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Morphometrics and cladistics: measuring phylogeny in the sea urchin Echinocardium.

What part should morphometric data play in evolutionary studies? The recent expansion of shape-analysis methods using landmarks (Sneath 1967; Benson et al. 1982; Siegel and Benson 1982; Bookstein et al. 1985; Rohlf and Bookstein 1990; Bookstein 1991 for a review) has revived the way morphometric data can enhance the exploration of evolutionary processes. Now that new morphometric tools are available, it is an opportune time to explore to what extent and for what purposes it could be fruitful to use pure morphological analyses in conjunction with phylogenetic approaches.

The purpose of a phylogenetic analysis is to uncover evolutionary patterns, whatever the assumptions about evolutionary processes might be (Nelson and Platnick 1981; Janvier 1984). In a cladistic approach, organisms are reduced to sets of discrete features, and the characters used in the analyses are assumed to be independent. Consequently, a certain number of morphological characters lie outside the scope of the analysis, namely features involved in epigenetic interactions. In contrast, in a morphometric approach, complementary sets of features can be taken into account, including those involved in allometric developmental coordination. Therefore, such an approach offers the opportunity to investigate particular kinds of evolutionary processes, such as those related to allometries and heterochronies (Gould 1977). The deciphering of heterochronic processes generally necessitates relating shape indices to the age and size of organisms (Alberch et al. 1979). However the shape indices classically used (e.g., dimensional ratios [Landman 1988; Dommergues and Meister 1989], principal components, or factorial coordinates [David and Laurin 1991; Tissot 1988]) are not always appropriate to fully separate size from shape. Instead of comparing ontogenies described by shape indices, shape analysis methods using landmarks address direct shape differences that are completely free of size effect (Bookstein 1991). Moreover, these methods provide accurate computation of morphometric distances (Chapman 1990; Reilly 1990; Din et al. 1993), thereby establishing trees of morphological relationships. However, morphology is not unambiguously related to phylogeny because of the occurrence of homoplastic events (reversals and convergences) in the course of evolution. Therefore, it is not appropriate to establish directly phylogenetic reconstruction on morphometrics (Bookstein 1990). Morphometric outcomes are necessarily subordinate to phylogenetic studies. Accordingly, we propose to use shape analyses to explore only the processes that could underlay the phylogenetic patterns, namely those related to ontogeny. This implies distinction of two concepts of homology: it is not of same nature in cladistic and morphometric studies. Smith (1990) proposed a clear-cut distinction between "taxic homology" (sensu Eldredge 1979) and "operational homology," the former referring to synapomorphy (Patterson 1982), and the latter referring to form-to-form (e.g., landmark-to-landmark) correspondence.

Shape-analysis methods based on landmarks have been used efficiently to address evolutionary questions. They appear pertinent in clarifying morphological evolutionary pathways (e.g., Benson 1976, 1983 in ostracode lineages; Chapman and Brett-Surman 1990 in dinosaurs; Laurin and David 1990a in brachiopods) as well as in elucidating processes involving ontogeny (e.g., Bookstein 1981, 1984 on the human skull; Reilly 1990 in salamanders; Zelditch et al. 1992 for the cotton rat). The aim of the present study is to explore the link between shape analysis, phylogenetic estimation, and ontogenetic processes through the use of an exemplary case. To do this, we will reconstruct the phylogenetic pattern of relationships for the spatangoid sea urchin Echinocardium, and explore, through shape analysis, the evolutionary processes involved in the differentiation of the species within the genus.

MATERIALS AND METHODS

Choosing Echinoids

The test of sea urchins is an array of 20 columns of plates radiating from the apical system. Adult tests contain several hundreds of plates (up to and exceeding 3000 plates in some cases, Kier 1974). The growth of the test results from two complementary processes: addition of new plates at the external edges of the apical system and size increase of the existing plates. The balance between plate allometries and the rate of appearance of new plates allows the emergence of a great diversity of outlines associated with various architectural patterns (Moore 1966). In the group known as spatangoids (a subgroup of irregular sea urchins), additional structures such as petals or fascioles interfere with the plate pattern, enlarging the range of morphologies. The diversity of the spatangoid clade represents evolutionary pathways exploiting possibilities offered by such developmental coordination. Sea urchins also have the advantage of displaying characters relatively free of ontogenetic influence and available for phylogenetic analysis, as well as traits more influenced by development and available for morphometric approaches.

Data

The spatangoid Echinocardium belongs to the family Lovenidae. It is a heart-shaped sea urchin quite common in epicontinental seas where it burrows in sandy or muddy bottoms. Echinocardium is a monophyletic genus that includes 12 nominal Recent species (according to Mortensen 1951; completed by Pequignat 1964) and about 20 fossil species (according to Lambert and Thiery 1924; completed by Kier 1972, 1983; Kotchetoff et al. 1975).

Among the Recent forms, the species Echinocardium cordatum [ILLUSTRATION FOR FIGURE 1 OMITTED], Echinocardium fenauxi, Echinocardium flavescens, Echinocardium mediterraneum [ILLUSTRATION FOR FIGURE 2 OMITTED] and Echinocardium pennatifidum [ILLUSTRATION FOR FIGURE 3 OMITTED] are widely distributed and clearly distinguishable. Four other species with restricted distribution areas [Echinocardium capense, Echinocardium laevigaster, Echinocardium lymani, and Echinocardium mortenseni [ILLUSTRATION FOR FIGURE 4 OMITTED]] are not firmly established and, although some authors have challenged their validity (Mortensen 1951; Baker 1969), they have been maintained as separate species on biogeographical grounds. The situation of Echinocardium australe is quite similar, as this species, erected for the populations of Echinocardium from New Zealand and Australia (Gray 1851), has been synonymized with E. cordatum by most of the modern workers (Clark 1917, Mortensen 1951, Higgins 1974). However all these species will be considered provisionally as separate entities (as species or subspecies) for the sake of the analyses because this provides the most all-encompassing estimate of species diversity and relationships within the genus. Two Recent species, Echinocardium connectens and Echinocardium keiense, are poorly known from only a few fragments and will not be further considered in this paper.

The earliest fossils referred to Echinocardium are from the Oligocene (Cotteau et al. 1885). The attribution of these old forms to the genus is not beyond doubt because they are poorly preserved and rare. Miocene and Pliocene forms are more common and unambiguously belong to Echinocardium (Cotteau 1885; Cooke 1959). However, the information on architectural features drawn from the paleontological data is not reliable enough to fully integrate the fossil species in the analyses.

Specimens of most of the Recent species and several Miocene species of Echinocardium were examined, and additional information was obtained from the literature (Clark 1917; Mortensen 1951; Pequignat 1964). For the 10 Recent species retained for the analyses, our data consist of: E. cordatum, several hundred specimens from varying European localities; E. cordatum australe, E. mediterraneum, and E. pennatifidum, some tens of specimens from New Zealand (housed at the MNHN, Paris and NMNZ, Wellington), Mediterranean sea, and northeastern Atlantic respectively; E. fenauxi, E. mortenseni, E. flavescens and E. capense, a few specimens from the Mediterranean Sea (the two former species), northeastern Atlantic, and southern Atlantic, respectively (MNHN, Paris); E. laevigaster, one specimen from the northwestern Atlantic (USNM, Washington); E. lymani, which we had no specimen in hand and can rely only on the figure in Clark 1917.

Phylogenetic Analysis

An analysis of the ten Recent Echinocardium species was undertaken on a set of about 30 characters dealing mostly [TABULAR DATA FOR TABLE 1 OMITTED] with the architectural array of the plates and with the general morphology and tuberculation of the test. From this examined set, uninformative characters (e.g., autapomorphies) as well as highly variable characters for which it was impossible to recognize discrete states were removed (as recommended by Farris 1990). Finally, a data matrix of 18 characters was retained for the analyses (Table 1). Polarization of character states was according to the outgroup criterion (Lovenia was used as sister group within the lorenlids, and the spatangid Maretia served as a more distantly related outgroup), using the formal rule of Maddison et al. (1984) when necessary. Binary coding of the characters was used. The phylogeny was then explored with the aid of the phylogenetic package PAUP 3.1.1 (Swofford 1993), using the exhaustive search and outgroup rooting options and excluding invariant characters (basal synapomorphies). An estimate of nod stability was obtained using 1000 bootstrapping replications (Felsenstein 1985).

Shape Analysis

The shape analyses using morphometric characters were done on the nine Recent species for which specimens were available (E. lymani was excluded). Twenty-one sea urchins were selected: an ontogenetic series (9 mm, 16 mm, 31 mm, 41 mm, and 49 mm in length) of five E. cotdatum (selected from a statistical average of a sample of about 200 specimens, David and Laurin 1991); another series of four E. pennatifidum (8 mm, 21 mm, 36 mm, and 52 mm); two specimens each of E. cordatum australe (18 mm and 49 mm), E. fenauxi (20 mm and 55 mm), E. mediterraneum (16 mm and 45 mm), E. mortenseni (12 mm and 27 mm), and E. flavescens (18 mm and 33 mm); one E. laevigaster (33 mm) and one E. caperise (24 mm). Plate patterns of each specimen were revealed using methods of David and Mooi (1990) and drawn in dorsal view, with the specimen's plastronal area parallel to the horizontal plane [ILLUSTRATION FOR FIGURES 1-4 OMITTED]. Camera lucida drawings were made on a binocular microscope at a magnification that allowed maintenance of a consistent plane of focus to control distortion. A set of 49 landmarks that depict the main traits of the apical side was identified on each figure [ILLUSTRATION FOR FIGURE 5 OMITTED]. The points were chosen following test architectural criteria, and all but two were branch points belonging to type 1 as defined by Bookstein (1991). Most of the points are fully independent of the characters used in the phylogenetic analysis (there is redundancy in only 3 of the 18 cladistic characters). The coordinates of the landmarks were digitized and an average calculated for each corresponding pair of bilaterally symmetric landmarks in order to avoid asymmetry in the comparisons. Despite this forced symmetry, the analyses were performed on the complete set of 49 landmarks in order to avoid over-emphasis of the five midline landmarks during rotational fit, as well as to obtain more realistic fitted graphics.

We have used superimposition methods to figure out the shape changes between the different specimens. These methods, known as "conventional Procrustes methods" (Chapman 1990), operate by matching one configuration of landmarks (the superimposed specimen) on top of another (the base specimen) such that their discrepancy is minimized by some criterion. The difference between two specimens is then expressed as a vector field. The algorithms used to extract the vector field fall into two main categories: LSTRA (Least-Squares Theta Rho Analysis) and RFTRA (Resistant Fit Theta Rho Analysis). In the former, the differences are calculated by minimizing the vector field (least-squares method, Sneath 1967). In the latter, differences are estimated by concentrating all the shape discrepancies into a limited deformed region, simultaneously resulting in an extremely close fit for other regions of the specimens (resistant method, Siegel and Benson 1982). Analyses of Echinocardium were first done with RFTRA in order to determine whether strong heterogeneities occur in the distribution of the shape changes (extreme localized deformation on one or few landmarks: the "Pinocchio effect," Chapman 1990). Only the LSTRA approach is retained in the presentation of the results, because the shape changes recorded between the analyzed specimens are evenly distributed. Nevertheless, the analyses depart slightly from the classical approach by constraining the vector fields to be centered on the apical system (landmark 48, [ILLUSTRATION FOR FIGURE 5 OMITTED]) instead of on the centroid. This amounts to fixing the comparisons on the point at which new plates originate, such that the superimpositions become biologically significant. Besides, some authors (Bookstein 1990, 1991; Rohlf 1990) have emphasized the necessity of distinguishing between uniform and nonuniform components of shape changes. This would require the use of "deformation models" (e.g., thin-plate splines) instead of rotational fit (superimposition) methods. But, as Echinocardium data are symmetrical, the uniform component of the shape changes emphasizes elongation of the sea urchins and has to be considered with the other components of the change. Therefore, Procrustes methods are appropriate for the purposes of this study, all the more because they offer the possibility of depicting ontogenetic changes point-by-point (e.g., plate-by-plate for a sea urchin).

The program PROCRUSTES 2.0 (David and Laurin 1992) was used to perform the shape analyses. For multiple comparisons, the sum of the vector lengths ([Sigma][Delta]) was used as a metric to measure morphological distance between each pair of specimens and to fill a distance matrix. The matrix was then processed with the program FITCH of the package PHYLIP (Felsenstein 1990) to compute additive distance trees (this program offers the advantage of requiring no assumptions about equal rates of evolution).

RESULTS

Phylogenetic Analysis

The exhaustive search option of PAUP yields two equally parsimonious cladograms (21 steps, CI = 0.76) differing only in the position of E. lymani (for which there are three missing values in the data matrix). The phylogeny we will rely on for subsequent analysis is represented by the cladogram in which missing values are considered as plesiomorphic states [ILLUSTRATION FOR FIGURE 6 OMITTED]. The monophyly of the genus Echinocardium is based on two synapomorphies: an anal branch is added to the subanal fasciole, and the labrum is short and bordered by two pairs of ambulacral plates. The five species E. capense, E. flavescens, E. laevigaster, E. lymani, and E. mortenseni constitute an unresolved polychotomy (metaphyletic grouping), at the base of the cladogram. No unequivocal synapomorphy exists to resolve this bush into a hierarchy. Only E. lymani could be separated on the basis of missing values, but this resolution is without significance in the bootstrap results. The five other species constitute a monophyletic group, supported by two synapomorphies. This clade is further resolved into a "Hennigian comb" sequence. From lowest to uppermost branch, this sequence is: E. pennatifidum, E. mediterraneum, E. fenauxi, E. cordatum, and E. cordatum australe. Each branch is supported by several synapomorphies with few incongruencies. The bootstrap indicates that the basal and internal nodes of the pectinate part of the cladogram are relatively stable, with bootstrap values between 69% and 97%. It should be noted that the obtained phylogenetic pattern is consistent with the timing of appearance of derived morphologies as suggested by the fossil record. For example, the morphology of the most primitive Recent species is close to the morphology of the oldest species (Oligocene).

Character Analysis

The 18 characters retained for the cladistic analysis are discussed below. The homoplasies are presented as they appear on the cladogram in Figure 6.

1. Subanal fasciole. Synapomorphy: anal branch present. Plesiomorphic condition: no anal branch.

2. Labrum. Synapomorphy: short labrum. Plesiomorphic condition: elongated labrum.

3. Shape of the posterior petals. Synapomorphy: petal rows strongly divergent such that the petals have a triangular shape [ILLUSTRATION FOR FIGURES 1-3 OMITTED]. Plesiomorphic condition: petal rows almost parallel [ILLUSTRATION FOR FIGURE 4 OMITTED].

4. Relative size of the internal fasciole. Synapomorphy: the length of the internal fasciole reaches 50% of the test length [ILLUSTRATION FOR FIGURES 1-3 OMITTED]. Plesiomorphic condition: the internal fasciole is about 30% of the test length [ILLUSTRATION FOR FIGURE 4 OMITTED].

5. Architecture of the paired anterior ambulacra (II and IV). Synapomorphy: strong size discontinuity between intra- and extrafasciolar plates and angular path of the petal [ILLUSTRATION FOR FIGURE 1-2 OMITTED]. Plesiomorphic condition: progressive size increase from intra- to extrafasciolar plates [ILLUSTRATION FOR FIGURE 3-4 OMITTED].

6. Shape of the peristome. Synapomorphy: peristome reniform with a projecting labrum. Plesiomorphic condition: peristome semicircular.

7. Shape of the second ambulacral plate adjacent to the plastron (Ia2 or Vb2). Synapomorphy: plate 2 joining the labrum by narrow forward projection. Plesiomorphic condition: plate 2 in broad contact with the labrum.

8. Shape of the paired ambulacra. Synapomorphy: external rows of the anterior and posterior paired ambulacra (Ib-IIa and IVb-Va) form a continuous, concave or bow-like curve with each other [ILLUSTRATION FOR FIGURES 1-2 OMITTED]. Plesiomorphic condition: external rows of the anterior and posterior paired ambulacra (Ib-IIa and IVb-Va) straight and discontinuous [ILLUSTRATION FOR FIGURE 3-4 OMITTED].

9. Depression of the frontal ambulacrum (III). Synapomorphy: upper part of the frontal ambulacrum depressed in a continuous groove. Plesiomorphic condition: upper part of the frontal ambulacrum flush with the test.

10. Number of pore pairs of the frontal ambulacrum enclosed in the internal fasciole. Synapomorphy: many more than ten pore pairs enclosed in the fasciole [ILLUSTRATION FOR FIGURE 1 OMITTED]. Plesiomorphic condition: about ten pore pairs enclosed in the fasciole [ILLUSTRATION FOR FIGURES 2-4 OMITTED]. (See also character 13).

11. Relationships between subanal and anal fascioles. Synapomorphy: disjunct fascioles in E. fenauxi, E. cordatum, and E. cordatum australe. Convergence in E. pennatifidum. Plesiomorphic condition: confluent fascioles.

12. Number of plates of the posterior ambulacra (rows Ia and Vb) entering the subanal fasciole. Synapomorphy: plates 6, 7, 8, and 9 spreading into the fasciole in E. fenauxi, E. cordatum, and E. cordatum australe. Convergence in E. laerigaster. Plesiomorphic condition: plate 9 not within fasciole.

13. Number of pore pairs of the frontal ambulacrum enclosed in the internal fasciole. Synapomorphy: approximately 50 pore pairs enclosed within the fasciole. Plesiomorphic condition: fewer than 50 (usually either 10 or 30) pore pairs within the fasciole.

14. Arrangement of the ambulacral pores enclosed in the internal fasciole. Synapomorphy: pores arranged in irregular double series [ILLUSTRATION FOR FIGURE 1 OMITTED]. Plesiomorphic condition: pores arranged in regular series [ILLUSTRATION FOR FIGURES 2-4 OMITTED].

15. Architectural position of the fasciole within the frontal ambulacrum. Synapomorphy: fasciole crossing the ambulacrum on plates 6 or 7. Plesiomorphic condition: fasciole crossing the ambulacrum on plates 8 or higher.

16. Shape of the labrum. Convergence: labrum extended laterally such that it appears relatively short. Plesiomorphic condition: labrum extended backward such that it appears conspicuously longer than wide. Autapomorphy of E. pennatifidum: labrum strongly expanded laterally so that it appears much wider than long.

17. Primary tubercles on the apical side of interambulacra 2 and 3. Convergence: no primary tubercles. Plesiomorphic condition: primary tubercles present.

18. Shape of the adoral primary tubercles of interambulacra 2 and 3. Convergence: ridged primary tubercles. Plesiomorphic condition: crenulate primary tubercles.

Shape Analysis

As a first step, comparisons are made for nine adult specimens representing the largest of each species. The result is an additive tree of morphological distances in which the species E. capense, E. flavescens, E. laevigaster, and E. mortenseni, all belonging to the unresolved basal polychotomy of the cladogram, are extremely close to each other on the distance tree, displaying no hierarchy [ILLUSTRATION FOR FIGURE 7 OMITTED]. Pairwise comparisons within this set of species also attest to the very small shape differences separating them. The five other species are significantly separated from the previous group. They are arranged in a clear hierarchical pattern with an early to late branching sequence of E. pennatifidum, E. mediterraneum, E. fenauxi, E. cordatum, and E. cordatum australe. This topology is fully consistent with that of the cladogram.

To search for evolutionary processes involving developmental shape changes, the comparisons are extended to ontogenetic series. A matrix of distances between each pair of the 21 selected specimens allows construction of a tree in which the adult specimens display the same topology as in the analysis described above [ILLUSTRATION FOR FIGURE 8 OMITTED]. In addition, the growth stages are interposed between the adults, displaying a pattern that reflects the contribution of ontogeny to shape change. The interposition is organized such that all the ontogenetic series are ordered in the same direction: the younger specimens are the closer to the set of the four primitive species. This pattern is particularly clear for the most complete ontogenetic series of the two derived species E. pennatifidum and E. cordatum. The unique exception concerns the two specimens of E. flavescens, which are reversed, but they remain at the base of the tree, in a subset of specimens whose pairwise distances are small.

Ontogenetic Processes: Generalized Comparisons

The global structure of the previous distance tree suggests that the diversification of Echinocardium is probably underlain by heterochronic processes. Such developmental alterations involve changes in allometric trends, and their study requires the comparison of developmental sequences. Keeping [Sigma][Delta] as a metric for shape differences, it is possible to construct ontogenetic trajectories. For a given species, morphological distances are calculated between the smallest specimen of that species and each of the other specimens of the ontogenetic series. A specific ontogenetic trajectory is then constructed by plotting these successive distances against the size of the corresponding specimens. But to undertake a generalized comparison of the ontogenies of the various species, it is necessary to align all the trajectories within a common frame of reference. We have chosen to place the starting point of each specific trajectory in reference to the 8 mm long E. pennatifidum, which may be viewed as a general juvenile state. The trajectory of a species is then shifted of a magnitude equal to the distance between the juvenile E. pennatifidum reference point and the smallest specimen of that species. However, the distance [Sigma][Delta] expresses a difference regardless of the orientation of the vectors and its value can be the same for several geometrical configurations of the vector field. Therefore, it is necessary to ascertain that the discrepancies recorded between the trajectories are mostly due to differences in the vector lengths and not to significant perturbations of their orientations. This requirement is not completely satisfied by the species of the metaphyletic group; thus, the analysis of heterochronies is restricted to the fully resolved part of the cladogram.

All the examined trajectories are roughly parallel and the amount of ontogenetic change recorded per size unit retains the same order in the different species [ILLUSTRATION FOR FIGURE 9 OMITTED]. The distances between the juvenile E. pennatifidum and the other species increase progressively from E. mediterraneum and E. fenauxi to E. cordatum australe, and then to E. cordatum. This arrangement shows that the most derived species (according to the cladogram) exhibit the greatest differences and confirms the patterns given by the distance trees. Hence, the heterochronic process underlying the evolution of Echinocardium appears to be a global peramorphic trend that can be quantified according to the [Sigma][Delta] axis of the diagram.

Ontogenetic Processes: Pairwise Comparisons

To analyze precisely how heterochronic changes occur in the evolution of the genus, we need to focus on comparisons between pairs of species.

A first comparison involves E. pennatifidum (52 mm) and E. mediterraneum (16 mm and 45 mm). The morphological differences between large adult specimens of these two species is an expression of their phyletic divergence. The resulting vector field [ILLUSTRATION FOR FIGURE 10 OMITTED] shows quite strong differences located along the outline of the test (frontal part; midline of interambulacra 1 and 4) and along the internal fasciole (lateral and posterior parts). In E. pennatifidum [ILLUSTRATION FOR FIGURE 3 OMITTED], the plate pattern is not modified along the path of the fasciole. In contrast, on the test of E. mediterraneum [ILLUSTRATION FOR FIGURE 2 OMITTED] the plates that support the fasciole are specifically designed. These transformations consist in an extreme enlargement of the paired ambulacral plates that support the fasciole and to an intense compaction of the corresponding interambulacral plates. The posterior interambulacra 1, 4, and 5 are almost interrupted, and the part of the skeleton encircled by the fasciole appears isolated from the rest of the test. Correlatively, there is a strong alteration of the radiating pattern of the ambulacra. The differences that separate the two extreme ontogenetic stages of E. mediterraneum are also rather strong [ILLUSTRATION FOR FIGURE 11 OMITTED], and the geometrical configuration of the vector field is close to that observed in the former comparison. However, the discrepancies noticed between the young E. mediterraneum and the adult E. pennatifidum are extremely weak [ILLUSTRATION FOR FIGURE 12 OMITTED]. The average length of the vectors is small, and the previously described areas of intense changes do not display salient vectors. Therefore, it appears that the amount and nature of the shape transformations occurring during the ontogeny of E. mediterraneum are closely allied with the differences distinguishing the adults of the two species. Such a close correlation between ontogenetic and phylogenetic differences corroborates the peramorphic trend suggested above.

A second comparison, following the same approach between E. pennatifidum (52 mm) and E. cordatum (9 mm and 49 mm) yields the same general result as in the first comparison: similar strong differences separate the adults of the two species [ILLUSTRATION FOR FIGURE 13 OMITTED] as well as the ontogenetic stages of E. cordatum [ILLUSTRATION FOR FIGURE 14 OMITTED]; weak differences occur between the young E. cordatum and the large E. pennatifidum [ILLUSTRATION FOR FIGURE 15 OMITTED]. But the differences noted herein have neither the same intensity, nor the same location on the test of the sea urchins as in the comparison involving E. mediterraneum. The degree of peramorphosis is much stronger in E. cordatum than in E. mediterraneum (compare [ILLUSTRATION FOR FIGURES 10, 13 OMITTED]). There is in E. cordatum a major uniform component of the deformation actually corresponding to a relative backward shift in the position of the apical system that does not occur in E. mediterraneum. This relative displacement is linked with the balance between the anterior and posterior parts of the test (manifested in the multiplication of the plates in ambulacrum III). This accounts for a marked modification in the distribution of the main shape changes. The same geometrical configuration of the vector field is obtained when the comparison involves an adult E. fenauxi instead of E. cordatum. However, the vectors are shorter, revealing a smaller degree of peramorphic change.

DISCUSSION

Patterns and Processes in Echinocardium

The perfect congruence between the phylogenetic and the morphometric analyses (on two sets of largely distinct features) demonstrates that the phylogenetic relationships established in Echinocardium are strictly coupled with the amount of morphological change separating the species. In theory, the occurrence of shape similarities between two species A and B that are not sister taxa (phylogenetically belonging to two well separated groups) ought to be due either to a convergence between A and B or to reversions in A to ancestral states borne by B. Contrary to this theoretical case, the congruence observed in Echinocardium occurs because the features taken into account by the morphometric approach do not display notable homoplasies (i.e., convergences or reversions). Our result indicates that the changes in proportions of the test of Echinocardium, as revealed by the morphometric approach, occur without homoplasy and without drastic remodeling of the test.

According to the polarization implied by the cladistic analysis, the morphological and architectural evolution of Echinocardium, as depicted by the morphometric approach, appears to result from peramorphic processes. The peramorphosis corresponds to an architectural differentiation of the species that encompasses the belt of plates bearing the internal fasciole and the anterior ambulacrum. However, even if all the derived species of the genus are the result of peramorphic evolution, they do not follow precisely the same trend. According to the cladogram, there exists an increasing degree of modification of the fasciole and of the ambulacrum III from E. fenauxi to E. cordatum australe, and to E. cordatum that suggests a peramorphocline (McNamara 1982). This cline is also apparent in the increase in number of plates in ambulacrum III. However, a unique path, implying only an overgrowth of the ambulacral plates supporting the fasciole, leads to the architecture of E. mediterraneum. At the genus level, the peramorphosis is not organized according to a simple cline, as exemplified by the differences in the vector fields of E. mediterraneum and E. cordatum when compared with E. pennatifidum [ILLUSTRATION FOR FIGURES 10, 13 OMITTED]. Thus, despite that the species arrays are identical on the cladogram and the distance tree, the succession of species is not a morphological cline as distances of the same magnitude exist between species separated by two (or more) steps on the cladogram. In fact, the peramorphic evolution of Echinocardium canalizes the differentiation of the species in at least two constrained directions (as guided by allometries).

Theoretical Implications

Phylogenetic and morphometric approaches investigate the morphology of an organism through two complementary points of view: characters express evolutionary events in the former, and characters are supposed to describe an integrated body in the latter. To generalize, it appears worthwhile to combine morphometric approaches with phylogenetic analyses for two main reasons: to understand heterochronic processes and to trace the morphological implications of phylogenetic patterns.

The deciphering of heterochronies supposes the study of processes but should also be associated with a relevant evolutionary pattern independently established with cladistic approach. To this end, morphometric approaches using landmarks represent a more powerful tool for the study of heterochronic processes than classical dimensional analyses. Besides a precise description of shape independently of size (Laurin and David 1990b; Zelditch et al. 1992), they are especially efficient to make comparisons expressed as distances that can be directly considered in regard to a phyletic pattern.

Landmark approaches allow consideration of patterns of morphological relationships (distance trees) grounded on morphometric distances. The mapping of distance trees onto cladograms permits searches for congruencies and incongruencies that express two opposite situations.

(1) In the situation of full congruence, the less related species are also the more distant morphologically (and conversely). This suggests that there is no homoplasy (e.g., no convergence) in the characters used in the morphometric approach. Besides, the perfect congruence makes it tempting to use the morphometric results to measure the evolution. The distance issued from a vector field ([Sigma][Delta]) can legitimately be used as an objective estimate of the morphological gap between a pair of species, whatever the distribution of the vectors might be. The steps between successive branches of a cladogram thus can be linked to morphological gaps. But, because there is no necessary transitivity in the distances (i.e., [Sigma][[Delta].sub.AC] [not equal to] [Sigma][[Delta].sub.AB] + [Sigma][[Delta].sub.BC]), it is not appropriate to establish a clinal trend from the shape distances (at least without being sure of the geometrical similarity of the vector fields). In this case of full congruence, the evolutionary processes underlying the diversification of the study group may be suspected to result from one type of heterochrony (paedo- or peramorphosis), but not necessarily according to a single, simple clinal trend.

(2) In cases of incongruence, species phylogenetically close may be morphologically distant, as well as species morphologically close may be phylogenetically distant. The former circumstance supposes an evolution having led to an important morphological divergence with no effect on the relationships. This divergence can correspond to autapomorphies, some of them may have result from rapid allometric transformations of characters. The latter circumstance supposes an evolution with homoplastic events. The morphometric approach can then enhance the interpretation of these homoplasies. For instance, it might be possible to use the shape analysis to quantify the convergences and evaluate the inconsistencies between cladogram and distance tree.

In cases of incongruence, the genuine homology (or taxic homology as expressed by the cladistic approach) would be in opposition to the geometrical homology (or operational homology as expressed by the landmarks). Therefore, we must emphasize the fact that Procrustes approaches are only geometrical (in the true sense of the term) and should be viewed only as tools to answer questions previously formulated on accurate phylogenetic grounds.

In a classical phylogenetic approach, the stratigraphic data can be a posteriori superimposed on the cladogram to infer a phyletic tree. In the morphological approach proposed in this paper, the constraints introduced by complementary morphological characters are a posteriori superimposed on the cladogram to deduce influences of evolutionary processes within lineages and to interpret homoplasies.

ACKNOWLEDGMENTS

We are grateful to R. Mooi (California Academy of Sciences) for his insightful comments and the correction of the English in the manuscript. Improvements are due to our colleagues in the Paleontological Department of Dijon, and particularly J. L. Dommergues, as well as to J. Kim (Yale University) and an anonymous reviewer. We thank N. Cominardi of the Museum National d'Histoire Naturelie de Paris, D. L. Pawson, and C. Ahearn of the United States National Museum of Natural History, and the New Zealand Museum of Natural History for loaning us specimens. This work is a contribution of the Unite de Recherche Associee n [degrees] 157 du Centre National de la Recherche Scientifique, and partially funded by the "Institut National des Sciences de l'Univers" and the council of the "Region Bourgogne."

SYSTEMATIC ANNEX

The above analysis leads us to reconsider some aspects of the systematics of the genus Echinocardium. Within the unresolved set of five species at the base of the cladogram [ILLUSTRATION FOR FIGURE 6 OMITTED], only Echinocardium laevigaster and Echinocardium flavescens have autapomorphies allowing them to be identified unambiguously. Echinocardium laevigaster displays four pairs of ambulacral plates entering the subanal fasciole (character 12). This feature also exists in some other Echinocardium species and is here considered to be convergent. E. flavescens is very well characterized by the primary tubercles in the apical part of interambulacrum V, a characteristic that is a clear autapomorphy. The three latter species bear no characters allowing distinction between them. In addition, the morphometric comparisons show that they are extremely close to each other [ILLUSTRATION FOR FIGURE 7 OMITTED]. Consequently, we propose to synonymize Echinocardium mortenseni Thiery 1909 and Echinocardium lymani (Lambert and Thiery 1924) with E. capense Mortensen 1907. This is full agreement with some previous remarks emphasizing the overall similarity between these species (Clark 1917; Mortensen 1951; Baker 1969). One consequence of the synonymy is the enlargement of the geographic range of Echinocardium capense from the South Atlantic to Mediterranean Sea and to the Pacific Ocean.

Echinocardium capense Mortensen 1907

Synonymy. - Echinocardium capense Mortensen 1907. "Ingolf" Echinoidea. 2.: 137, pl. II figs. 5-6, 11, pl. XVI figs. 12, pl. XVII figs. 5-6, 9, 13, 16, 35, 39.

Echinocardium intermedium Mortensen 1907. "Ingolf" Echinoidea. 2.: 143, pl. XVII figs 14, 36, 46; Koehler 1909, Echinodermes des campagnes du Yatch "Princesse Alice": 240, pl. XXX figs. 2-6. (preoccupied name).

Echinocardium dubium A. Agassiz and H. L. Clark 1907. Bull. Mus. Comp. Zool. 51: 134; H. L. CLARK 1917, Hawaiian and other Pacific Echini: 265, pl. 150 figs. 1-3. (preoccupied name).

Echinocardium mortenseni Thiery 1909. Rev. Crit. Paleozool. 13: 137; MORTENSEN 1951, Monograph of the Echinoidea: 161.

Echinocardium capense; H. L. Clark 1917, Hawaiian and other Pacific Echini: 266; MORTENSEN 1951, Monograph of the Echinoidea: 160.

Amphidetus lymani Lambert and Thiery 1924. Ess. Nom. Rais.: 471.

Echinocardium lymani (Lambert and Thiery); MORTENSEN 1951, Monograph of the Echinoidea: 164; BAKER 1969, Records Dominion Mus., 6 (16): 270, pl. 2 figs. 1-4.

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