samemorphological structure (Table 1): they differin terms of constraint or channeling (or lackthereof) along the ancestral ontogenetic trajec-tory, with implications regarding how devel-opment was modified at more proximal levels.

In some cases, difference in form of a ho-mologous structure in the ancestor and de-scendant can be described either in terms ofmodified ontogenetic allometry (allometric re-patterning) or in terms of qualitative differ-ence in type (perhaps defined by function;heterotypy). This is particularly evident incases concerning appendage morphology(e.g., vertebrate forelimb versus hind limb;some arthropod appendages), but is also seenin cases of other features (e.g., brachiopodlophophore support structures; see below).Cases where ultimate interpretation is deter-mined by choice of analytical style are exam-ples of dimensionality bias in a broad sense(above). When the form of one structure can-not be (or is not) described in terms of dynam-ic modification of elements present in another(e.g., changes in shell microstructure or ap-pendage type), then any evolutionary changewill be interpreted as heterotypy. Heterotypicchange can be treated as ontogenetically spon-taneous, whereas difference in form resultingfrom allometric repatterning can graduallydevelop over a longer interval of ontogeny.

Heterometry and heterotopy are distinctfrom allometric repatterning in that they re-late to modification of the number and spatial


distribution of structures on the organism (Ta-ble 1). Allometric repatterning describes thedynamics of shape change (of a structure orthe organism) through ontogeny. Of course,rate or event heterochrony, heterotypy, heter-ometry, or heterotopy in local morphologicalstructures can have a ‘‘shunting’’ effect re-sulting in modification to shape on a moreglobal scale. Wake and Roth (1989; Wake 1996)termed the complex morphological outcomeof a mosaic of heterochronic changes on a localscale (with some traits unmodified) ‘‘ontoge-netic repatterning.’’ If allometric repatterningon one scale is to be fully accounted for bysuch processes on a more local scale, then itshould be possible to demonstrate conserva-tion of ancestral patterns of ontogenetic shapechange at that local scale (subject to dimen-sionality bias, above). Wake (1996) used theterm heteroplasy to describe interspecific dif-ferences in rates of cell proliferation leading todifferences in patterns of allometry. Identify-ing heteroplasy therefore requires knowledgeof process, and the concept lies at a more prox-imal level of investigation. (Not all cases of al-lometric repatterning will ultimately stemfrom modification to the rate of cell prolifer-ation: differences in rate of cell death, cell size,or cell arrangement, for example, would alsolead to allometric repatterning at the structur-al scale.)

Examples. Allometric repatterning hasbeen documented in the evolution of the ce-phalon of the Early Cambrian trilobite Ne-phrolenellus geniculatus from N. multinodus(Webster et al. 2001; see also case study be-low), in the evolution of the piranha generaSerrasalmus and Pygocentrus (Zelditch et al.2000) (allometric repatterning was consideredsynonymous with heterotopy in both of thesestudies), and between the rodents Mus mus-culus domesticus and Sigmodon fulviventer(Zelditch et al. 2003b).

Stephen et al. (2002) documented ‘‘heter-ochrony’’ affecting shell width and diameterin dimorphic Carboniferous ammonoids. Thecompressed morph showed slower increase ineach of these traits relative to the number ofsepta laid down (a proxy for time) in compar-ison to the depressed morph. However, the re-lationship between shell width and diameter

was itself modified (Stephen et al. 2002: Fig.6.1). The rate of increase in shell width was notmodified to the same degree as the rate of in-crease in shell diameter between the di-morphs. A hypothesis of allometric repattern-ing (with rate modification) is more satisfac-tory than one of independent heterochronicmodification to each of the morphological pa-rameters by which shape was summarized.Other examples of allometric repatterningcoupled with rate or timing modificationswere discussed above.

Evolutionary change in the degree of com-plexity of brachiopod lophophore supportstructures (Jaecks and Carlson 2001) high-lights the need to consider methodological di-mensionality bias. If assessed in terms of pat-terns of shape change, then evolutionary mod-ification would have been either through al-lometric repatterning of the ontogeneticdevelopment of the structures (perhaps withrate or timing modification), or through rateor event heterochrony. However, if supportstructure morphology were assessed in termsof a linear progression of ‘‘types’’ (i.e., degreesof complexity), then evolutionary modifica-tion would likely be described in terms of rateor timing modifications (perhaps with heter-otypy, depending on whether the successionof types follows a conserved order). In the lat-ter case, no inference is made regarding con-strained patterns of shape change, and hy-potheses of heterochrony or allometric repat-terning have not been tested.

A Detailed Case Study: MorphologicalEvolution in the Trilobite Nephrolenellus

An empirical case study will serve to dem-onstrate how the modes of ontogenetic mod-ification can be recognized. Trilobites havelong been a source of empirical support forheterochrony in paleontology (e.g., McNa-mara 1978, 1981, 1983, 1986b, 1988; but seeWebster et al. 2001) and it is appropriate thatthe evolution of a Cambrian olenelloid trilo-bite is used as an example.

A strong case can be made for the evolutionof Nephrolenellus geniculatus from its ancestralsister taxon N. multinodus through peramorph-ic heterochrony (Fig. 3) (Webster et al. 2001; asystematic revision of the clade plus formal


FIGURE 3. A, The ontogenetic development of the cephalon (head shield) of the trilobite Nephrolenellus geniculatus(top) and its ancestral sister taxon N. multinodus (bottom). Development of the cephalon of these animals was di-vided into four discrete phases (see Webster et al. 2001), each represented here (size measurement refers to sagittalcephalic length). The distinguishing features of mature specimens (phase 4) of these species are (1) the fewer axialnodes on the glabella of N. geniculatus; (2) the stronger adgenal angle in N. geniculatus; and (3) the absence of apreglabellar field in N. geniculatus. Note that in the ancestral species the axial nodes are progressively lost, theadgenal angle progressively developed, and the size of the preglabellar field progressively reduced during ontog-eny. These facts can be used to make a strong case for N. geniculatus having evolved from N. multinodus by simpleextrapolation of the ancestral ontogenetic trajectory—a case of peramorphic heterochrony (see Webster et al. 2001).B, Morphological terms used in describing the trilobite cephalon. The glabella consists of lobes LO, L1, L2, L3, andLA, separated by furrows. Each of the circles represents a landmark used in the geometric morphometric analysisof cephalic development (Webster et al. 2001). Black circles represent landmarks also used in the analysis of oculo-glabellar development in the present paper. For clarity, landmarks are shown for the right half of the cephalon only.For such geometric data, size of a specimen can be quantified as its centroid size (the square root of the sum ofsquared distances between each landmark and the centroid of the form [Bookstein 1991]).


FIGURE 4. Location of the anteriormost axial node onthe glabella during the ontogeny of N. multinodus (cir-cles, upper regression line) and N. geniculatus (squares,lower regression line). For each specimen, all glabellarlobes posterior to the one indicated bore an axial node.Note the progressive loss of nodes during developmentof each species. See text for details and interpretation.

documentation of the ontogenies of these taxais provided in a forthcoming paper). However,a detailed investigation of the pattern of on-togenetic shape change for the cephalon ofeach species found that the ancestral trajectoryof ontogenetic shape change was not con-served in the descendant. Webster et al. (2001)therefore argued that the evolution of N. gen-iculatus from N. multinodus was better de-scribed in terms of ‘‘spatial repatterning,’’ andthat ‘‘any heterochronic shifts were localizedand of minor importance.’’ Some details of thedevelopment of the oculo-glabellar region(Fig. 3) of Nephrolenellus are now examined inlight of the evolutionary modes discussedabove.

An important feature distinguishing N. gen-iculatus from N. multinodus was the number ofaxial nodes on the glabella through ontogeny.Nephrolenellus multinodus initially bore an axialnode on each lobe of the glabella and pro-gressively lost nodes (in an anteroposteriordirection) during ontogeny (Figs. 3, 4). In ma-turity, nodes were retained on lobes LO, L1,L2, and rarely L3. Nephrolenellus geniculatusinitially bore axial nodes on all glabellar lobesexcept the anteriormost (LA) and progressive-ly lost nodes in the same fashion, retaining anode only on LO (occasionally also L1, ex-tremely rarely on L2) in maturity (Figs. 3, 4).Analysis of covariance (ANCOVA) demon-strates that the rate of node loss (relative to logcentroid size) was significantly different be-tween the species (p , 0.001). This difference

represents a rate modification, but is far froma complete description of the interspecific on-togenetic differences.

Was the increased relative rate of node lossin N. geniculatus part of a more integrated ac-celeration of ontogenetic development? Usinggeometric data, Webster et al. (2001) demon-strated that the pattern of ontogenetic shapechange for the entire cephalon had been evo-lutionarily modified from at least as early asphase 3 of development and (depending onchoice of analytical technique) perhaps as ear-ly as phase 1. Clearly the increased rate ofnode loss relative to size in N. geniculatus wasnot part of a global (cephalic) acceleration ofmorphological development accounting for allinterspecific differences, but is there evidencefor integration on a more local scale? This pos-sibility is now investigated by studying thedevelopment of the glabella in each species.

First, let us examine the rate of glabellarshape change relative to size. Size is quanti-fied as the log centroid size of the oculo-gla-bellar landmark configuration (Fig. 3B) ofeach specimen. Glabellar development hassometimes been quantified by linear measures(e.g., Edgecombe and Chatterton 1987). Rateof glabellar shape change quantified as gla-bella length relative to log centroid sizeshowed no statistically significant differencesbetween N. multinodus and N. geniculatus (Fig.5A; ANCOVA: p 5 0.64). However, when gla-bellar shape change is quantified as Procrus-tes distance away from the average juvenileform, a significant interspecific difference inrate of glabellar shape change relative to sizeis evident (Fig. 5B; ANCOVA: p , 0.001). (Inthis case the average juvenile was specified asthe consensus of all early phase 3 individuals,although results are robust to referencechoice; data not presented.) Again, modifica-tion of the ancestral ontogeny (in terms of rateof development of the glabella relative to size)is described as a rate modification. However,although the rate of node loss relative to sizewas increased, the rate of glabellar develop-ment relative to size was decreased betweenthese taxa.

Assessment of the pattern of glabellar shapechange in each taxon further complicates thesituation. Vectors of glabellar shape change


FIGURE 5. Rate of shape change of the oculo-glabellarstructure as a function of size during phases 3 and 4 ofdevelopment in N. multinodus (circles) and N. geniculatus(squares). A, Using glabella length to summarize shapeof the oculo-glabellar structure. B, Using Procrustes dis-tance (the square root of the summed squared distancesbetween homologous landmarks on two configurationsfollowing Procrustes superimposition [Bookstein 1991])to summarize shape of the oculo-glabellar structure. Aregression line has been fitted for each species. See textfor details and interpretation.

for each species were calculated from thewarp scores following decomposition of athin-plate spline analysis (methods outlinedin Webster et al. 2001; software written by H.D. Sheets available at http://www.canisius.edu/;sheets/morphsoft.html; data availablefrom senior author upon request). Duringphase 3 of development the species showedsignificantly different patterns of glabellarshape change (between-species angle of 648,significantly different to 95% confidence),

mirroring results obtained from study of theentire cephalon (Webster et al. 2001). Duringphase 4 of development high within-speciesvariance rendered a between-species angle of448 statistically insignificant, suggesting con-servation of the ancestral ontogenetic trajec-tory of glabellar shape change during thisphase. (This conservation was local to the gla-bella, because the pattern of shape change ofentire cephalon differed significantly betweenthe species during this phase [Webster et al.2001].)

The description of the evolution of N. geni-culatus from N. multinodus can now be en-hanced by considering the modes of ontoge-netic modification defined above. The evolu-tionary increase in rate of axial node loss rel-ative to size throughout ontogeny was a ratemodification. During phases 3 and 4 of devel-opment the rate of glabellar development rel-ative to size was evolutionarily decreased—also a rate modification but in the opposite di-rection to that describing node loss. The an-cestral pattern of glabellar ontogenetic shapechange was modified through allometric re-patterning during phase 3 in N. geniculatus.However, upon entry into phase 4 N. genicu-latus apparently returned to the ancestral pat-tern of glabellar shape change (although themorphological parallelism between ancestorand descendant was already lost during phase3). It is difficult to determine the extent towhich these localized modifications of glabel-lar development may have been responsiblefor the overall interspecific differences in ce-phalic development (Webster et al. 2001), al-though vectors of landmark movement sug-gest interspecific differences in nonglabellarfeatures (Fig. 6).

One additional noteworthy feature was theabsence of an axial node on the anteriormostglabellar lobe (LA) in the earliest preserveddevelopmental stages of N. geniculatus. Giventhe presence of the node in the earliest onto-genetic stages of N. multinodus, this represent-ed a case of deletive heterometry (above).However, it has been demonstrated that therate of ontogenetic loss of axial nodes relativeto size was higher in N. geniculatus. Absence ofthe node on LA in N. geniculatus may conceiv-ably have resulted from this increased rate of


FIGURE 6. Vectors of cephalic landmark movement dur-ing phase 3 (A) and phase 4 (B) of development of N.multinodus (dashed arrows) and N. geniculatus (solid ar-rows). For simplicity, only the landmarks on the righthalf of the cephalon are shown (see Fig. 3B). Note thatnon-glabellar landmarks show species-specific vectorsof movement apparently independent of glabellar land-marks.

node loss. If this were true, it would be pre-dicted that developmentally younger individ-uals of N. geniculatus (not covered by the sam-ple) would have possessed such a node. Dis-covery of smaller specimens of N. geniculatustherefore has the potential to change the in-terpretation from one of heterometry into oneof rate modification. However, this is unlikelyto happen as the smallest individuals exam-ined are believed to be in the earliest ontoge-netic stage at which a mineralized exoskeletonwas developed. The time at which trilobitesinitiate mineralization of their exoskeleton

provides an unavoidable, preservation-relatedlower limit to knowledge of their develop-ment. This highlights the fact that identifica-tion of the modes by which morphologicalevolution occurred is dependent upon thecompleteness of ontogenetic coverage.

Recognition and accurate characterizationof such a suite of modifications to ontogeny isa necessary step toward linking patterns ofmorphological evolution to changes at moreproximal developmental levels. Much of thecomplexity uncovered in this deceptively sim-ple case would have been unrecognized or as-signed to peramorphic heterochrony underprevious conceptual frameworks. We considerit likely that such complexity in developmen-tal reprogramming will be found to be typicalof morphological evolution, and that casestudies fully explained by a single mode ofmodification will be rare.

Conclusions

Consideration of all the distinct modes ofevolutionary change in development allowsidentification of modified and conserved as-pects of ontogeny. As a result, understandingof the patterns and constraints in evolution isenhanced. In particular, we can recognize farmore than heterochrony, which is sometimesregarded as the dominant mode of evolution-ary change in development (e.g., McKinneyand McNamara 1991; McNamara 1997; Reillyet al. 1997). Recognizing modes of modifica-tion to morphological development offers ascheme applicable to specimen-based studies,which includes the vast majority of paleonto-logical studies (as well as the majority of neon-tological studies).

We recognize six modes of developmentalmodification. Rate modification is a modifica-tion of the amount of morphological changeachieved over a specified interval. Timing mod-ification is a modification of the timing of de-velopmental events and can be independent ofdevelopmental rate. Rate or timing modifica-tion to an otherwise conserved ontogenetictrajectory of shape change can be further qual-ified as rate or event heterochrony, respective-ly. Heterotopy is a change in location of a par-ticular morphological structure. Heterotypy isthe replacement of a morphological structure


of one type by one of a different type at a givenlocation. Heterometry is a change in the num-ber of a particular morphological feature (notattained through replacement or throughtruncation/extrapolation of the ancestral tra-jectory). Allometric repatterning is a modifica-tion of the trajectory of ontogenetic shapechange. Our systematic treatment of thesemodes of evolutionary change in developmentuses clearly defined and consistent evidentia-ry criteria, which should help to reduce theconfusion in the literature. Each of the modesof evolution makes unique and explicit pre-dictions regarding the type of morphologicalchange it engenders, and hypotheses of theiroperation can therefore be rigorously tested.Nevertheless, the degree of morphologicaland ontogenetic coverage, as well as the levelof detail in which morphology is investigated,can affect the type of evolutionary change de-tected. Caution is therefore required whenmaking generalizations regarding the relativecontribution of each mode to evolution.

Although discrete and independent interms of their effects on morphological devel-opment, the modes of evolutionary change arenot necessarily independent in terms of typesof change to cellular and subcellular process-es. We suggest that evolutionary changesbased on such non-morphological criteria willrequire a different terminology in order toavoid unwarranted inference of mechanisticcause and morphological effect (see also Al-berch and Blanco 1996). Utilization of thescheme presented here will allow a thoroughand meaningful investigation of the modes ofmorphological evolution.

Acknowledgments

Our thanks extend to the ‘‘HeteroCronies’’(P. Fitzgerald, R. Guralnick, N. C. Hughes, G.Jaecks, P. Kaplan, D. Lindberg, R. Mooi, R.Nehm, P. Roopnarine, and B. Waggoner), whoparticipated in discussions following the De-veloping Paleontology topical session at theGeological Society of America Annual Meet-ing in Reno, 2000. Morphometrics softwarewas written by H. D. Sheets. Comments by N.C. Hughes, P. M. Sadler, and M. Foote and re-views by S. Carlson, D. Wake, and an anony-mous reviewer helped improve the manu-

script. L. Knox (now L. Webster) helped M.W.retain (some) sanity during the effort to makesense of the heterochrony literature. M.W. wasfunded by National Science Foundation grantEAR-9980372.

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