Comparing the differential filling of morphospace and allometricspace through time: the morphological and developmentaldynamics of Early Jurassic ammonoids

Sylvain Gerber

Abstract.—The evolutionary history of shell geometry of Early Jurassic ammonoids during thePliensbachian–Toarcian second-order mass extinction is explored at both adult and ontogenetic levels.The ontogenetic approach builds on the concept of allometric space to get insights into thedevelopmental aspects of morphological evolution. Investigation of the deployment of taxa in adultmorphospace and allometric space allows the appraisal of the temporal evolution of morphologicaland allometric disparities. Curves of taxonomic diversity, adult morphological disparity, allometricdisparity, and average adult size are contrasted. Results show that during the Pliensbachian–Toarcianinterval, ammonoids underwent two successive and drastic declines in taxonomic diversity. Patternsof morphospace and allometric space occupancy suggest nonselective extinction at both morpholog-ical and developmental levels. Another measure of allometric disparity suggests the occurrence of twoheterochronic trends, a peramorphocline followed by a paedomorphocline, during the Toarcian.These trends are concomitant with changes in average adult size that compensate for theheterochronic effects and explain the striking stability of morphological disparity despite changesin diversity. The results also emphasize the existence of two contrasted evolutionary dynamics inPliensbachian and Toarcian ammonoids. Methodologically, the allometric disparity approach appearsto be a fruitful tool to analyze the rather understudied clade-wide ontogenetic aspects ofmorphological evolution. Combining multiple approaches to describe clade morphological dynamicsleads to a better characterization and understanding of the diversity-disparities relationships and abetter distinction of the potential processes driving these macroevolutionary patterns.

Sylvain Gerber. Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue,Chicago, Illinois 60637

Present address: Department of Biology and Biochemistry, University of Bath, Claverton Down, BathBA2 3LR, United Kingdom. E-mail: s.gerber@bath.ac.uk

Accepted: 31 December 2010

Introduction

Following their near complete extinction atthe Triassic/Jurassic boundary, the ammo-noids of the Early Jurassic underwent a phaseof recovery and radiation from one or fewsurviving phylloceratid genera. This periodopens the fourth and last chapter of ammo-noid history finally concluded by the end-Cretaceous extinction events. In greater detail,the evolutionary dynamics of early Jurassicammonoids appears to consist in complexphases of temporal and geographic diversifi-cation. These large-scale patterns have beendescribed in taxonomic terms, as well asenriched with quantitative analyses of tem-poral changes in morphospace occupation(morphological disparity [Dommergues et al.1996, 2001]) and body-size range variations(scalar disparity [Dommergues et al. 2002]).Despite this morphological focus, the ontoge-

netic dynamic of ammonoids and its potentialrole in the group’s evolutionary history havenever been investigated at such scales. Onto-genetic aspects of morphological evolutionhave only been explored at the lineage level,through several independent heterochronicstudies always confined to relatively smallsets of related taxa (Dommergues et al. 1986,1989; Marchand and Dommergues 1988;Dommergues and Meister 1989; Landman etal. 1991). This lack of explicit incorporationand quantitative characterization of the onto-genetic dimension of taxa in large-scalestudies is a general problem that unfortunate-ly holds for most biological groups. It likelyresults from the relative difficulties in (i)gathering ontogenetic data in studies involv-ing large numbers of taxa, (ii) providing thedetailed phylogenetic framework at hightaxonomic levels that ensures the reliability

Paleobiology, 37(3), 2011, pp. 369–382

’ 2011 The Paleontological Society. All rights reserved. 0094-8373/11/3703–0003/$1.00

of evolutionary developmental changes hy-pothesized in ancestor-descendant transi-tions, and (iii) devising proxies that couldhelp characterize the ontogenetic dynamics oftaxa at the clade level. As a consequence,emphasis is usually given to external bioticand abiotic factors to explain the macroevo-lutionary patterns observed. However, theadult stage—the usual target of phenotypicstudies—is only the last snapshot of theindividual ontogeny and thus it encapsulatesonly a limited part of the phenotypic varia-tion.

Ontogeny has been pragmatically decom-posed into three processes: growth, develop-ment, and maturation (Needham 1933; Gould1977). A growing organism can be envisionedas a point moving in a size-shape-age space(S-s-a space), and the pathway drawn by thispoint represents its ontogenetic trajectory(Alberch et al. 1979; Klingenberg 1998).Evolutionary changes relating ancestor-de-scendant pairs through the modification ofthe ancestral ontogenetic trajectory implydisjunctions among these three ontogeneticprocesses and have been addressed mainly inthe context of heterochrony (Gould 1977;McKinney 1988; McKinney and McNamara1991; McNamara 1995, 1997; Klingenberg1998). Paleobiological analysis of such evolu-tionary changes involves caution because ofthe way ontogenetic information is preservedin the fossil record. In most cases, size andshape data are the only data available, andeven though age and size usually display amonotonic relationship, they rarely do so in alinear way. Attempts to use one for the other(size as a proxy for age) have thus often beenmisleading and led to the conflicting resultsand terminological chaos that has emerged inthe heterochronic literature since the renewedinterest in the ontogeny-phylogeny relation-ships (Godfrey and Sutherland 1995a,b; Klin-genberg 1998; Gould 2000; Webster andZelditch 2005). In contrast, size and shapedata can be clearly defined and comprehen-sively characterized with the tools of modernmorphometrics (e.g., Mitteroecker and Gunz2009). The size-shape ‘‘plane’’ (Alberch et al.1979: Fig. 9, albeit that shape is obviouslyhighly multidimensional) defines the domain

of allometry and provides an unambiguousangle to look at ontogeny in paleontologicalstudies. Following this reasoning, Gerber etal. (2008) suggested the concept of allometricdisparity as a possible way to provide adevelopmental perspective in large-scaleanalyses of morphological disparity. Allome-tric disparity analysis is a quantitative explo-ration of allometric space, a phenotypic spacethat complements standard morphospaces(shape spaces). Whereas a standard morpho-space is a multivariate ordination of taxabased on their morphologies at a givendevelopmental stage (usually adult stage)and within which a point corresponds to ashape, an allometric space is a multivariateordination of taxa based on the characteristicsof their ontogenies (allometric coefficients;Solignac et al. 1990; Klingenberg 1996) withinwhich a point corresponds to an allometrictrajectory, i.e., a continuous succession ofshapes. Allometric disparity is the quantita-tive estimate of the occupation of the allome-tric space in terms of spread and spacing oftaxa (Gerber et al. 2008). Note that allometricdisparity and juvenile disparity (morpholog-ical disparity at an early developmental stage[Eble 2002, 2003]) are distinct quantities andprovide different characterization of develop-mental information in disparity analyses (see‘‘Discussion’’).

Ammonoids are an especially appropriatemodel system for such large-scale analyses aswell as for addressing macroevolutionaryquestions in general (see Neige et al. 2009for recent discussions). Ammonoids are awell-known group of extinct, externallyshelled cephalopods. Because of their exten-sive use in biostratigraphy, ammonoids havea rich, highly resolved record, both strati-graphically and geographically. This permitslarge-scale studies with both a high temporalresolution (zone, subzone, or horizon level)and a good knowledge of the paleobiogeo-graphical dynamics. Regarding the particularontogenetic focus of the present study, am-monoids also display interesting features.Shell growth proceeds as discrete additionof material at the apertural margin (Bucher etal. 1996). Because of this incremental growthprocess, the whole ontogeny of the shell is

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recorded, providing a convenient access tothe ontogenetic dimension of the taxon.Despite their gnomonic appearance and theirfrequent modeling based on the logarithmicspiral (Thompson 1942: Chap. XI), planispiralammonoid shells often show significant de-partures from purely isometric growth.

Important changes in ammonoid diversityare observed during the Early Jurassic (e.g.,Cecca and Macchioni 2004; Dera et al. 2010).These changes offer the opportunity to dis-cuss the behavior of diversity and disparitymetrics, and to observe potential selectivitypatterns of extinction. In addition to thesediversity-disparity contrasts commonly ad-dressed in the disparity literature, the onto-genetic focus of this paper also allows therecognition and the discussion of the multi-variate nature of the global morphologicalsignal. The adult morphological signal is onlyone aspect of the global signal, and neglectingits underlying developmental machinery istaking the chance of missing macroevolution-ary patterns and events or restricting thearray of causal hypotheses (e.g., prevalenceand/or interaction of ecological and develop-mental explanations).

Materials and Methods

Taxonomic Sampling.—This study focuseson the evolutionary history of Early Jurassicammonites over the Pliensbachian–Toarcianinterval (189.6–175.6 Ma [Gradstein 2004]),subdivided into 13 zones (average duration of1 Myr). The taxonomic sampling consists of164 genera belonging to the suborders Psilo-ceratina and Phylloceratina and representingmore than 90% (92.6%) of the genera recog-nized as valid (J.-L. Dommergues and P.Neige personal communication 2008). I choseto select one representative species per genus,on the basis of the best quality of preservationso as to minimize measurement error in shapeanalysis and characterization of growth pat-terns. Sexual dimorphism frequently has beensuggested in Jurassic ammonoids (Makowski1962; Callomon 1963, 1981; Davis et al. 1996).Here, dimorphism was not considered andonly macroconchs were included in theanalyses for species with hypothesized di-morphism.

Diversity Pattern.—The diversity curveshown in Figure 1 corresponds to a simpleraw count of valid genera per zone over thePliensbachian–Toarcian interval. At the Uni-versity of Burgundy important ongoing sys-tematic and database work is under way tobuild bias-corrected diversity curves and todocument major taxonomic patterns in EarlyJurassic ammonites at the species and genuslevels. First results (Dera et al. 2010) confirmthe pattern displayed in Figure 1 and inval-idate the potential effect of sampling. Thisexhaustive and homogeneous characteriza-tion of ammonoid faunas through time againlargely results from their important role asbiostratigraphic markers. At the genus level,the main pattern consists of two successivephases of drastic decline in diversity ( Jame-soni–Tenuicostatum and Bifrons–Pseudora-diosa) separated by a short phase of almostcomplete recovery. These two declines are ofequivalent length (,6 Myr) and magnitude(.50% drop in diversity), and can be treatedas repetitions of the same experiment forwhich diversity-disparity covariation patternscan be compared.

Morphological Analysis.—The methodologyused is similar to that of Gerber et al. (2008).Temporal morphological variation is investi-gated at both the adult and the ontogeneticlevels, the latter being tackled through theallometric disparity approach. The morpho-metric description of shell shape and coilinggeometry is based on the standard set ofmeasurements used in ammonite morpho-metrics. Lateral shell shape is characterized

FIGURE 1. Curve of ammonoid generic diversity duringthe Pliensbachian–Toarcian interval (Early Jurassic).Standard error of taxonomic diversity is estimated asthe square root of number of genera (Sepkoski and Raup1986; Foote 1994). Chronozone abbreviations: J, Jamesoni;I, Ibex; Da, Davoei; M, Margaritatus; Sp, Spinatum; Te,Tenuicostatum; Fa, Falciferum; B, Bifrons; V, Variabilis;Th, Thouarsense; Di, Dispansum; P, Pseudoradiosa;A, Aalensis.

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with four linear measurements taken at thesame developmental stage: the shell diameterD, the umbilical width U, the radius length R,and the whorl height Wh (Fig. 2). All mea-surements are carried out on the phragmo-cone (chambered part of the shell). Measure-ments on the adult body chamber are avoidedbecause maturation sometimes entails chang-es in ornamentation and peristome shape, aswell as small departures from the overallgrowth pattern (Davis et al. 1996).

Raup Model and Morphospace.—D, R, and Whare the variables used to compute Raup’sshell coiling parameters DR (distance of thegenerating curve from the coiling axis) andWR (shell expansion rate) (Raup 1966, 1967).The Raup model supplies an explicit bivariateordination of planispiral ammonites based ontheir coiling geometry. Despite its visualelegance and its descriptive power, the DR-WR plane does not allow direct quantitativeappraisals of morphospace occupation, be-cause of the difficulty in defining an unam-biguous measure of intershape distance (Ger-ber 2007). Therefore, I have chosen a parallellandmark-based approach that considerslandmarks instead of inter-landmark distanc-es. Each specimen is then described by avector of coordinates [0, Wh, R, D], corre-sponding to a set of four collinear landmarks.

Expressed this way, morphological data canthen be submitted to landmark-based geo-metric morphometric methods, and the Pro-crustes distance used as a metric for shapedifference. Because the generalized Procrus-tes analysis (GPA; Rohlf and Slice 1990) ofone-dimensional data does not require rota-tional fit, only two degrees of freedom are lost(one for unit-centroid size scaling and one fortranslation; Goodall 1991) and the resultingshape space is the surface of a (hyper)spherehomologous to the preshape space instead ofthe usual Procrustes (hyper)hemisphere(Small 1996; Rohlf 1999; Slice 2001). Never-theless, as in most morphometric studies, theextent of shape variation displayed by theempirical sample is small, making the tangentapproximation an appropriate way to circum-vent the nonlinearity of Procrustes spaces,even in the case of orthogonal projection. Inother words, despite the sphericity of theshape space, the observed shape variation issmall enough to ensure a one-to-one mappingof specimens from shape space to tangentspace (see Gerber et al. 2007, 2008 forprevious empirical applications; data depos-ited at Dryad: doi:10.5061/dryad.8594).

Morphological Disparity Measures.—A largenumber of indices have been proposed toquantify the various aspects of morphospaceoccupation and to accommodate the diversityof morphometric frameworks and descriptors(e.g., Foote 1991, 1997; Wills et al. 1994;Ciampaglio et al. 2001; Wills 2001; Navarro2003). The two disparity indices used here arethe sum of variances (total variance) and thesum of ranges (total range). The former isproportional to the average squared distancebetween taxa (spacing of taxa) and is com-puted as the trace of the covariance matrix ofshape variables (Procrustes shape coordi-nates). The latter quantifies morphospaceoccupation in terms of surface or (hyper)volume (spread of taxa) and corresponds tothe sum of ranges measured along theprincipal axes of the shape space (relativewarps). Because the sum of ranges is sensitiveto peripheral taxa and sample size, a rarefac-tion procedure is performed to ensure thecommensurability of disparity estimates overtime (Foote 1992).

FIGURE 2. Morphometrics of ammonoid shell. The coilinggeometry of shell lateral shape is described by four linearmeasurements: D, shell diameter; U, umbilical width; R,radius; and Wh, whorl height. These four variables, takenat different developmental stages, are used in theallometric space analysis. For the adult morphospaceanalysis, only D, R, and Wh are required to describe shellcoiling in the Raup model and define its geometricexpression as a vector of collinear landmarks [0, Wh, R, D].

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Allometric Space.—Quantitative allometricdescription of ammonite shell growth is basedon the same set of measurements, but takenon specimens at many different developmen-tal stages using both longitudinal and cross-sectional data (Cock 1966), resulting in 1847sets of measurements. Shell growth describedby log-transformed measurements fits Hux-ley’s equation for simple allometry and itsmultivariate extension (Huxley 1932; Joli-coeur 1963; Shea 1985; Klingenberg 1996).For a given taxon, only 10–15 specimens arerequired to obtain a reasonable description ofthe growth pattern in the space of log-transformed measurements (log-space), pro-vided these specimens offer a satisfyingcoverage of the average range of ontogeneticsize variation. For each taxon, the eigen-analysis of the covariance matrix of the log-transformed measurements supplies the di-rection of the ontogenetic trajectory in the log-space through the coefficients of the firsteigenvector. The associated eigenvalue, inaddition to being the highest, usually sum-marizes most of the initial variance (here,97.8% on average), validating the adequacy ofthe simple allometric model. Each taxon isthus allometrically described by four coeffi-cients (vector of allometric pattern), which arethe loadings of the log-transformed variablesD, R, U, and Wh on the first principalcomponent of the distribution in the log-space of specimens at different developmen-tal stages. The allometric space is simply thematrix obtained by the vertical concatenationof the vectors of allometric patterns. Thisspace can be explored using the toolkit ofdisparity analyses, so as to quantify allo-metric disparity, i.e., the variety of allometricpatterns displayed within a given clade at agiven time (Gerber et al. 2008). Besidesvariance and range-based metrics of dispari-ty, the average distance to isometry is ameasure specifically devised to explore com-plementary aspects of allometric space occu-pation. This index is based on the relativepositions of the isometric growth vector andof the empirical distribution of taxa. Althoughdirectly calculated in the allometric spacehere, it is equivalent to the average anglebetween the isometric vector and the set of

empirical trajectories (Gerber et al. 2008).Thus, contrary to total range and totalvariance, the average distance to isometryincorporates positional information. Hence,two equally disparate empirical distributionsin the allometric space, but differing in theiraverage allometric patterns (e.g., one slightlyallometric and one strongly allometric), willhave similar variances but different averagedistances to isometry. When ancestral, de-scendant, and isometric trajectories are in thesame plane within the log-space, the polari-zation—paedo- versus peramorphic—of theevolutionary change in ontogeny between theancestor and the descendant can be assessedby using the average distance to isometry(Fig. 3) (and see Klingenberg 1998). Hence,applied over large time scales, and providedthe geometrical assumption above is met, thisindex allows the detection of large-scaleheterochronic trends or heterochronoclines,i.e., directional morphological evolution in-volving sustained paedo- or peramorphicchanges within a lineage (Alberch 1980;McNamara 1982; McKinney and McNamara1991 and see ‘‘Results’’). If the above assump-tion is not met, then heterochronic explana-tions at the morphological level investigatedis not valid. The patterns observed resulteither from a different type of evolutionarydevelopmental change (e.g., allometric repat-terning [Webster and Zelditch 2005; Gerber etal. 2007]) or perhaps, in the case of complexphenotypes, from a combination of localchanges (e.g., local heterochrony, mosaicpattern) that are indistinguishable within themorphometric framework used.

Size Pattern.—Because allometry expressessize-related shape changes, it logically followsthat morphological and allometric disparitiescan show complex connections depending onthe variation in adult size observed amongthe taxa studied (Gerber et al. 2011). It is thusimportant to supplement the analysis ofchange in allometric disparity with a surveyof the change in average adult size. Adult sizein ammonoids is commonly measured as thediameter of the adult phragmocone, the latterbeing characterized by the septal approxima-tion criterion outlining the slowdown andtermination of growth (determinate growth).

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Volumetric measures of size (i.e., accountingfor shell width) have been used but theyprovide comparable patterns because shelldiameter and whorl width are highly andsignificantly correlated (rS . 0.9, p , 0.001 inEarly Jurassic ammonoids [based on datafrom Dommergues et al. 2002]). Changes inadult size are estimated with both mean andmedian adult shell diameter so as to avoidpotential distortions caused by skewed dis-tributions. Standard errors were calculatedvia bootstrap resampling (1000 replicates).Different sampling choices for species asgenus representatives, with various criteria(genus minimal, maximal, and average size),have been tested to ensure the consistency ofthe size patterns documented. No significantchanges in results have been found.

Results

Distribution in Morphospace and AllometricSpace.—Figure 4 displays the global empiricaldistributions of the 164 ammonoid genera in

the adult morphospace and in the allometricspace. In the adult morphospace, visualizedin the DR-WR Raup plane, taxa show a broadspectrum of morphologies ranging fromhighly involute forms with high spiral expan-sion rate (Phylloceratina, lower left quadrantof Fig. 4A) to forms with low whorl overlapand expansion rate (mainly Psiloceratina,upper right quadrant of Fig. 4A). The varia-tion in planispiral shell shape expressedduring the Pliensbachian–Toarcian time in-terval is similar to that observed for the entireJurassic and Cretaceous (e.g., Ward 1980) andoutlines the early morphological diversifica-tion of the clade to its known maximum. Theinterpretation of allometric space occupationis different from that of typical morpho-spaces. A convenient first step is to locatethe position of the isometric growth vector. InJurassic ammonites, the average growth pat-tern does not markedly deviate from isome-try, making the cloud’s centroid in thevicinity of the isometric growth vector

FIGURE 3. Polarity of evolutionary developmental changes between ancestor and descendant illustrated forhypothetical rectangular organisms. When the descendant trajectory is within the plane defined by the ancestraltrajectory and the isometric growth vector, the evolutionary change can be ascribed to heterochrony (see text andKlingenberg 1998). The example here presents the peramorphic case. The descendant trajectory (D) appears to departmore from the isometric axis than the ancestral trajectory (A) does, while remaining in the same plane (A; this ismathematically constrained in this simplified 2-D log-space example). Hence, the shape changes observed during theontogeny of the ancestor correspond only to an early ontogenetic part of the descendant shape trajectory. Because oftiming or rate-based changes, the descendant runs along the ancestral shape trajectory early in its ontogeny and thenextends it and displays peramorphic, hyper-adult shapes (B and C; sharing the ontogenetic trajectory of shape changeis the prerequisite for heterochronic explanation). Again, this reasoning is valid only if the descendant trajectory lies onthe plane spanned by the isometric growth vector and the ancestral trajectory. If not, heterochronic explanation for theevolutionary change observed does not hold. When this geometric requirement is met, the use of the average distanceto isometry offers a large-scale proxy for this ontogenetic polarity and allows the detection of sustained heterochronictrends (paedo- or peramorphocline).

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(Fig. 4B) (Gerber et al. 2008). The closer ataxon is to this isometric referential, the lessallometric its growth is. Another seeminglyrecurring pattern when focusing on allometryin shell coiling is the large amount of variancesummarized by the first principal componentof the allometric space (here 92.73%). Thisindicates that allometric growth patternsobservable in coiling geometry can be roughlycharacterized either by a decreasing whorloverlap throughout ontogeny or by theconverse. Hence, the almost one-dimensionaldistribution of taxa is not a methodologicalbias or a mathematical constraint, but ratherreflects the characteristics of shell growth inammonites.

Temporal Changes in Disparities.—Quantita-tive description of Raup morphospace occu-pation through time is given in Figure 5. Jointanalysis of range- and variance-based adultmorphological disparity curves reveals astrikingly stable pattern. In terms of range,no significant variation can be detectedthroughout the Pliensbachian–Toarcian inter-val. This fact results mainly from the mor-phological stability of Phylloceratina andLytoceratina taxa over time and their locationat the periphery of the morphological spec-trum. Nonetheless, the sum of variancesallows the detection of slight variations.Minimal disparity is observed at the Pliens-bachian/Toarcian boundary, also correspond-ing to the lowest diversity reached during thePliensbachian taxonomic decline. The highestdisparity value occurred in the Pseudoradiosazone, which also corresponds to the time oflowest diversity over the whole intervalstudied, after a relatively constant increasethroughout the Toarcian. Hence, these twodisparity curves mostly reflect changes indensity of occupation within stable morpho-logical boundaries, especially among Psilo-ceratina, caused by seemingly random extinc-tion of taxa and entailing the homogenizationof the filling of morphospace.

Variance and range-based estimates ofallometric disparity show sustained concor-dant variations over time and a markedcontrast between Pliensbachian and Toarcianpatterns (Fig. 6). The Pliensbachian interval ischaracterized by a stable occupation of the

allometric space, whereas the Toarcian inter-val displays a regular spreading and spacingof taxa, suggesting an unbounded diffusionwithin the allometric space. Like morpholog-ical variance, maximum allometric disparityis reached in the Pseudoradiosa zone.

Heterochronoclines and Size Variations.—Al-lometric disparity measured as the averagedistance to isometry provides additionalinformation about the occupation of theallometric space and about the evolutionarysignificance of temporal changes in thisoccupation. The unidimensional and isome-try-centered distribution of ammonoid allo-metric patterns (Fig. 4B) makes the interpre-tation of this additional allometric disparitymetric relevant. Although the average dis-tance to isometry shows no significant varia-tion during the Pliensbachian, it emphasizestwo successive, opposite trends during theToarcian (Fig. 7A). Assuming that strati-graphic precedence can be used as a smooth,large-scale indicator of ancestor-descendantpolarity (an implicit assumption in all dispar-ity analyses, and an even more reliable onefor ammonoids given their high taxonomicturnover rate), the initial increase in disparity(Tenuicostatum–Variabilis zones) can be in-terpreted as a peramorphocline (manifestedby an increasing departure from isometrythrough time) and the following decrease(Variabilis–Aalensis zones) as a paedomor-phocline. Median and average size curvesshow variations opposite to changes inaverage distance to isometry (Fig. 7B). Duringthe Pliensbachian, no significant changes areobserved and average size is ,70 mm. Theearly Toarcian peramorphocline seems to beassociated with a slight decrease in size(,60 mm) and the late Toarcian paedomor-phocline with an increase in size (,100–120 mm).

Discussion

The aim of this work was to provide adescription of the evolutionary history ofshell geometry in early Jurassic ammonitesover the Pliensbachian–Toarcian interval withan explicit, quantitative focus on the ontoge-netic aspects of the phenotypic variation tocomplement standard curves of adult mor-

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FIGURE 4. Adult morphospace (A) and allometric space (B) of Pliensbachian–Toarcian ammonoid genera. The adultmorphospace is visualized in the DR-WR plane of Raup morphospace (Raup 1967). Some extreme morphologies areillustrated. The allometric space shows the ordination of the same set of taxa based on their allometric growth patterns.In this space, each taxon is also represented by a single point, but this point encapsulates the information about thecontinuous succession of shapes displayed by the taxon during its ontogeny (post-embryonic growth here). Theisometric vector (encircled star) is used as a reference to interpret the distribution of taxa in the allometric space. The

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phological disparity. This aim has beenachieved through the quantification of allo-metric disparity, i.e., the variety of multivar-iate growth patterns, whose variations de-scribe the filling and emptying of theallometric space.

Juvenile morphological disparity has alsobeen suggested as a possible index fordevelopmental disparity to enrich the de-scription and our understanding of a clade’shistory (Eble 2002, 2003; Zelditch et al. 2003;McNamara and McKinney 2005; Gerber et al.2007). Juvenile morphological disparity is thedisparity expressed by a clade computed forits constituent taxa at an early developmentalstage. In the most convenient case, bothjuvenile and their related adult forms can bedescribed under a common morphometricscheme (e.g., the same set of landmarks) anddepicted in the same developmental morpho-space. Juvenile and adult disparity estimatescan then be directly compared. If the shapesat the ontogenetic stages chosen preventcommensurable morphometric descriptions,alternative statistical approaches can stillallow comparisons of disparity levels (Eble2002). A more serious impediment to theapplicability of the juvenile disparity ap-proach is when homologous developmentalstages or transitions cannot be unambiguous-ly identified among the taxa analyzed. Incases that are missing criteria for recognizing

developmental stages (e.g., larval-postlarvaltransition, dental stage, instars), the allo-metric disparity is a promising alternative tostudying clade developmental dynamics.Furthermore, juvenile disparity patterns canalso be inferred from the inspection ofallometric disparity patterns (Gerber et al.2011). Lastly, because it incorporates a de-scription of the whole ontogenetic trajectory,allometric disparity can more successfullyaccommodate various types of growth (poly-phasic and complex allometries) than thesampling of a single pre-adult stage fromthe trajectory (but see Eble 2002 and Gerber etal. 2007 for multistage extensions of juveniledisparity).

As mentioned earlier, previous paleonto-logical investigations of the role of develop-ment in evolution have been carried outwithin the framework of heterochrony. Al-though a greater variety of evolutionarydevelopmental changes have since been rec-ognized, categorized, and provided withmore efficient statistical and analytical ap-proaches (Arthur 2000; Webster et al. 2001;Webster and Zelditch 2005; Mitteroecker et al.2005; Gerber et al. 2007), their sampling scopeis still limited because the proper identifica-tion of the evolutionary developmentalchanges involved requires the knowledge ofancestor-descendant successions. These stud-ies have thus been restricted to analyses of

r

closer a taxon is to isometry, the less allometric its growth is. As an example, the ontogenetic shape changes (fortriplication of the shell diameter) of three taxa at specific locations in the allometric space are illustrated (one close tothe isometric vector and two at the opposite ends of the empirical spectrum of growth pattern variation). Note that theisometric vector is in the vicinity of the centroid of the empirical distribution (0,0), outlining the sub-isometric averagegrowth pattern of Pliensbachian–Toarcian ammonoids.

FIGURE 5. Curves of morphological disparity during the Pliensbachian–Toarcian interval, measured as variance (A)and range (B). The slight variations of the sum of variances and the stability of the sum of ranges reflect diversity-driven changes in the density of morphospace occupation, within a stable morphological spectrum. Error bars arebootstrapped standard errors (1000 replicates). Chronozone abbreviations are as in Figure 1.

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small sets of taxa and have never beenincorporated into disparity analyses, wherehundreds of species or genera are generallyconsidered simultaneously. For such cases,obtaining a comprehensive phylogeneticframework still remains elusive. For large-scale morphological analyses, contrasts ofjuvenile and adult disparities or curves ofallometric disparity can help reveal generaldevelopmental trends and shed light on thedevelopmental mechanisms that underliemorphological changes.

In the present study, the allometric dispar-ity approach has been applied to ammonoidshell growth. The main results outline twosubstantially different morphological anddevelopmental evolutionary dynamics duringthe Pliensbachian and the Toarcian Stages.Each of these intervals is characterized by asevere decline in generic diversity. In the faceof these two successive, comparable declines,the amount of morphospace occupied re-mains strikingly stable over the Pliensba-chian–Toarcian interval (total range), suggest-ing nonselective extinction regarding adult

coiling geometry, and only minor changes indensity of occupation (total variance) oc-curred, notably during the Toarcian. Never-theless, a developmental focus on ammonoidevolutionary history suggests two differentdynamics for the Pliensbachian and theToarcian intervals. Whereas Pliensbachianammonoids were developmentally stable,Toarcian taxa expanded and then reducedthe spectrum of allometric growth patternswith concomitant variations in their averageadult size. The pattern given by the averagedistance to isometry and the distribution oftaxa in the allometric space (unidimensionaldistribution in alignment with isometricgrowth) imply heterochrony-based evolution-ary developmental changes in the evolutionof coiling geometry in Early Jurassic ammo-noid. Interestingly, the size variations weresuch that they compensated for the evolutionof allometric disparity: the Early Toarciandeployment of taxa in the allometric space,corresponding to a peramorphocline, waspossibly accompanied by a decrease inaverage adult size; the attrition in allometric

FIGURE 6. Curves of allometric disparity during the Pliensbachian–Toarcian interval, measured as variance (A) andrange (B). No significant variations are observed during the Pliensbachian. A slow increase in spreading and spacingwithin the allometric space occurs during the Toarcian. Error bars are bootstrapped standard errors (1000 replicates).Chronozone abbreviations are as in Figure 1.

FIGURE 7. Curve of allometric disparity during the Pliensbachian–Toarcian interval (A), measured as the averagedistance to isometry (see text), and curves of average adult size (B), measured as mean (black squares) and median(open circles) diameters of adult phragmocone. Although stable during the Pliensbachian, the average distance toisometry increases during the first part of the Toarcian (Tenuicostatum–Variabilis) and then declines (Variabilis–Aalensis). This suggests the succession of two heterochronoclines: a peramorphocline followed by a paedomorpho-cline. The size pattern tends to display coincident variations. Error bars are bootstrapped standard errors (1000replicates). Chronozone abbreviations are as in Figure 1.

378 SYLVAIN GERBER

space, corresponding to a paedomorphocline,was accompanied by an increase in size. As aresult, the combination of these changescanceled out their respective paedo- andperamorphic effects and thus had no impacton adult morphospace occupation and dis-parity. For instance, a sustained departurefrom a more isometric growth in a lineagecould have been counterbalanced by a trun-cation of ontogenetic trajectories, leavingadult morphologies potentially unchanged.A similar relationship between size variationand allometric disparity has been observed ina recent study of ammonoids at the Early–Middle Jurassic transition (Gerber et al. 2008).The Hammatoceratidae family showed animportant allometric diversification at thebeginning of the Middle Jurassic, and a coevalmarked decrease in average adult size (from,150 to ,75 mm). Such counterbalancingchanges between size and allometric varia-tion, with one maybe varying in response to‘‘stresses’’ acting on the other, could be aneffective factor structuring ammonoid mor-phospace and could explain its temporalstability since the Paleozoic.

The Pliensbachian–Toarcian interval isknown to be a second-order mass extinctionevent likely related to a conjunction ofdramatic environmental changes includingsea-level variation, oceanic anoxia, seawatertemperature variation, disruption of the car-bon cycle, and volcanic activity (e.g., Hallam1987; Palfy and Smith 2000; Dera et al. 2009,2010). Interestingly, the marked increase inallometric disparity via peramorphic diversi-fication appears to be concomitant with theearly Toarcian anoxic event (Jenkyns andClayton 1997), a significant warming ofseawater temperatures (Dera et al. 2009),and the flood basalt events in the Karoo-Ferrar province (Jourdan et al. 2007; Riley andKnight 2001). The heterochronic shifts ob-served could reflect a change in life-historymodes during this period of environmentalstress. Guex (2006) also documented drasticdevelopmental changes in ammonites con-fronting such stresses, resulting in simplifica-tion of many morphological aspects towardancestral morphologies (proteromorphosis).Further work is still required before drawing

conclusions linking specific environmentalfactors to the changes observed in thedevelopmental dynamics of ammonoids dur-ing this period; the recurrence of suchdevelopmental patterns in the face of similarenvironmental changes has to be exploredand tested. Nevertheless, a link between thedevelopmental characteristics of taxa andtheir dynamics during extinction and recov-ery processes is plausible.

Because this paper was concerned onlywith the ontogenetic changes in coilinggeometry, the morphometric scheme waslimited to the two-dimensional descriptionof shell lateral shapes, summarized by Raup’smodel (DR and WR) phrased in a geometricmorphometric fashion. Ammonoid globalshell morphology is obviously not reducibleto a set of four collinear landmarks. Patternsof shell ornamentation and apertural shapeare also major aspects of shell morphology,and their large-scale ontogenetic character-ization would provide additional insights intothe evolutionary history of ammonoids. Nev-ertheless, coiling geometry and whorl widthare generally correlated, forms with overlap-ping whorls (involute) generally having lat-erally compressed sections (see for instanceRaup’s [1967] Text-fig. 6 for the covariation ofapertural shape SR with DR and WR). Like-wise, covariation between shell shape andornamentation has been a longstanding ob-servation referred to as Buckman’s first law ofcovariation (Buckman 1892; Westermann1966; Guex et al. 2003; Yacobucci 2004;Hammer and Bucher 1999). Involute, com-pressed shells almost always display weakerribbing patterns. Hence, analyses taking intoaccount shell width or specifically addressingthe evolution of ornamental patterns shouldnot invalidate the significance of the patternsdescribed in the present study but wouldinstead enrich our understanding of covaria-tion among shell characters at a broadertaxonomic level.

Further analyses will also have to investi-gate these morphological and developmentalpatterns at the subclade level to assess therelative contribution of Psiloceratina andPhylloceratina to the global signal. Suchpartial disparity analyses should help detect

AMMONOID DEVELOPMENTAL DYNAMICS 379

variable degrees of ‘‘developmental flexibili-ty’’ that may explain the differential evolu-tionary dynamics and success of some am-monoid clades in the face of biological orenvironmental perturbations.

Summary

1. The seemingly stable temporal evolution ofmorphological disparity of shell coiling inearly Jurassic (Pliensbachian–Toarcian)ammonoids, as it could be inferred fromthe analysis of their adult morphospace,appears to be more complex when theontogenies of taxa are taken into account.The incorporation of ontogenetic data intothe disparity analysis is done through theuse of the allometric space, providing aquantitative description of the variety ofshell allometric growth patterns.

2. The contrast of morphological and allo-metric disparity metrics emphasizes twodifferent evolutionary dynamics for Pliens-bachian and Toarcian ammonoids. Bothtime intervals are characterized by declinein taxonomic diversity and stable adultdisparity, but whereas Pliensbachian am-monoid genera show no significant chang-es in allometric disparity and average adultsize, Toarcian genera do.

3. The trajectory of the average distance toisometry during the Toarcian suggests thatthe evolutionary developmental changesinvolved can arguably be ascribed toheterochrony. This supports the previouslynoticed role of heterochrony in the evolu-tion of ammonoid shell shape, but alsoshows that these heterochronic changescan act as sustained temporal trends(heterochronocline). A pera- and a paedo-morphocline are successively observedduring the Toarcian.

4. These heterochronoclines tend to coincidewith variations in the average adult size.Their counterbalancing effects on the finaladult morphologies explain the stability ofthe adult disparity signal. Variations inadult size can substantially alter morpho-space occupation when taxa display allo-metric growth. Their potential effectsshould be accounted for when looking for

explanations of morphological (shape) pat-terns and trends.

Acknowledgments

I thank J.-L. Dommergues and P. Neige fortheir help with ammonite systematics. Fordiscussions on some aspects of this work andvaluable comments on earlier drafts, I thankG. Dera, G. J. Eble, M. J. Foote, M. J. Hopkins,A. Haber, E. King, C. Belanger, D. Bapst, andY. Savriama. I thank P. J. Wagner, M. M.Yacobucci, and D. Korn for their constructivereviews and helpful suggestions. For theirsupport at successive stages of the complexontogeny of this work, I warmly thank S. E.Strano, Y. Savriama, and A. Haber. This paperis a contribution to the team FED (Forme,Evolution, Diversite) of the UMR CNRS 5561Biogeosciences, the GDR MEF (Morphometrieet Evolution des Formes), and the ECLIPSE II(CNRS) research program. This work wassupported by a teaching and research grantfrom the University of Burgundy (2007-41), apostdoctoral fellowship from the Universityof Chicago, and a research grant from theLeverhulme Trust (F/00 351/Z).

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