Parallel evolution controlled by adaptation and covariation in ammonoid cephalopods
© Monnet et al; licensee BioMed Central Ltd. 2011
Received: 13 September 2010
Accepted: 29 April 2011
Published: 29 April 2011
A major goal in evolutionary biology is to understand the processes that shape the evolutionary trajectory of clades. The repeated and similar large-scale morphological evolutionary trends of distinct lineages suggest that adaptation by means of natural selection (functional constraints) is the major cause of parallel evolution, a very common phenomenon in extinct and extant lineages. However, parallel evolution can result from other processes, which are usually ignored or difficult to identify, such as developmental constraints. Hence, understanding the underlying processes of parallel evolution still requires further research.
Herein, we present a possible case of parallel evolution between two ammonoid lineages (Auguritidae and Pinacitidae) of Early-Middle Devonian age (405-395 Ma), which are extinct cephalopods with an external, chambered shell. In time and through phylogenetic order of appearance, both lineages display a morphological shift toward more involute coiling (i.e. more tightly coiled whorls), larger adult body size, more complex suture line (the folded walls separating the gas-filled buoyancy-chambers), and the development of an umbilical lid (a very peculiar extension of the lateral shell wall covering the umbilicus) in the most derived taxa. Increased involution toward shells with closed umbilicus has been demonstrated to reflect improved hydrodynamic properties of the shell and thus likely results from similar natural selection pressures. The peculiar umbilical lid might have also added to the improvement of the hydrodynamic properties of the shell. Finally, increasing complexity of suture lines likely results from covariation induced by trends of increasing adult size and whorl overlap given the morphogenetic properties of the suture.
The morphological evolution of these two Devonian ammonoid lineages follows a near parallel evolutionary path for some important shell characters during several million years and through their phylogeny. Evolution of some traits (involution, umbilical lid) appears to be mainly driven by adaptation to improve the hydrodynamic properties of the shell, whereas other characters (sutural complexity) evolved due to covariation with features that play a central role in the morphogenesis of mollusc shells. This example provides evidence that parallel evolution can be driven simultaneously by different factors such as covariation (constructional constraints) and adaptation (natural selection).
Independent evolution of similar biological traits in two different lineages branching off from the same ancestor defines parallel evolution [1–3]. It is a common phenomenon described for many animal clades (see e.g., [4–13]), including molluscs [1, 14–19]. Repeated patterns of parallel evolutionary change of phenotypic traits are commonly regarded as evidence of adaptation under common selection pressures such as common environmental factors [20–22], therefore illustrating natural selection's major role in shaping morphological evolution and the repeatability of evolutionary processes. Several additional processes have been proposed that could contribute to the fabric of parallel evolution. However, the contribution and conditions in which these various processes trigger parallel morphological evolution are still insufficiently investigated. Furthermore, understanding the processes involved in parallel evolution is also important for solving systematic problems and thus to estimate evolutionary rates and diversity .
Evolutionary steps in two independent lineages will never be absolutely identical [1, 15, 16, 23, 24]. Nevertheless, morphological (phenotypic) evolutionary trends do occur in independent lineages and can display striking parallel changes (for a Recent mollusc example, see ). Here, the term parallel evolution is used in a broad sense, implying that not all parts of the organism undergo parallel evolutionary transformations and that the trends are nearly parallel, resulting in very similar organs/structures in a phylogenetic series of more than one species in at least two lineages.
Parallel evolution is often difficult to differentiate from convergence (evolution from two different stages of separate lineages toward an evolutionary stage that has evolved striking similarities among some phenetic, genetic or other traits; ) and some authors have even suggested a continuum between convergent and parallel evolution [2, 26]. The distinction between convergent, parallel, and divergent evolution indeed requires the historical evolutionary aspect of studied lineages. Because it is the only direct evidence of evolution in the past over long time spans, palaeontological data can provide important insights into patterns and processes of parallel evolution.
In the fossil record, the Ammonoidea (Cephalopoda, Mollusca) are well-known to display large-scale morphological macroevolutionary trends [27–39]. These marine extinct cephalopods with an external, chambered shell have repeatedly been proven to be valuable study objects to develop or test evolutionary hypotheses [27, 29, 34–36, 40–50]. Besides, ammonoids "are for palaeontologists what Drosophila is in genetics" . Their usefulness in evolutionary biology originates in their high evolutionary rates, high taxonomic diversity and morphological disparity, and usually well-known stratigraphic (i.e. temporal) framework (see [52–54]). However, such morphological evolutionary trends among ammonoids have been rarely discussed and quantified in detail [38, 39, 47, 55–58]. Knowledge of details in such lineages with seemingly "directed" morphological changes is of great interest, because not all evolutionary morphological changes in the ammonoid shell have the same causes. On the one hand, some evolutionary changes in ammonoid shell morphology may be constrained by covariation (e.g., Buckman's laws of covariation ; see discussion) and may thus be a result of constructional and/or developmental constraints. On the other hand, cases of parallel evolution of oxyconic shells (i.e. slender, compressed conchs with acute venter) in various lineages of ammonoids have been repeatedly documented and interpreted as adaptations to rapid and/or improved swimming (e.g., [58, 60–63] and see discussion) and thus as a result of natural selection.
In the present ammonoid case study, we first describe and investigate the morphological evolutionary patterns of both families along their phylogenetic sequence (i.e. their phylogenetic order of appearance) with bivariate plots of quantitative characters of the ammonoid shell. Then, we identify and evaluate statistically the characters, which may have evolved in parallel and identically. Finally, we try to decipher the characters, which evolved identically because of covariation (constructional constraints) and/or because of adaptation (selective constraints).
The maximal diameter (Dmx) is the maximal shell diameter known for each species and is used to approximate the adult body size of the ammonoid species under consideration.
The whorl expansion rate (WER) is a measure of the proportional increase of shell diameter through growth (initially defined by [97, 98], but we used the equation of , which is much easier to apply on actual specimens). It is considered one of the most important and biologically meaningful parameters because it roughly reflects the growth rates of the coiled shell tube and strongly correlates with body chamber length, soft part volume and the syn vivo-orientation of the shell [58, 97–99].
The whorl shape compression (WSC) is a measure of the ellipsoid of the whorl section of the ammonoid shell aperture, which is a very important ammonoid taxonomic character due to the accretionary growth of the shell.
The umbilical width index (UWI) is the ratio between the umbilicus and the shell diameter and thus approximates the amount of shell coiling (degree of involution).
The imprint zone rate (IZR) describes the relative overlap of two succeeding whorls in terms of height.
The flank convergence index (FCI; modified after ) approximates the relative compression of the ventral part of the shell compared to its dorsal part (i.e. acute vs. low-arched rounded venter).
The number of lobes (NLb) approximates the indentation of the suture line, which is the junction line of the septa (chamber walls) with the internal side of the shell. Here, we counted only the lobes on one flank, including those in the plane of symmetry (i.e. internal and external lobes).
Last, the relative depth of the lateral lobe (= "O-lobe" of ; OLb), which is the ratio between width and height of the lateral lobe, measured from the apertural apices of the neighbouring saddles (see Figure 4).
All available specimens of the two families have been measured to quantify these characters. Most data are based on own measurements and some were taken from the literature [66, 76, 77, 88, 95]. The material referred to in this paper is housed in the following institutional collections: Palaeontological Institute, Moscow (PIN); Palaeontological Institute and Museum, University of Zürich (PIMUZ); National Museum, Prague (L 11705); Institute for Geosciences, University of Tübingen (GPIT).
The eight quantitative parameters are composed of one size measure (Dmx), six ratios (WSC, WER, UWI, IZR, FCI, OLb) and one ordinal count (NLb). For Dmx, FCI, NLb and OLb, only the adult value of each species is reported and not juvenile values, because these parameters always lie near structural boundaries at hatching (e.g., the suture is simple and will necessarily increase its complexity through growth; see discussion).
We here consider parallel evolution in a broad sense by assuming that not all characters are involved in the parallel evolution and by not assuming that evolutionary changes are accomplished by similar alterations in the developmental program (contra [2, 102]). From these definitions, parallel evolution of some characters can be identified when the evolutionary trajectories of the studied lineages in the morphological space defined by this subset of characters (1) start with the same morphotypes, (2) evolve in parallel and are overlapping, and (3) end with the same forms. In other words, the evolutionary trajectories are identical in origin, magnitude and direction. This pattern of parallel evolution must be distinguished from parallelism in phenotypic space. This different phenomenon concerns lineages having parallel trajectories (same direction), but not necessarily the same origin and/or magnitude (for an example of parallelism but not parallel evolution, see , p. 828, figure 3C). It has to be taken into account that the likelihood of (1) finding statistical support of parallel evolution as well as of (2) parallel evolution itself to occur is dramatically reduced when the evolutionary transformations change more often in several aspects (direction, quality, quantity, proportion) in both lineages. Simple cases of parallel evolution are thus easier to test but less meaningful with respect to selective forces and vice versa.
In order to assess the parallel evolution of the two studied lineages, we use two different approaches, both based on a multivariate analysis using the subset of characters previously identified to be potentially involved in this case of parallel evolution. Note that univariate approaches can suffer from a "dimensionality bias" and similarities of trajectories in a morphospace should preferably be tested multivariately [121, 122]. First, the parallel evolution of this subset of characters is evaluated by means of a method developed for comparing evolutionary trajectories of phenotypic change . According to this method, the phenotypic evolution of a lineage is defined as a trajectory across a set of evolutionary levels in a multivariate morphological space. Attributes of these trajectories (magnitude, direction and shape) are quantified and statistically compared across pairs of taxa by means of a residual randomization permutation method [123, 124], and a summary statistic is used to determine the extent to which patterns of phenotypic evolution are concordant. Note that the method currently requires that the compared trajectories have the same number of evolutionary levels (i.e. in our case the same number of species). Since more species of pinacitids have been described, the analysis is performed by first merging the data of the phylogenetically closest species of the pinacitid lineage in order to obtain the same number of studied evolutionary levels or steps for both families. The two species of Pinacites have thus been merged, as well as Foordites succedens with F. platypleurus and Achguigites with Fidelites. This constraint of the method reduces the power of the test since the species of different lineages cannot be considered as equivalent.
The second method to test the parallel evolution of these Devonian ammonoids follows the approach proposed by  for comparing ontogenetic trajectories. This method is a permutation test based on within-lineage multivariate regression of the characters hypothesized to be involved in the parallel evolution. If the two lineages evolved in parallel, then their phylogenetic trajectories are identical in the morphological space defined by the subset of characters involved. To test this hypothesis, we first compute for each lineage separately a linear total least square regression, then we sum the squared orthogonal distance for each specimen from its nearest point on the regression curve. This sum provides the original test statistic for subsequent comparison. Then, we randomly resample without replacement a large number of times the taxonomic assignment of studied specimens to the two lineages and recompute the summed squared distances of these permuted families (this provides the permutation distribution). If the two studied lineages evolved in parallel, the original test statistic should not be an outlier in the permutation distribution of summed squared distances (see ). In other words, permuting specimens' affiliation does not increase the residuals of the multivariate regressions and this is possible only if specimens of both families are close together in the studied morphological space.
Evolution of Auguritidae (Early Devonian)
The evolution of shell characters through the phylogenetic sequence of the lineage that includes the Auguritidae is described and reported in Figures 5, 6, 7 and 8. Within this lineage, several evolutionary trajectories can be empirically suggested: the adult shell size (Dmx), whorl shape compression (WSC), number of lobes of the suture (NLb) and relative depth of the lateral lobe (OLb) increase simultaneously with decreasing umbilical diameter (more tightly coiled shells; UWI). The whorl expansion rate (WER) also increases slightly. The flank convergence index (FCI) and imprint zone rate (IZR) fluctuates without emerging trends.
Of great interest is the general trend of increasing involution (more tightly coiled shells as shown by the decreasing UWI, Figure 6). Indeed, most ammonoid specimens of lower Emsian age are very openly coiled and share a wide umbilical perforation . It is striking that all forms of this lineage are still associated with loosely coiled Anetoceratinae (Figure 3E; see references in the background section), which indicate that their evolution must have been comparably fast. In addition to this trend toward a closed umbilicus, the lineage is characterized by the appearance of an umbilical lid. Although the most derived forms of this lineage are rather rare, re-examination of the material from the Urals (Russian) and the Zeravshan Range (Uzbekistan) in the Palaeontological Museum of Moscow [75, 93] and new specimens from Morocco  reveals that the two most derived genera Weyeroceras and Celaeceras both possess extensions of the lateral shell wall covering the umbilicus (i.e. umbilical lid; Figures 3, 7). This structure was previously known in this form only from the pinacitids . Noteworthy, the trends toward more compressed (WSC) and more involute (UWI) shells levelled off with the appearance of the umbilical lid. The appearance of the umbilical lid is also associated with the smallest UWI (almost closed umbilicus).
Evolution of Pinacitidae (Early and Middle Devonian)
The evolution of shell characters for the lineage that includes the Pinacitidae and which evolved from the same remote ancestor of auguritids is reported in Figures 5, 6, 7 and 8. Within this lineage, the adult shell size (Dmx), the number of lobes of the suture (NLb) and their relative depth (OLb), as well as the acuteness of the venter (FCI) increased simultaneously, especially among the more derived species. The umbilical width index (UWI) and the imprint zone rate (IZR) also display trends but these occur only among the more primitive species. Evolutionary changes of whorl shape compression (WSC) and whorl expansion rate (WER) display different, slightly more complex evolutionary patterns: a quick increase in the most primitive species, an abrupt reset and then a slight increase in the most derived species, giving the trend a sigmoid course.
This lineage is better known, much more abundant and more diverse than auguritids. The pinacitids had a nearly cosmopolitan distribution during the Middle Devonian (see Figure 2B; [87, 88]) and even the most derived representatives were locally quite common. Like in the auguritids, the derived species of pinacitids acquire more oxyconic shells and more complex sutures, as well as an umbilical lid. With the appearance of the umbilical lid, the trends toward greater involution (decreasing UWI) and whorl overlap (IZR) levelled off (Figure 6). This levelling off may correspond to a "left-wall" effect, i.e. the trend cannot go further once the umbilicus is closed, because the closure of the umbilicus marks a constructional boundary (whorls completely overlap).
Parallel evolution of the two lineages
The results of the morphological principal components analysis are plotted in Figure 8. The first three components extracted from the dataset accounted for 79.4% of the morphological variation. The PCA plots indicate which shell characters contribute to the morphological evolution of Devonian ammonoids by creating high variation. Vectors of shell characters (length and direction compared to the PC axes) revealed that variation on PC1 is mainly associated with Dmx, WSC, NLb/OLb, FCI and UWI, PC2 with WER and IZR, and PC3 with WSC. When viewed in the PC1/PC2 plot (Figuer 8), the morphological evolutionary trajectories of Auguritidae and Pinacitidae display a seemingly pattern of parallelism. However, this pattern is absent on other PC axes and is thus an artefact of projection onto a reduced number of axes (compare figure 5 in ). Noteworthy, it does not reflect the case of parallel evolution discussed here, since this PCA is based on the eight quantitative characters and not only those really evolving in parallel (see below). Finally, this principal component analysis shows that the two studied clades are clearly distinct morphological clusters even if related to a common ancestor, because they occupy distinct areas of morphospace. Therefore, even if these lineages experience a parallel evolution of some characters (see below), each lineage is clearly distinct and has its own evolutionary history. The auguritid lineage has also a more irregular evolutionary trend than the pinacitid clade. This higher inter-specific variation probably originated from the poorer database and the fewer evolutionary steps for this rare family.
Both ammonoid lineages display empirical morphological evolutionary trends of some shell characters. Their statistical evaluation by means of the method of  is illustrated and reported in Figure 9. Among the three tested evolutionary patterns (directed trend, GRW; random trend, URW; stasis), the studied quantitative characters are mainly characterized by random trends and/or stasis (Akaike weights of URW or Stasis > 0.5). The only well-supported directional trend (GRW > 0.5) is for UWI (increasing involution) in the pinacitids, as well as in the auguritids if we remove one "outlier species" (Figure 9). Hence, this suggests that, except for UWI, the two ammonoid lineages have no directed evolutionary changes of their morphology. However, we must acknowledge that the power of this statistical test is reduced by the current state of our data. First, although we managed to acquire a comprehensive dataset from a palaeontological point of view, the number of species and specimens in the studied dataset remains low. Second, the studied ammonoids display important ontogenetic changes [88, 125], which largely increase the variance and range of studied characters. However, the scarcity of well-preserved, adult specimens of these earliest ammonoids prevents using only adult values. If we relax the necessary statistical support, two studied shell characters may display possible directed trends for both lineages: Dmx and NLb, which have negligible values for stasis and low but not negligible support for GRW. By comparison with other ammonoid groups [28, 29, 31–33, 35, 36, 39], trends in these two characters are expectable, but it remains to be tested by additional material in the future. Nevertheless, all other characters remain devoid of directional trends. Thus, the two studied lineages share the same directed trends for UWI with certainty, and more hypothetically for Dmx and NLb. Finally, it also appears plausible that the evolutionary trajectories for these three characters end with forms having equal means: for UWI, the last auguritid and the last pinacitid have no significant difference in their mean (Welch t = -1.588, p = 0.139); for Dmx, the last auguritid has the same value has the penultimate pinacitid but the last pinacitid is larger than the last auguritid; and for NLb, both lineages have at the end the same number of suture elements. This is also suggested graphically in Figure 9.
Using the regression approach of , it appears that the hypothesis of parallel trajectories of the two studied lineages cannot be rejected (p = 0.019), but the value is low (Figure 10B). The statistical evidence for the parallel evolution in UWI, Dmx and NLb of auguritids and pinacitids is thus controversial between the two approaches we used. As discussed previously, our sparse and unbalanced dataset is probably responsible for the low power of these statistical tests. Additional data are thus required to better test this hypothesis of parallel evolution. Noteworthy, both lineages developed the peculiar umbilical lid, not known in any other ammonoid group. It still appears likely that auguritids and pinacitids evolved in parallel with respect to the increasing involution, adult size, suture complexity and evolution of an umbilical lid.
In summary, this probable but not fully proven case of parallel evolution included the following quantitative and qualitative traits and their corresponding evolutionary trends (Figuers 5, 6, 7, 8 and 9): (1) adult body size (Dmx: from less than 50 mm to more than 150 mm for auguritids and 300 mm for pinacitids); (2) umbilical width (UWI: from moderately wide to closed; and with formation of an umbilical lid by extending the lateral shell wall across the umbilicus); (3) sutural complexity (NLb: from simple to more complex by ventral and umbilical insertion of accessory elements); (4) siphuncle position (not quantified: from ventral to subventral, see e.g. Figuer 3H); (5) aperture shape/whorl cross section (from platycone to oxycone, i.e. more compressed shell and/or more acute venter); and (6) shape of venter (not quantified: from rounded to acute; Figuer 7). These trends occurred in a phase that lasted ca. 10 My from the last common ancestor of both lineages to the extinction of the last representative of the pinacitids. As shortly discussed in the introduction, parallel evolution is never exact and never includes all traits of the members of the lineages under consideration. Differences between the two ammonoid lineages can be seen in the following traits for example (Figuers 5, 6, 7, 8 and 9): (1) adult body size (Dmx: both increasing, but pinacitids reach over twice the size of the auguritids); (2) whorl overlap (IZR: trend and higher values for pinacitids); (3) suture line (higher values of OLb for pinacitids); and (4) aperture shape/whorl cross section (both from platycone to oxycone, but by increasing WSC for auguritids and increasing FCI for pinacitids).
Parallel evolution could theoretically have various causes such as chance, genetic heritage, covariation/developmental constraints, and/or adaptation/selection. In the context of cases of protracted parallel evolution of more or less complex structures or organs, which comprise many taxa in the lineages under consideration, the likelihood is very low that this parallel evolution is a result of sheer chance. Therefore, it is necessary to determine which causes contributed how, and to what degree to the documented evolutionary parallel and identical trends. In the case of auguritids and pinacitids, covariation of some traits is evident while we can suggest adaptation for other morphological aspects of the shell.
Functional traits (adaptation)
Among the documented parallel morphological evolutionary trends, the most important are: increasing involution (more tightly coiled whorls toward a closed umbilicus); development of an oxyconic shell (more compressed shell and/or more acute venter); larger shell diameters (body size); and the terminal acquisition of an umbilical lid.
The increasing body size of both studied lineages constitutes an example of Cope's rule, known as the widespread tendency of animal groups to evolve toward larger body size [126–129]. This type of trend has been attributed to certain advantages of size increase such as increased defence against predation, increased food competition, increased success in mating, increased individual longevity, and better energy use [20, 126–128, 130–132]. Since the lineage starts with small shells, the observed trend toward a larger shell size conforms to the traditional gradualist and adaptive interpretation that large-scale evolutionary trends result from persistent selection within long-ranging lineages. Several authors have illustrated examples of increasing ammonoid shell size during initial radiation of a group [46, 129, 133, 134]. However,  found no evidence for Cope's rule among Early Jurassic ammonoids, after the initial recovery radiation following the Triassic/Jurassic boundary extinction.
The persistent increasing involution (i.e. more tightly coiled whorls toward a closed umbilicus) coupled with the oxyconic shell as displayed by the auguritids and pinacitids is surely one of the most frequently observed large-scale morphological evolutionary trends among ammonoids [27, 28, 31–33, 38, 39, 66, 136–139]. This highly recurrent trend among numerous and distantly related ammonoid clades (thus independent of phylogeny) suggests that it may have a strong adaptive significance due to functional constraints [140, 141]. Since ammonoids are an extinct group, we have no direct evidence of the cause and advantage of this possible adaptation. However, thanks to mechanical experiments on shell models and analytical calculations of shell hydrodynamics [61–63, 99, 142–144], as well as by analogy with Recent nautiloids (the only extant cephalopod with a chambered external shell; see [145, 146]), numerous studies evaluated the hydrodynamic performances (locomotion) of the ammonoid shell shape. It has been widely demonstrated that, for shells with oxyconic shell shapes, the energy consumption for swimming is the lowest and potential maximal swimming speed is the highest. Manoeuvrability is best with roughly horizontal apertures at relatively short body chambers and more or less high whorl expansion rates [58, 60, 62, 63, 147]. Indications for a link between water energy, facies and conch form are not rare but only few publications on that matter are available [55, 57, 88, 139, 148–155]. Increased involution of the shell (decreased UWI) therefore appears to represent a consistent adaptation toward improved hydrodynamic properties of the shell (decreased drag, increased streamlining) and consequently probably improved predation efficiency, increased food competition, increased predator escape, and/or improved search for mating partners and suitable spawning regions. Hence, the parallel and identical trend of ammonoid shell involution in the Auguritidae and Pinacitidae is here suggested to be best and most plausibly explained by functional adaptation.
The umbilical lid could represent an adaptation for the improvement of the hydrodynamic properties of the shell. Indeed, it has been shown repeatedly that the size and shape of the umbilicus in combination with the overall shell geometry has a profound influence on the hydrodynamic properties of the shell [57, 61–63, 142]. For instance, forms with a closed umbilicus reduce added mass (such as the water trapped by the umbilicus) and confer better acceleration and deceleration during swimming . In this context, this hypothesis supports the adaptation to improve swimming, but it does not explain completely why the umbilical lid is constructed in such a peculiar way in only these two groups.
In addition to the previous hypothesis, the umbilical lid could act as a device directing water into the mantle cavity from behind when swimming backwards by means of jet propulsion. Indeed, most cephalopods swim "backwards" by taking in water into the mantle cavity and by expelling this water by mantle cavity compression through the hyponome (e.g., ; for a discussion on the functional analogy between ammonoids and Nautilus, the only extant cephalopod with an external shell, see [63, 146]). Note that all recent and all fossil cephalopods still have or had a hyponome . This is corroborated by the presence of a hyponomic sinus in our forms just like in Nautilus . In this case, the umbilical lid has hydrodynamic advantages because the water enters from the swimming direction and leaves in the opposite direction (i.e. in the direction of the aperture, where the animal came from) with a deviation through the mantle cavity where it is accelerated by the animal's musculature (Figuer 11). Furthermore, the umbilical lid is not formed at the beginning of ontogeny but rather at a diameter of about 5 mm. This roughly coincides with the size when swimming movements become more effective in the course of ammonoid development [62, 63], thus supporting a link between shell hydrodynamics and the evolution of the lid. True evidence for this function is missing, but both lineages lived in a time when a general increase in mobility among swimming animals occurred .
Finally, the umbilical lid might have been caused by, or linked to, features unrelated to the hard parts (e.g., soft-tissues, genes). For instance, the parallel evolution of an umbilical lid may speculatively result from the repetitive loss of expression of regulatory Hox genes (e.g., ; for the description of such a case in the evolution of crustacean maxillipeds, see ) or the repeated selection of developmental genes (see e.g., [10, 160]). Logically, this is impossible to test on Devonian fossils. Furthermore, the genetic underpinnings of parallel and convergent evolution are generally unknown in Recent organisms . Although it is not yet possible to find evidence for another function of this lid, it appears likely that it served indeed as a structure to improve swimming abilities.
Covarying traits (constructional constraints)
Among the documented parallel morphological evolutionary trends, some can be explained as covarying traits, meaning that some morphological trends can result from constructional constraints [39, 162–165]. The characters involved in such indirectly triggered trends are important to identify because, in this case, there is no need to search for an adaptive or genetic explanation.
Covariation of shell characters is well-known for ammonoids . For instance, the intraspecific variation of an ammonoid species is usually expressed by the following gradient: the more evolute the shell, the thicker the whorl shape, and the more robust the ornamentation. It is referred to as Buckman's first law of covariation [59, 163, 167, 168] and has been abundantly documented and discussed (e.g., [38, 169–174]). Shape and differentiation of suture lines (i.e. the kind and degree of folding of the phragmocone chamber walls) also covary with shell shape and shell size (Buckman's second law of covariation). More precisely, the number of suture elements (frilling of the suture line) increases with the size of the shell (whorl height) and/or with the compression of the shell. This is evidenced by the widely documented increase in the suture complexity through ontogeny of the ammonoid shell (for Devonian taxa see, e.g., [47, 66, 93]; see also inside frame of Figure 7). Furthermore, both patterns are usually linked because in most ammonoid ontogenies, a more or less rapid change from more circular to either compressed or depressed apertures happened (see Figure 7). During this change in whorl section, the relative number of suture elements changes in such way that less suture elements occur when the whorl cross section is closer to a circle, and vice versa [51, 175]. Both patterns are abundantly documented for all ammonoid groups (e.g., [44, 47, 55, 60, 66, 93, 95, 176–184]).
The function of the septal folding is the subject of much debate (e.g., [150, 185, 186]) and many hypotheses have been proposed, such as buttressing [144, 187, 188], muscle attachment , cameral liquid transfer , metabolic effect , developmental epiphenomena [175, 192–194], and/or locomotion . Nevertheless, the increase with size and through ontogeny is expected because septal formation behaves like a "viscous fingering" phenomenon (see review of ); in this morphogenetic model, the details (not the general outline) of the suture pattern depend on the space and shape available for the suture during its formation ("domain effect").
Very early in the course of the evolution of the Ammonoidea, the two families Auguritidae and Pinacitidae evolved independently but display a striking pattern of probably parallel morphological evolution. These two families share several essential morphological traits such as shell shape, suture line course, and the presence of an umbilical lid, which is an extension of the lateral shell wall and is unknown in this form from any other ammonoid lineage. The similar and parallel evolution of both lineages toward large, involute shells with more complex suture lines and with closed umbilicus including the formation of an umbilical lid can be explained best by selection for enhanced hydrodynamic properties of the shell (selective/adaptive constraints). Speculatively, the umbilical lid might have facilitated the intake of water from the swimming direction during repulsion swimming. Some other shell parameters also show a parallel evolution, but most likely due to covariation (constructional constraints). The increase in sutural complexity represents a typical case of covariation induced by the evolution toward involute and larger shells with acute venter and deep imprint zone.
Covariation and adaptive constraints are thus not mutually exclusive and both can contribute to parallel evolution of ammonoid lineages. Constructional constraints belong therefore to the primary factors governing evolutionary trends of the ammonoid shell, indirectly triggered by adaptive trends. Furthermore, this underlines that form, and the controls upon it, can never be truly understood in isolation from functional adaptation and constructional covariation. Distinction between covariation and adaptation in the process of evolutionary trends is also important in order to avoid over-interpretation of the patterns; in such cases, detailed studies of convergent or parallel evolutionary trends can contribute important impetus toward a decision for either cause. For instance, recurrence of particular combinations of morphology and their strong independence of phylogeny are commonly regarded as strong arguments for functional constraints. The evolutionary recurrence of these combinations of characters depends partially on selection for certain functional aspects (e.g., trend of increased involution induced by selection for improved hydrodynamic properties), and partially on shell morphogenesis and associated covariation following functional adaptations (e.g., trend of increased suture complexity induced by size- and involution-increase trends), thus representing "fabricational noise" [162, 196] (i.e. constructional constraints). In other words, evolutionary transformations that occurred in these ammonoid lineages may be directly or indirectly linked to some kind of adaptation, but not all innovations are necessarily functional. For instance, some authors have interpreted the adaptive signification of sutural complexity, especially to water depth against implosion (for a discussion and references, see e.g., [144, 190, 197]). Such interpretations are questionable because trends in suture complexity may be (at least partially) a side effect and not the target of evolution. Furthermore, several studies also tried to demonstrate the increasing complexity of life by focusing on the ammonoid suture complexity (e.g., [36, 198, 199]). All these studies resulted in more or less equivocal results and this may be explained by the fact that many changes in suture patterns can be induced by covariation. It is thus crucial for phylogenetic analyses, especially at higher systematic ranks , to understand the driving factors behind evolutionary morphological modifications, whether they are driven by some selective force, sheer covariation or even random processes.
Those evolutionary trends which are not parallel between the two studied groups also highlights that these are independent characters of the ammonoid shell. Hence, although adaptation and covariation largely shape the morphological evolution of ammonoids, the still divergent evolution of several shell characters of both lineages in our case of parallel evolution imply that the unique histories of organisms still play a large role in shaping the evolutionary trajectory of clades . As large-scale macroevolutionary studies can only proceed gradually, we hope that further fossil discoveries and the application of new methods and better knowledge of mollusc shell morphogenesis (see e.g., [164, 165]) will help to test the hypotheses advocated in this paper, and continue to reveal information about the evolutionary history of this major marine extinct group, the ammonoids.
The field work in Morocco was kindly supported by the Swiss National Science Foundation (project number: 200021-113956/1 to CK). The Moroccan colleagues of the Ministère de l'Energie et des Mines (Rabat and Midelt) and the Uzbek colleagues from the State Committee on Geology and Mineral Resources of the Republic of Uzbekistan (Tashkent) and the Kitab State Geological Reserve benignly provided permits for the field work and for the export of samples. We greatly appreciate the patient help of N. A. Meshankina, F. A. Salimova (Tashkent), U. D. Rakhmonov (Kitab) during our field work in the Kitab State Geological Reserve (Uzbekistan). V. Konovalova, S. Nikolaeva and T. Leonova (all Moscow) supported us during our visit at the Palaeontological Institute in Moscow. V. Turek (Prague) kindly examined and photographed the holotype of Celaeceras praematurum for us and also supported us during our museum visit in Prague. R. Montesinos (A Coruña) kindly supplied photos of the Spanish Weyeroceras specimens. M. Wasmer and J. Rath are thanked for donations of ammonoid specimens. L. Wilson (Zürich) kindly corrected the English of the manuscript. The constructive comments of an anonymous reviewer and of A.J. McGowan have been greatly appreciated and contributed to improve this manuscript.
- Serb JM, Eernisse DJ: Charting evolution's trajectory: using Molluscan eye diversity to understand parallel and convergent evolution. Evolution: Education and Outreach. 2008, 1: 439-447. 10.1007/s12052-008-0084-1.Google Scholar
- Gould SJ: The structure of evolutionary theory. 2002, Cambridge, Harvard University PressGoogle Scholar
- Revell LJ, Johnson MA, Schulte JA, Kolbe JJ, Losos JB: A phylogenetic test for adaptive convergence in rock-dwelling lizards. Evolution. 2007, 61: 2898-2912. 10.1111/j.1558-5646.2007.00225.x.PubMedView ArticleGoogle Scholar
- Palmer AR: Predation and parallel evolution: recurrent parietal plate reduction in balanomorph barnacles. Paleobiology. 1982, 8: 31-44.View ArticleGoogle Scholar
- Sheldon PR: Parallel gradualistic evolution of Ordovician trilobites. Nature. 1987, 330: 561-563. 10.1038/330561a0.PubMedView ArticleGoogle Scholar
- Reznick DN, Rodd FH, Cardenas M: Life-history evolution in guppies (Poecilia reticulata: Poecilidae). IV. Parallelism in life-history phenotypes. American Naturalist. 1996, 147: 319-338. 10.1086/285854.View ArticleGoogle Scholar
- Averoff M, Patel NH: Crustacean appendage evolution associated with changes in Hox gene expression. Nature. 1997, 388: 682-686. 10.1038/41786.View ArticleGoogle Scholar
- Morrison CL, Harvey AW, Lavery S, Tieu K, Huang Y, Cunningham CW: Mitochondrial gene rearrangements confirm the parallel evolution of the crab-like form. Proc R Soc Lond B. 2002, 269: 345-350. 10.1098/rspb.2001.1886.View ArticleGoogle Scholar
- Schluter D, Clifford EA, Nemethy M, McKinnon JS: Parallel evolution and inheritance of quantitative traits. American Naturalist. 2004, 163: 809-822. 10.1086/383621.PubMedView ArticleGoogle Scholar
- Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM: Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin allelles. Science. 2005, 307: 1928-1933. 10.1126/science.1107239.PubMedView ArticleGoogle Scholar
- Shapiro MD, Bell MA, Kingsley DM: Parallel genetic origins of pelvic reduction in vertebrates. Proc Natl Acad Sci USA. 2006, 103: 13753-13758. 10.1073/pnas.0604706103.PubMedPubMed CentralView ArticleGoogle Scholar
- Tehler A, Irestedt M: Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales, Ascomycota). Cladistics. 2007, 23: 432-454. 10.1111/j.1096-0031.2007.00156.x.View ArticleGoogle Scholar
- Adams DC: Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evolutionary Biology. 2010, 10: 72-10.1186/1471-2148-10-72.PubMedPubMed CentralView ArticleGoogle Scholar
- Gosliner TM, Ghiselin MT: Parallel evolution in opisthobranch gastropods and its implications for phylogenetic methodology. Systematic Zoology. 1984, 33: 255-274. 10.2307/2413073.View ArticleGoogle Scholar
- Kyle CJ, Boulding EG: Molecular genetic evidence for parallel evolution in a marine gastropod, Littorina subrotundata. Proceedings of the Royal Society Biological Sciences. 1998, 265: 303-308. 10.1098/rspb.1998.0296.PubMedPubMed CentralView ArticleGoogle Scholar
- Jackson DJ, McDougall C, Woodcroft B, Moase P, Rose RA, Kube M, Reinhardt R, Rokhsar DS, Montagnani C, Joubert C, Piquemal D, Degnan BM: Parallel evolution of nacre building gene sets in molluscs. Molecular Biology and Evolution. 2009, 27: 591-608.PubMedView ArticleGoogle Scholar
- Cimino G, Ghiselin MT: Chemical defense and evolution in the Sacoglossa (Mollusca: Gastropoda: Opisthobranchia). Chemoecology. 1998, 8: 51-60. 10.1007/PL00001804.View ArticleGoogle Scholar
- Ponder WF, Lindberg DR: Phylogeny and evolution of the Mollusca. 2008, Berkeley, University of California PressView ArticleGoogle Scholar
- van Moorsel CHM, Dijkstra EGM, Gittenberger E: Molecular evidence for repetitive parallel evolution of shell structure in Clausiliidae (Gastropoda, Pulmonata). Molecular Phylogenetics and Evolution. 2000, 17: 200-208. 10.1006/mpev.2000.0826.PubMedView ArticleGoogle Scholar
- Simpson GG: The major features of evolution. 1953, New York, Columbia University PressGoogle Scholar
- Endler JA: Natural selection in the wild. 1986, Princeton, Princeton University PressGoogle Scholar
- Schluter D: The ecology of adaptive radiations. 2000, Oxford, Oxford University PressGoogle Scholar
- Zuckerkandl E: Molecular pathways to parallel evolution: I. Gene nexuses and their morphological correlates. J Molecular Evolution. 1994, 39: 661-678. 10.1007/BF00160412.View ArticleGoogle Scholar
- Dreyer H, Steiner G, Harper EM: Molecular phylogeny of Anomalodesmata (Mollusca: Bivalvia) inferred from 18S rRNA sequences. Zoological Journal of the Linnean Society. 2003, 139: 229-246. 10.1046/j.1096-3642.2003.00065.x.View ArticleGoogle Scholar
- Haas O, Simpson GG: Analysis of some phylogenetic terms, with attempts at redefinition. Proceedings of the American Philosophical Society. 1946, 90: 319-349.PubMedGoogle Scholar
- Donoghue MJ: Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny. Paleobiology. 2005, 31: 77-93. 10.1666/0094-8373(2005)031[0077:KICASM]2.0.CO;2.View ArticleGoogle Scholar
- Schindewolf OH: Konvergenz bei Korallen und bei Ammoniten. Fortschr Geol Paläontol. 1940, 12: 387-491.Google Scholar
- Haas O: Recurrence of morphologic types and evolutionary cycles in Mesozoic ammonites. J Paleontol. 1942, 16: 643-650.Google Scholar
- Kennedy WJ: Ammonoid evolution. Patterns of evolution as illustrated by the fossil record. Edited by: Hallam A. 1977, Amsterdam, Elsevier, 251-302.View ArticleGoogle Scholar
- Kennedy WJ: Thoughts on the evolution and extinction of Cretaceous ammonites. Proc Geol Ass. 1989, 100: 251-279. 10.1016/S0016-7878(89)80047-1.View ArticleGoogle Scholar
- Bayer U, McGhee GR: Iterative evolution of Middle Jurassic ammonite faunas. Lethaia. 1984, 17: 1-6. 10.1111/j.1502-3931.1984.tb00661.x.View ArticleGoogle Scholar
- Dommergues JL: Ammonoids. Evolutionary trends. Edited by: McNamara K. London. 1990, 162-187. Belhaven PressGoogle Scholar
- Guex J: Origine des sauts évolutifs chez les ammonites. Bull Soc Vaud Sci Nat. 1992, 82: 117-144.Google Scholar
- Guex J: Environmental stress and atavism in ammonoid evolution. Eclogae Geologicae Helveticae. 2001, 94: 321-328.Google Scholar
- Guex J: Reinitialization of evolutionary clocks during sublethal environmental stress in some invertebrates. Earth Planetary Science Letters. 2006, 243: 240-253.View ArticleGoogle Scholar
- Saunders WB, Work DM, Nikolaeva SV: Evolution of complexity in Paleozoic ammonoid sutures. Science. 1999, 286: 760-763. 10.1126/science.286.5440.760.PubMedView ArticleGoogle Scholar
- Kiselev DN: Parallel evolution of the Arctic and central-Russian Paracadoceras (Cadoceratinae, Ammonoidea). Contributions to current Cephalopod research: morphology, systematics, evolution, ecology and biostratigraphy. Edited by: Leonova TB, Barskov IS, Mitta VV. 2009, Moscow, PIN RAS, 41-46. [in Russian with English summary].Google Scholar
- Monnet C, Bucher H, Wasmer M, Guex J: Revision of the genus Acrochordiceras Hyatt, 1877 (Ammonoidea, Middle Triassic): morphology, biometry, biostratigraphy and intraspecific variability. Palaeontology. 2010, 53: 961-996. 10.1111/j.1475-4983.2010.00956.x.View ArticleGoogle Scholar
- Monnet C, Bucher H, Guex J, Wasmer M: Large-scale evolutionary trends of Acrochordiceratidae Arthaber, 1911 (Ammonoidea, Middle Triassic) and Cope's rule. Palaeontology.
- Schindewolf OH: Vergleichende Morphologie und Phylogenie der Anfangskammern tetrabranchiater Cephalopoden. Eine Studie über Herkunft, Stammesentwicklung und System der niederen Ammoneen. Abhandlungen der Preußischen Geologischen Landesanstalt Neue Folge. 1933, 148: 1-115.Google Scholar
- Schindewolf OH: Grundfragen der Paläontologie. Geologische Zeitmessung. Organische Stammesentwicklung. Biologische Systematik. 1950, Stuttgart, SchweizerbartGoogle Scholar
- Landman NH: Heterochrony in ammonites. Heterochrony in evolution. Edited by: McKinney NL. 1988, New York, Plenum Press, 159-182.View ArticleGoogle Scholar
- Korn D: Impact of environmental perturbations on heterochronic development in Palaeozoic ammonoids. Evolutionary change and heterochrony. Edited by: McNamara KJ. 1995, Chichester, Wiley & Sons, 245-260.Google Scholar
- Korn D: Typostrophism in Palaeozoic ammonoids. Paläont Zeit. 2003, 77: 445-470. [http://www.springerlink.com/content/c536721013x67551/]View ArticleGoogle Scholar
- House MR: Juvenile goniatite survival strategies following Devonian extinction events. Biotic recovery from mass extinction events. Edited by: Hart MB. 1996, Geological Society Spec. Pub, 102: 163-185.Google Scholar
- Guex J: A generalization of Cope's rule. Bull Soc géol France. 2003, 174: 449-452. 10.2113/174.5.449.View ArticleGoogle Scholar
- Korn D, Klug C: Morphological pathways in the evolution of Early and Middle Devonian ammonoids. Paleobiology. 2003, 29: 329-348. 10.1666/0094-8373(2003)029<0329:MPITEO>2.0.CO;2.View ArticleGoogle Scholar
- Gerber S, Eble GJ, Neige P: Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity. Evolution. 2008, 62: 1450-1457. 10.1111/j.1558-5646.2008.00370.x.PubMedView ArticleGoogle Scholar
- Brayard A, Escarguel G, Bucher H, Monnet C, Brühwiler T, Goudemand N, Galfetti T, Guex J: Good Genes and Good Luck: Ammonoid Diversity and the End-Permian Mass Extinction. Science. 2009, 325: 1118-1121. 10.1126/science.1174638.PubMedView ArticleGoogle Scholar
- De Baets K, Klug C, Korn D: Devonian pearls and ammonoid-endoparasite co-evolution. Acta Palaeontologica Polonica. 2011, 56: 159-180. 10.4202/app.2010.0044.View ArticleGoogle Scholar
- Seilacher A: Why are nautiloid and ammonoid sutures so different?. N Jb Geol Paläont Abh. 1988, 177: 41-69.Google Scholar
- Stanley SM: Macroevolution: pattern and process. 1979, San Francisco, W.H. FreemanGoogle Scholar
- Sepkoski JJ: Rates of speciation in the fossil record. Phil Trans R Soc London B. 1998, 353: 315-326. 10.1098/rstb.1998.0212.View ArticleGoogle Scholar
- Foote M, Sepkoski JJ: Absolute measures of the completeness of the fossil record. Nature. 1999, 398: 415-417. 10.1038/18872.PubMedView ArticleGoogle Scholar
- Bayer U, McGhee GR: Evolution in marginal epicontinental basins: the role of phylogenetic and ecological factors. Sedimentary and evolutionary cycles. Edited by: Bayer U, Seilacher A. 1985, Lecture Notes in Earth Sciences, 1: 164-220.View ArticleGoogle Scholar
- Dommergues JL, Cariou E, Contini D, Hantzpergue P, Marchand D, Meister C, Thierry J: Homéomorphies et canalisations évolutives: le rôle de l'ontogenèse. Quelques exemples pris chez les ammonites du Jurassique. Géobios. 1989, 22: 5-48. 10.1016/S0016-6995(89)80087-7.View ArticleGoogle Scholar
- Jacobs DK, Landman NH, Chamberlain JA: Ammonite shell shape covaries with facies and hydrodynamics: iterative evolution as a response to changes in basinal environment. Geology. 1994, 22: 905-908. 10.1130/0091-7613(1994)022<0905:ASSCWF>2.3.CO;2.View ArticleGoogle Scholar
- Klug C, Korn D: The origin of ammonoid locomotion. Acta Palaeontologica Polonica. 2004, 49: 235-242.Google Scholar
- Westermann GEG: Covariation and taxonomy of the Jurassic ammonite Sonninia adicra (Waagen). N Jb Geol Pal Abh. 1966, 124: 289-312.Google Scholar
- Trueman AE: The meaning of orthogenesis. Transactions of the Geological Society of Glasgow. 1940, 20: 77-95.View ArticleGoogle Scholar
- Elmi S: Données expérimentales sur l'architecture fonctionelle de la coquille des ammonoïdes Jurassiques. Géobios, Mémoire Spécial. 1991, 13: 155-160. 10.1016/S0016-6995(66)80020-7.View ArticleGoogle Scholar
- Jacobs DK: Shape, drag, and power in ammonoid swimming. Paleobiology. 1992, 18: 203-220.View ArticleGoogle Scholar
- Jacobs DK, Chamberlain JA: Buoyancy and hydrodynamics in ammonoids. Ammonoid paleobiology. Edited by: Landman NH, Tanabe K, Davis RA. 1996, New York, Plenum Press, Topics in Geobiology, 13: 169-223.View ArticleGoogle Scholar
- Kaufmann B, Trapp E, Mezger K, Weddige K: Two new Emsian (Early Devonian) U-Pb zircon ages from volcanic rocks of the Rhenish Massif (Germany): implications for the Devonian time scale. Journal of the Geological Society, London. 2005, 162: 363-371. 10.1144/0016-764904-012.View ArticleGoogle Scholar
- Nishiguchi MK, Mapes RH: Cephalopoda. Phylogeny and evolution of the Mollusca. Edited by: Ponder WF, Lindberg DR. 2008, Berkeley, University of California Press, 163-199.Google Scholar
- Erben HK: Primitive Ammonoidea aus dem Unterdevon Frankreichs und Deutschlands. N Jb Geol Pal Abh. 1960, 110: 1-128.Google Scholar
- Erben HK: Die Evolution der ältesten Ammonoidea (Lieferung I). N Jb Geol Pal Abh. 1964, 120: 107-212.Google Scholar
- Erben HK: Über den Ürsprung der Ammonoidea. Biological Reviews. 1966, 41: 641-658. 10.1111/j.1469-185X.1966.tb01626.x.PubMedView ArticleGoogle Scholar
- Kröger B, Mapes RH: On the origin of bactritoids (Cephalopoda). Paläont Zeit. 2007, 81: 316-327. [http://www.springerlink.com/content/m2010544527231rv/]View ArticleGoogle Scholar
- De Baets K, Klug C, Korn D: New Anetoceratinae (Ammonoidea, Early Devonian) from Germany with a revision of their genera. N Jb Geol Pal Abh. 2009, 252: 361-376. 10.1127/0077-7749/2009/0252-0361.View ArticleGoogle Scholar
- Barrande J: Systême Silurien du centre de la Bohême. I. Vol.II. Céphalopodes. 1865, Paris, PrahaGoogle Scholar
- Ruan Y: Devonian and earliest Carboniferous Ammonoids from Guangxi and Guizhou. Memoires of Nanjing Institute of Geology and Paleontology, Academia Sinica. 1981, 15: 1-152.Google Scholar
- Bogoslovskji BI: Eyfelskie ammonoidei Urale i voprosy klassifikatsii agoniatitov. Paleontologicheskiy Zhurnal. 1961, 60-70.Google Scholar
- Bogoslovskji BI: Rannedevonskiye ammonoidei zeravchanskogo Khreta. Paleontologicheskiy Zhurnal. 1980, 51-66.Google Scholar
- Bogoslovskji BI: Novyy rod semeystva Auguritidae i soputstvuyushchie emu ammonoidei iz nizhnego Devona zeravshanskogo Khreta. Paleontologicheskiy Zhurnal. 1984, 30-36.Google Scholar
- Chlupáč I, Turek V: Devonian goniatites from the Barrandian area, Czechoslovakia. Rozpravy Ustředního ústavu geologického. 1983, 46: 1-159.Google Scholar
- Klug C: Early Emsian ammonoids from the eastern Anti-Atlas (Morocco). Paläont Zeit. 2001, 74: 479-515. [http://www.springerlink.com/content/2h2w51h10871814l/]View ArticleGoogle Scholar
- De Baets K, Klug C, Plusquellec Y: Zlíchovian faunas with early ammonoids from Morocco and their use for the correlation of the eastern Anti-Atlas and the western Dra Valley. Bulletin of Geosciences. 2010, 85: 317-352.View ArticleGoogle Scholar
- Klug C, Kröger B, Kiessling W, Mullins GL, Servais T, Frýda J, Korn D, Turner S: The Devonian nekton revolution. Lethaia. 2010, 43: 465-477. 10.1111/j.1502-3931.2009.00206.x.View ArticleGoogle Scholar
- Nützel A, Frýda J: Paleozoic plankton revolution: evidence from early gastropod ontogeny. Geology. 2003, 31: 829-831. 10.1130/G19616.1.View ArticleGoogle Scholar
- Alberti GKB: Dacryoconaride und homoctenide Tentaculiten des Unter- und Miteldevons. Courier Forschungsinstitut Senckenberg. 1993, 158: 1-229.Google Scholar
- Koren TN, Kim AI, Walliser OH: Contribution to the biostratigraphy around the Lochkovian-Pragian boundary in Central Asia (graptolites, tentaculites, conodonts). Palaeobiodiversity Palaeoenvironments. 2007, 87: 187-219.Google Scholar
- Dzik J: Phylogeny of the Nautiloidea. Palaeontologia Polonica. 1984, 45: 1-219.Google Scholar
- Kröger B: Adaptive evolution in Paleozoic coiled Cephalopods. Paleobiology. 2005, 31: 253-268. 10.1666/0094-8373(2005)031[0253:AEIPCC]2.0.CO;2.View ArticleGoogle Scholar
- Klug C, Meyer EP, Richter U, Korn D: Soft-tissue imprints in fossil and Recent cephalopod septa and septum formation. Lethaia. 2008, 41: 477-492. 10.1111/j.1502-3931.2008.00100.x.View ArticleGoogle Scholar
- Kaufmann B: Calibrating the Devonian Time Scale: a synthesis of U-Pb ID-TIMS ages and conodont stratigraphy. Earth Science Reviews. 2006, 76: 175-190. 10.1016/j.earscirev.2006.01.001.View ArticleGoogle Scholar
- Becker RT, House MR: International Devonian goniatite zonation, Emsian to Givetian, with new records from Morocco. Courier Forschungsinstitut Senckenberg. 1994, 169: 79-135.Google Scholar
- Klug C: Quantitative stratigraphy and taxonomy of late Emsian and Eifelian ammonoids of the eastern Anti-Atlas (Morocco). Courier Forschungsinstitut Senckenberg. 2002, 238: 1-109.Google Scholar
- Korn D: Morphometric evolution and phylogeny of Palaeozoic ammonoids. Early and Middle Devonian. Acta Geologica Polonica. 2001, 51: 193-215.Google Scholar
- Becker RT, De Baets K, Nikolaeva S: New ammonoid records from the lower Emsian of the Kitab Reserve (Uzbekistan) - Preliminary Results. SDS Newsletter. 2010, 25: 20-28.Google Scholar
- Monnet C, Klug C, Goudemand N, Bucher H, De Baets K: Quantitative biochronology of Devonian ammonoids from Morocco and refinement of the unitary association method. Lethaia.
- Klug C, Korn D: Occluded umbilicus in the Pinacitinae (Devonian) and its palaeoecological implications. Palaeontology. 2002, 45: 917-931. 10.1111/1475-4983.00268.View ArticleGoogle Scholar
- Bogoslovskji BI: Devonskie ammonoidei. I. Agoniatity. Trudy Paleontologicheskogo Instituta Akademiya Nauk SSSR. 1969, 124: 1-341.Google Scholar
- Cecca F: Late Jurassic and Early Cretaceous uncoiled ammonites: trophism-related evolutionary processes. C R Acad Sci, Series IIA - Earth and Planetary Science. 1997, 325: 629-634.Google Scholar
- Korn D, Klug C: Ammoneae Devonicae. Fossilium Catalogus 1: Animalia. Edited by: Riegraf W. 2002, Leiden, Backhuys, 138: 1-375.Google Scholar
- Korn D: A key for the description of Palaeozoic ammonoids. Fossil Record. 2010, 13: 5-12. 10.1002/mmng.200900008.View ArticleGoogle Scholar
- Raup DM: Geometric analysis of shell coiling: general problems. J Paleont. 1966, 40: 1178-1190.Google Scholar
- Raup DM: Geometrical analysis of shell coiling: coiling in ammonoids. J Paleont. 1967, 41: 43-65.Google Scholar
- Saunders WB, Shapiro EA: Calculation and simulation of ammonoid hydrostatics. Paleobiology. 1986, 12: 64-79.View ArticleGoogle Scholar
- Korn D, Klug C: Conch form analysis, variability, and morphological disparity of a Frasnian (Late Devonian) ammonoid assemblage from Coumiac (Montagne Noire, France). Cephalopods - Present and Past. Edited by: Landman NH, Davis RA, Manger W, Mapes RH. 2007, New York, Springer, 57-86.Google Scholar
- Ruzhencev VE: Filogeneticheskaya sistema paleozoyskikh ammonoidey. Byulleten' Moskovskogo obshchestva ispytately prirody, novaya seriya, otdel geologicheskiy. 1957, 31: 49-64.Google Scholar
- Wake DB: Homoplasy: the result of natural selection or evidence of design constraints?. American Naturalist. 1991, 138: 543-567. 10.1086/285234.View ArticleGoogle Scholar
- Stayton CT: Testing hypotheses of convergence with multivariate data: morphological and functional convergence among herbivorous lizards. Evolution. 2006, 60: 824-841.PubMedView ArticleGoogle Scholar
- Jackson JE: A user's guide to principal components. New York, John Wiley, 10.1002/0471725331.
- Hammer Ø, Harper DAT, Ryan PD: PAST, Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica. 2001, 4: 1D-Google Scholar
- Hammer Ø, Harper DAT: Paleontological data analysis. 2005, Oxford, Blackwell PublishingView ArticleGoogle Scholar
- Raup DM, Crick RE: Evolution of single characters in the Jurassic ammonite Kosmoceras. Paleobiology. 1981, 7: 200-215.View ArticleGoogle Scholar
- Bookstein FL: Random walk and the existence of evolutionary rates. Paleobiology. 1987, 13: 446-464.View ArticleGoogle Scholar
- Bookstein FL: Random walk and the biometrics of morphological characters. Evolutionary Biology. 1988, 9: 369-398.Google Scholar
- Raup DM: Stochastic models in evolutionary paleobiology. Patterns of evolution as illustrated by the fossil record. Edited by: Hallam A. 1997, Amsterdam, Elsevier, 59-78.Google Scholar
- Raup DM, Gould SJ: Stochastic simulation and evolution of morphology - towards a nomothetic paleontology. Systematic Zoology. 1974, 23: 305-322. 10.2307/2412538.View ArticleGoogle Scholar
- Roopnarine PD, Byars G, Fitzgerald P: Anagenetic evolution, stratophenetic patterns, and random walk models. Paleobiology. 1999, 25: 41-57.Google Scholar
- Sheets HD, Mitchell CE: Why the null matters: statistical tests, random walks and evolution. Genetica. 2001, 112-113: 105-125.PubMedView ArticleGoogle Scholar
- Gingerich PD: Quantification and comparison of evolutionary rates. American Journal of Science. 1993, 293A: 453-478.View ArticleGoogle Scholar
- Roopnarine PD: The description and classification of evolutionary mode: a computational approach. Paleobiology. 2001, 27: 446-465. 10.1666/0094-8373(2001)027<0446:TDACOE>2.0.CO;2.View ArticleGoogle Scholar
- Hunt G: Fitting and comparing models of phyletic evolution: random walks and beyond. Paleobiology. 2006, 32: 578-601. 10.1666/05070.1.View ArticleGoogle Scholar
- Hunt G: Phenotypic variation in fossil samples: modeling the consequences of time-averaging. Paleobiology. 2004, 30: 426-443. 10.1666/0094-8373(2004)030<0426:PVIFSM>2.0.CO;2.View ArticleGoogle Scholar
- Hunt G, Bell MA, Travis MP: Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution. 2008, 62: 700-710. 10.1111/j.1558-5646.2007.00310.x.PubMedView ArticleGoogle Scholar
- Hunt G: The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proc Natl Acad Sci USA. 2007, 104: 18404-18408. 10.1073/pnas.0704088104.PubMedPubMed CentralView ArticleGoogle Scholar
- Anderson DR, Burnham KP, Thompson WL: Null hypothesis testing: problems, prevalence, and an alternative. Journal of Wildlife Management. 2000, 64: 912-923. 10.2307/3803199.View ArticleGoogle Scholar
- Mitteroecker P, Gunz P, Bookstein FL: Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evolution & Development. 2005, 7: 244-258. 10.1111/j.1525-142X.2005.05027.x.View ArticleGoogle Scholar
- Webster M, Zelditch ML: Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology. 2005, 31: 354-372. 10.1666/0094-8373(2005)031[0354:EMOOHA]2.0.CO;2.View ArticleGoogle Scholar
- Adams DC, Collyer ML: A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution. 2009, 63: 1143-1154. 10.1111/j.1558-5646.2009.00649.x.PubMedView ArticleGoogle Scholar
- Collyer ML, Adams DC: Analysis of two-state multivariate phenotypic change in ecological studies. Ecology. 2007, 88: 683-692. 10.1890/06-0727.PubMedView ArticleGoogle Scholar
- Klug C: Life-cycles of some Devonian ammonoids. Lethaia. 2001, 34: 215-233. 10.1111/j.1502-3931.2001.tb00051.x.View ArticleGoogle Scholar
- Newell ND: Phyletic size increase, an important trend illustrated by fossil invertebrates. Evolution. 1949, 3: 103-124. 10.2307/2405545.PubMedView ArticleGoogle Scholar
- Rensch B: Evolution above the species level. 1959, New York, Columbia University PressGoogle Scholar
- Gould SJ: Allometry and size in ontogeny and phylogeny. Biological Reviews. 1966, 41: 587-640. 10.1111/j.1469-185X.1966.tb01624.x.PubMedView ArticleGoogle Scholar
- Stanley SM: An explanation for Cope's rule. Evolution. 1973, 27: 1-26. 10.2307/2407115.View ArticleGoogle Scholar
- Kurten B: On the variation and population dynamics of fossil and Recent mammal populations. Acta Zool Fennica. 1953, 76: 1-122.Google Scholar
- Brown JH, Maurer BA: Body size, ecological dominance and Cope's rule. Nature. 1986, 324: 248-250. 10.1038/324248a0.View ArticleGoogle Scholar
- Hone DWE, Benton MJ: The evolution of large size: how does Cope's Rule work?. Trends in Ecology & Evolution. 2005, 20: 4-6. 10.1016/j.tree.2004.10.012.View ArticleGoogle Scholar
- Hallam A: Evolutionary size increase and longevity in Jurassic bivalves and ammonites. Nature. 1975, 258: 493-496. 10.1038/258493a0.View ArticleGoogle Scholar
- Thierry J: Rythme d'évolution des caractères morphologiques chez les Macrocephalitidae (Cephalopoda, Ammonitina, Jurassique moyen). Modalités, rythmes, mécanismes de l'évolution biologique. Edited by: Chaline J. 1982, Paris, Editions du CNRS, Colloques Internationaux du Centre National de la Recherche Scientifique, 330: 211-218.Google Scholar
- Dommergues JL, Montuire S, Neige P: Size patterns through time: the case of the Early Jurassic ammonite radiation. Paleobiology. 2002, 28: 423-434. 10.1666/0094-8373(2002)028<0423:SPTTTC>2.0.CO;2.View ArticleGoogle Scholar
- Hyatt A: Genesis of the Arietitidae. Smithsonian Contributions to Knowledge. 1889, 673: 1-238.Google Scholar
- Guex J: Observations sur la répartition biostratigraphique des ammonites du Toarcien supérieur de l'Aveyron (France). Bull Lab Géol Minéral Géophys Univ Lausanne. 1973, 207: 1-14.Google Scholar
- Guex J: Associations virtuelles et discontinuités dans la distribution des espèces fossiles: un exemple intéressant. Bull Soc Vaud Sci Nat. 1981, 359: 179-197.Google Scholar
- Donovan DT: Ammonite shell form and transgression in the British Lower Jurassic. Sedimentary and evolutionary cycles. Edited by: Bayer U, Seilacher A. 1985, Lecture Notes in Earth Sciences, 1: 164-220.View ArticleGoogle Scholar
- Saunders WB, Work DM, Nikolaeva SV: The evolutionary history of shell geometry in Paleozoic ammonoids. Paleobiology. 2004, 30: 19-43. 10.1666/0094-8373(2004)030<0019:TEHOSG>2.0.CO;2.View ArticleGoogle Scholar
- Saunders WB, Greenfest-Allen E, Work DM, Nikolaeva SV: Morphologic and taxonomic history of Paleozoic ammonoids in time and morphospace. Paleobiology. 2008, 34: 128-154. 10.1666/07053.1.View ArticleGoogle Scholar
- Elmi S: Loi des aires, couche-limite et morphologie fonctionnelle de la coquille des cephalopods (ammonoïdes). Géobios, Mémoire Spécial. 1993, 15: 121-138. 10.1016/S0016-6995(06)80367-0.View ArticleGoogle Scholar
- Seki K, Tanabe K, Landman NH, Jacobs DK: Hydrodynamic analysis of Late Cretaceous desmoceratine ammonites. Revue Paléobiologie, Volume spécial. 2000, 8: 141-155.Google Scholar
- De Blasio FV: The role of suture complexity in diminishing strain and stress in ammonoid phragmocones. Lethaia. 2008, 41: 15-24. 10.1111/j.1502-3931.2007.00037.x.View ArticleGoogle Scholar
- Ward PD: In search of Nautilus. 1988, New York, Simon and SchusterGoogle Scholar
- Jacobs DK, Landman NH: Nautilus, a poor model for the function and behavior of ammonoids?. Lethaia. 1993, 26: 101-111. 10.1111/j.1502-3931.1993.tb01799.x.View ArticleGoogle Scholar
- Klug C, Meyer E, Richter U, Korn D: Soft-tissue imprints in fossil and Recent cephalopod septa and septum formation. Lethaia. 2008, 41: 477-492. 10.1111/j.1502-3931.2008.00100.x.View ArticleGoogle Scholar
- Batt RJ: Ammonite shell morphotype distributions in the Western Interior Greenhorn Sea and some paleoecological implications. Palaios. 1989, 4: 32-42. 10.2307/3514731.View ArticleGoogle Scholar
- Westermann GEG: Ammonoid life and habitat. Ammonoid paleobiology. Edited by: Landman NH, Tanabe K, Davis RA. 1996, New York, Plenum Press, Topics in Geobiology, 13: 607-707.View ArticleGoogle Scholar
- Westermann GEG, Tsujita CJ: Life habits of ammonoids. Functional morphology of the invertebrate skeleton. Edited by: Savazzi E. 1999, Chichester, John Wiley and Sons, 299-325.Google Scholar
- Neige P, Marchand D, Bonnot A: Ammonoid morphological signal versus sea-level changes. Geol Mag. 1997, 134: 261-264. 10.1017/S0016756897006687.View ArticleGoogle Scholar
- Olóriz F, Palmqvist P, Pérez-Claros A: Shell features, main colonized environments, and fractal analysis of sutures in Late Jurassic ammonites. Lethaia. 1997, 30: 191-204.View ArticleGoogle Scholar
- Olóriz F, Palmqvist P, Pérez-Claros A: Recent advances in morphometric approaches to covariation of shell features and the complexity of suture lines in Late Jurassic ammonites, with reference to the major environments colonized. Advancing research on living and fossil cephalopods. Edited by: Olóriz F, Rodríguez-Tovar FJ. 1999, New York, Kluwer/Plenum, 273-293.View ArticleGoogle Scholar
- Olóriz F, Palmqvist P, Pérez-Claros A: Morphostructural constraints and phylogenetic overprint on sutural frilling in Late Jurassic ammonites. Lethaia. 2002, 35: 158-168. 10.1111/j.1502-3931.2002.tb00076.x.View ArticleGoogle Scholar
- Kawabe F: Relationship between mid-Cretaceous (upper Albian-Cenomanian) ammonoid facies and lithofacies in the Yezo forearc basin, Hokkaido, Japan. Cretaceous Research. 2003, 24: 751-763. 10.1016/j.cretres.2003.08.001.View ArticleGoogle Scholar
- Tozer ET: Observations on the shell structure of Triassic ammonoids. Palaeontology. 1972, 15: 637-654.Google Scholar
- Packard A, Bone Q, Hignette M: Breathing and swimming movements in a captive Nautilus. J Marine Biol Assoc United Kingdom. 1980, 60: 313-327. 10.1017/S0025315400028368.View ArticleGoogle Scholar
- Engeser T: The Position of the Ammonoidea within the Cephalopoda. Ammonoid paleobiology. Edited by: Landman NH, Tanabe K, Davis RA. 1996, New York, Plenum Press, Topics in Geobiology, 13: 3-19.View ArticleGoogle Scholar
- Prud'homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh SD, True JR, Caroll SB: Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature. 2006, 440: 1050-1053. 10.1038/nature04597.PubMedView ArticleGoogle Scholar
- Lindsey CC: Experimental study of meristic variation in a population of threespine sticklebacks, Gasterosteus aculeatus. Can J Zool. 1962, 40: 271-312. 10.1139/z62-028.View ArticleGoogle Scholar
- Minelli A: Perspectives in animal phylogeny and evolution. 2009, Oxford, Oxford University PressGoogle Scholar
- Seilacher A: Fabricational noise in adaptive morphology. Systematic Zoology. 1973, 222: 451-465.View ArticleGoogle Scholar
- Hammer Ø, Bucher H: Buckman's first law of covariation - a case of proportionality. Lethaia. 2005, 38: 67-72. [http://onlinelibrary.wiley.com/doi/10.1080/00241160510013196/abstract]View ArticleGoogle Scholar
- Urdy S, Goudemand N, Bucher H, Chirat R: Allometries and the morphogenesis of the molluscan shell: a quantitative and theoretical model. J Exp Zool (Mol Dev Evol). 2010, 314B: 280-302. 10.1002/jez.b.21337.View ArticleGoogle Scholar
- Urdy S, Goudemand N, Bucher H, Chirat R: Growth-dependent phenotypic variation of molluscan shells: implications for allometric data interpretation. J Exp Zool (Mol Dev Evol). 2010, 314B: 303-326. 10.1002/jez.b.21338.View ArticleGoogle Scholar
- Buckman SS: A monograph of the ammonites of the Inferior Oolite Series. 1892, London, Palaeontographical SocietyGoogle Scholar
- Guex J, Koch A, O'Dogherty L, Bucher H: A morphogenetic explanation of Buckman's law of covariation. Bull Soc géol France. 2003, 174: 603-606. 10.2113/174.6.603.View ArticleGoogle Scholar
- Yacobucci MM: Buckman's paradox: variability and constraints on ammonoid ornament and shell shape. Lethaia. 2004, 37: 57-69. [http://onlinelibrary.wiley.com/doi/10.1080/00241160410004755/abstract]View ArticleGoogle Scholar
- Reeside JB, Cobban WA: Studies of the Mowry Shale (Cretaceous) and contemporary formations in the United States and Canada. US Prof Pap Geol Surv. 1960, 355: 1-126.Google Scholar
- Kennedy WJ, Cobban WA: Aspects of ammonite biology, biogeography, and biostratigraphy. Spec Pap Palaeontol. 1976, 17: 1-94.Google Scholar
- Silberling NJ, Nichols KM: Middle Triassic molluscan fossils of biostratigraphic significance from the Humboldt Range, north-western Nevada. US Prof Pap Geol Surv. 1982, 1207: 1-77.Google Scholar
- Dagys A, Weitschat W: Intraspecific variation in Boreal Triassic ammonoids. Géobios. 1993, 26: 107-109. 10.1016/S0016-6995(06)80365-7.View ArticleGoogle Scholar
- Kaplan P: Buckman's rule of covariation and other trends in Paleozoic Ammonoidea; morphological integration as key innovation. Geological Society of America, Abstracts with Programs. 1999, 31: 172-Google Scholar
- Morard A, Guex J: Ontogeny and covariation in the Toarcian genus Osperleioceras (Ammonoidea). Bull Soc géol France. 2003, 174: 607-615. 10.2113/174.6.607.View ArticleGoogle Scholar
- Checa AG, Garcia-Ruiz JM: Morphogenesis of the septum in ammonoids. Ammonoid paleobiology. Edited by: Landman NH, Tanabe K, Davies RA. 1996, New York, Plenum Press, 253-296.View ArticleGoogle Scholar
- Kullmann J, Wiedmann J: Significance of sutures in phylogeny of Ammonoidea. University of Kansas Paleontological Contributions Paper. 1970, 47: 1-32.Google Scholar
- Donovan DT: Evolution of the Arietitidae and their descendants. Deuxième colloque du Centre International d'Etude du Lias (C.I.E.L.), Lyon 27-30 Mai 1996. Edited by: Almeras Y, Rouget C. 1987, Lyon, Les Cahiers de l'Institut Catholique de Lyon, Série Sciences, 123-138.Google Scholar
- Donovan DT: Evolution in some early Jurassic ammonites: Asteroceratinae, Oxnoticeratidae and related forms. Proceedings of the Third Pergola International Symposium ''Fossili, Evolution, Ambiente'' October 1990. Edited by: Pallini G. 1994, Palaeopelagos Special Publication, 1: 383-396.Google Scholar
- Korn D: A modified Balloon model for septa of early ammonoids. Lethaia. 1997, 30: 39-40.View ArticleGoogle Scholar
- Landman NH, Cobban WA: Ammonites from the Upper Part of the Pierre Shale and Fox Hills Formation of Colorado. American Museum Novitates. 2003, 3388: 1-45.View ArticleGoogle Scholar
- Dommergues JL, Dommergues CH, Meister C: Exploration of the Oxynoticeratidae ornamental morphospace using the discrete cosine transform (DCT) to analyze rib patterns. Paleobiology. 2006, 32: 628-651. 10.1666/05046.1.View ArticleGoogle Scholar
- Pérez-Claros JA, Olóriz F, Palmqvist P: Sutural complexity in Late Jurassic ammonites and its relationship with phragmocone size and shape: a multidimensional approach using fractal analysis. Lethaia. 2007, 40: 253-272. 10.1111/j.1502-3931.2007.00022.x.View ArticleGoogle Scholar
- Bockwinkel J, Becker RT, Ebbighausen V: Upper Givetian ammonoids from Dar Kaoua (Tafilalt, SE Anti-Atlas, Morocco). Berliner Paläobiologische Abhandlungen. 2009, 10: 61-128.Google Scholar
- Brühwiler T, Bucher H, Goudemand N: Smithian (Early Triassic) ammonoids from Tulong, South Tibet. Géobios. 2010, 43: 403-431. 10.1016/j.geobios.2009.12.004.View ArticleGoogle Scholar
- Saunders WB: The ammonoid suture problem: relationships between shell and septum thickness and suture complexity in Paleozoic ammonoids. Paleobiology. 1995, 21: 343-355.View ArticleGoogle Scholar
- Checa AG: Fabrication and function of ammonite septa, comment on Lewy. J Paleont. 2003, 77: 790-791. 10.1666/0022-3360(2003)077<0790:FAFOAS>2.0.CO;2.View ArticleGoogle Scholar
- Hewitt RA, Westermann GEG: Function of complexly fluted septa in ammonoid shell. II. Septal evolution and conclusion. N Jb Geol Paläontol Abh. 1986, 174: 135-169.Google Scholar
- Hewitt RA, Westermann GEG: Mechanical significance of ammonoid septa with complex sutures. Lethaia. 1997, 30: 205-212.View ArticleGoogle Scholar
- Henderson RA: A muscle attachment proposal for septal function in Mesozoic ammonites. Palaeontology. 1984, 27: 461-486.Google Scholar
- Daniel TL, Helmuth BS, Saunders WB, Ward PD: Septal complexity in ammonoid cephalopods increased mechanical risk and limited depth. Paleobiology. 1997, 23: 470-481.View ArticleGoogle Scholar
- Pérez-Claros JA: Allometric and fractal exponents indicate a connection between metabolism and complex septa in ammonites. Paleobiology. 2005, 31: 221-232. 10.1666/0094-8373(2005)031[0221:AAFEIA]2.0.CO;2.View ArticleGoogle Scholar
- Garcia-Ruiz JM, Checa A: A model for the morphogenesis of ammonoid septal sutures. Géobios, Mémoire Spécial. 1993, 15: 157-162. 10.1016/S0016-6995(06)80369-4.View ArticleGoogle Scholar
- Garcia-Ruiz JM, Checa A, Rivas P: On the origin of ammonite sutures. Paleobiology. 1990, 16: 349-354.View ArticleGoogle Scholar
- Hammer Ø: The development of ammonoid septa: an epithelial invagination process controlled by morphogens?. Historical Biology. 1999, 13: 153-171. 10.1080/08912969909386579.View ArticleGoogle Scholar
- Seilacher A, LaBarbera M: Ammonites as Cartesian divers. Palaios. 1995, 10: 493-506. 10.2307/3515089.View ArticleGoogle Scholar
- Seilacher A: Arbeitskonzept zur Konstruktions-Morphologie. Lethaia. 1970, 3: 393-396. 10.1111/j.1502-3931.1970.tb00830.x.View ArticleGoogle Scholar
- Hewitt RA: Architecture and strength of the ammonoid shell. Ammonoid paleobiology. Edited by: Landman NH, Tanabe K, Davis RA. 1996, New York, Plenum Press, Topics in Geobiology, 13: 297-339.View ArticleGoogle Scholar
- Saunders WB, Work DM: Shell morphology and suture complexity in Upper Carboniferous ammonoids. Paleobiology. 1996, 22: 189-218.View ArticleGoogle Scholar
- Allen EG: Understanding ammonoid sutures. New insights into the dynamic evolution of Paleozoic suture morphology. Cephalopods Present and Past: new insights and fresh perpsectives. Edited by: Landman NH, Davis RA, Mapes RH. 2007, Dordrecht, Springer, 159-180.View ArticleGoogle Scholar
- Willmer P: Convergence and homoplasy in the evolution of organismal form. Origination of organismal form. Edited by: Muller GB, Newman SA. 2003, Massachusetts, MIT Press, The Vienna series of theoretical biology, 33-50.Google Scholar
- Shigeno S, Sasaki T, Boletzky Sv: Origins of cephalopod body plans: A geometrical and developmental basis for the evolution of vertebrate-like organ systems. Cephalopods Present and Past. Edited by: Tanabe K, Shigeta Y, Sasaki T, Hirano H. 2010, Tokai University Press, 23-34.Google Scholar
- Lardeux H, Morzadec P, Bultynck P, Walliser OH: La Grange Limestone. Massif Armoricain, Field Excursion Guidebook. Edited by: Lardeux H, Morzadec P. 1979, International Subcommission on Devonian Stratigraphy, 5-7.Google Scholar
- Scotese CR: Digital Paleogeographic Map Archive on CD-ROM. 2001, Arlington, Texas, PALEOMAP ProjectGoogle Scholar
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