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Open Access Highly Accessed Research article

Parallel evolution controlled by adaptation and covariation in ammonoid cephalopods

Claude Monnet*, Kenneth De Baets and Christian Klug

Author Affiliations

Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid Strasse 4, 8006 Zürich, Switzerland

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BMC Evolutionary Biology 2011, 11:115  doi:10.1186/1471-2148-11-115


The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1471-2148/11/115


Received:13 September 2010
Accepted:29 April 2011
Published:29 April 2011

© 2011 Monnet et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

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.

Results

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.

Conclusions

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).

Background

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 [14].

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 [17]). 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; [25]) 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" [51]. 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 [59]; 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.

We here report on a probable, recently discovered case of parallel evolution among ammonoids. It happened very early in the history and rapid diversification of the Ammonoidea during the Early and Middle Devonian in the time interval between about 405 and 395 Ma [64]. The ammonoid shell, which grew by accretion, consists of a roughly conic, chambered, calcified, often ornamented and (more or less regularly) coiled conch. Yet, during this early diversification phase, the history of ammonoids is characterized by a morphological macroevolutionary trend from straight-shelled ancestors (bactritoids; for a review of cephalopod phylogeny, see [65]) via loosely coiled earliest ammonoids toward completely tightly coiled forms with closed umbilicus (Figure 1; [58,66-70]). This major evolutionary trend is thought to have occurred in a time interval of only about 2 My (see [58,69]). This rather fast evolution is evidenced by the co-occurrence of loosely coiled primitive forms, which are associated with contemporaneous, more derived, coiled forms in several localities that yielded the earliest ammonoids [71-78]. Furthermore, this morphological evolutionary trend occurred during the most intense phase of the "Devonian nekton revolution" [79]. This macroecological event corresponds to an explosive trend from planktonic and demersal marine animals toward true nekton as represented by the great diversification of jawed fish and ammonoids, reflecting a selection for swimming capabilities. It coincided with macroevolutionary transformations among various mollusc groups: an increasing proportion of gastropods formed tightly coiled protoconchs [80]; some dacryoconarids [81,82], ammonoids [58] and some nautiloids [83,84] more or less simultaneously evolved coiled shells, mainly during the Early Devonian. Among ammonoids, these post-embryonic morphological transformations enhanced buoyancy and swimming capabilities [58,85].

thumbnailFigure 1. Morphological evolution of externally-shelled cephalopods during the most intense phase of the "Devonian Nekton Revolution" in the Early and early Middle Devonian. Reconstructions of the loosely coiled ancestors of the two lineages under consideration and two representatives of each of the lineages leading to and comprising the Auguritidae and Pinacitidae. The reconstruction of the soft-body are largely speculative: 10 arms are based on the knowledge that both plesiomorphic coleoids have ten arms and the sister group of the Ammonoidea + Bactritoidea + Coleoidea, the Nautiloidea, is known to begin with ten arms buds in early embryonic development [201]. The orientation can be reconstructed from the shell morphology [58]. Presence of a hood and of a camera lucida-style eye as in Recent Nautilida is speculative [158]. The position of the eye and the hyponome are deduced from the position of the ocular sinus and hyponomic sinus, respectively. The reconstructions are not shown at the same scale.

The case of parallel evolution studied here includes two families of ammonoids, namely the Auguritidae and Pinacitidae (Figure 2A). These two ammonoid lineages are of Emsian and Eifelian age (~ 405-395 Ma; [86]) and have a widespread palaeogeographical distribution (Figure 2B). Their stratigraphy and taxonomy have been revised recently [77,87-91]. Representatives of the older lineage are very rare [77,78]. The study of recently discovered material [78] and reinvestigation of the most complete material available in museum collections yielded comprehensive morphometric data and revealed the presence of an umbilical lid (see below) in the auguritid lineage, previously only known in the pinacitid lineage [92]. Both lineages under consideration share a common ancestor (which probably resembled Convoluticeras lardeuxi, Figure 2A) and their end-members have a very similar morphology in post-embryonic ontogeny. Although closely related and in spite of their great morphological resemblance, there is clear evidence for these two families being distinct clades. For instance, the embryonic shell was openly coiled in the auguritids [75,76,93] and became tightly coiled in later ammonoid evolution, including the pinacitids [88]; this is a character that was never reversed throughout ammonoid evolution, not even in Mesozoic ammonoids with uncoiled post-embryonic shells [45,94]. Additionally, the youngest representatives of the auguritids are at least 5 My older than the youngest representatives of the pinacitids. The evolutionary relationships of the auguritids and pinacitids were elucidated with a comprehensive cladistic analysis [89] that considered all currently known valid taxa (except Achguigites tafilaltensis [88] and Weyeroceras angustus [77], which were introduced later; for their phylogenetic position, see [95]). The resultant strict consensus is well resolved (Figure 2A). Both lineages are characterized at the end of their evolution by the development of a very peculiar morphological feature not known in this specific form in any other ammonoids (including forms with similar conch shapes). This peculiarity is the development of an umbilical lid (Figure 3), which is an extension of the lateral shell wall covering the umbilicus [92].

thumbnailFigure 2. Spatial and temporal distribution of Auguritidae and Pinacitidae in the Devonian. A, Phylogeny and stratigraphic ranges of studied Devonian ammonoids. Stratigraphic ranges of taxa compiled from [74-77,88,91,93,202] and own unpublished data. The phylogenetic bifurcations are at an arbitrary stratigraphic position; thick vertical bars indicate temporal ranges based on fossil evidence (black = stratigraphic range after [77,88]; grey = stratigraphic range after literature, see text). B, Palaeogeographical maps (modified from [203]; see http://www.scotese.com webcite) for the Early and Middle Devonian showing auguritid (bottom) and pinacitid (top) occurrences: AA: Anti-Atlas, Morocco; CA: Cantabrian Mountains, Spain; CE: Celtiberian Mountains, Spain; NU: Northern Urals; ZG: Zeravshan-Gissar Range, Uzbekistan.

thumbnailFigure 3. Auguritidae and Pinacitidae showing the peculiar umbilical lid. A-D, Celaeceras mirandum, PIN No. 1869/4, lower Emsian, North Urals, Russia. The specimen and its mould from both sides (B, D) and in apertural view (C). Note the mould of a whorl fragment of Erbenoceras or a closely related early ammonoid taxon on the top left in A, documenting the rapid evolution from loosely to tightly coiled ammonoids, which resulted in the co-occurrence of both morphological extremes. E, Kimoceras lentiforme associated with a fragment of a loosely coiled anetoceratid, PIMUZ 28869, lower Emsian of Shirdak Stow, Zeravshan, Uzbekistan. F-I, Weyeroceras angustum, PIMUZ 28449, lower Emsian, Bou Tchrafine, Tafilalt, Morocco. F, left side; note the broad yellowish umbilical lid. G, apertural view; note the slender oxyconic shell morphology and the relatively complicated suture line. H, right side; note the subventral position of the siphuncle. I, septal perforation (refigured from [73]). J, Exopinacites singularis, internal mould, PIMUZ 28866, middle Eifelian, El Kahla, Tafilalt, Morocco; note the relatively complicated ventral part of the suture line.

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).

Methods

To describe and analyze this case of parallel evolution of ammonoids, their shell geometry is here quantified by means of eight classical linear measurements, which characterize the major morphological features of the ammonoid shell (Figure 4; see also [47,96]).

thumbnailFigure 4. Studied morphological parameters of the ammonoid shell. Scheme showing the linear measurements used to characterize and quantify the morphological evolution of the ammonoid shell in this study (see text for further details).

• 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 [47], 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 [100]) 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 [101]; 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 [103], 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.

Before evaluating the parallel evolution of auguritids and pinacitids, we describe the patterns of morphological variation and evolution of these two lineages (Figures 5, 6, 7, 8). Patterns of morphological evolution are examined globally by means of a multivariate analysis based on the eight studied quantitative characters of the ammonoid shell (Figure 8). We perform a principal component analysis (PCA; [104]) to examine the variation of the variables within the sample and identify the characters that contribute to observed evolutionary changes by creating high variation. Since the studied characters are of different types (size, ratio, ordinal), the PCA has been performed on the correlation matrix (data standardized to mean zero and unit standard deviation) for all characters. Then, we examine the evolution of each quantitative shell character separately by means of bivariate plots depicting their distribution through the phylogenetic sequence for the two ammonoid lineages separately (Figures 5 and 6). These plots enable an empirical evaluation of the presence or absence of directed evolutionary changes (trends) for each character. Bivariate and multivariate exploratory analyses are performed by means of the versatile palaeontological data analysis freeware PAST ([105,106]; http://folk.uio.no/ohammer/past webcite), as well as by scripts programmed by C.M. in MATLAB® (http://www.mathworks.com/ webcite).

thumbnailFigure 5. Evolution of Dmx, FCI, NLb and OLb in auguritids and pinacitids. Bivariate plots of the evolution of adult size, flank convergence index, number of lobes and relative depth of the lateral lobe through the phylogenetic sequence of the two studied ammonoid lineages, separately. Grey line indicates empirical evolutionary trend.

thumbnailFigure 6. Evolution of WSC, WER, UWI and IZR in auguritids and pinacitids. Box plots of the evolution of whorl shape compression, whorl expansion rate, umbilical index and imprint zone rate through the phylogenetic sequence of the two studied ammonoid lineages, separately. Grey line indicates empirical evolutionary trend.

thumbnailFigure 7. Outlines of shell whorl section and suture line for Auguritidae and Pinacitidae. Cladograms of the lineages leading to, and including, the Eifelian Pinacitidae and the Emsian Auguritidae. Where available, a sketch of the cross section and a suture line drawing is given. Note the parallel trend toward oxyconic shells with acute venter, with umbilical lids, and with increasing numbers of sutural elements at venter and near the umbilicus divided by a broad lobe. Sections and sutures redrawn or taken from [66,73,76,77,88,92,93]. Sections of Foordites veniens, Weyeroceras angustum and Gaurites sperandus newly drawn after PIMUZ 28867, PIMUZ 28449 and PIN No. 3981/22 from the lowermost Eifelian of Hamar Laghdad, Morocco and the lower Emsian of Bou Tchrafine, Morocco and Yusupkul Stow, Uzbekistan, and that of Celaeceras mirandum from the lower Emsian of the North Urals, Russia, after PIN No. 1869/4. Scale bars all at 1 cm length.

thumbnailFigure 8. Multivariate analysis of the eight measured shell parameters. Results of the principal component analysis (PCA) based on the eight measured shell parameters. The PCA was done on a correlation matrix. The first three principal components axes account for about 80% of the total variation in shell morphology. 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.

Since apparent trends in evolutionary series can be produced randomly [107-113], the previously and empirically identified evolutionary trends are tested statistically. Several methods exist, which are based on random walk models, to test and characterize observed trends and to distinguish the three modes of evolutionary change commonly considered in palaeontological studies: directional change (GRW, general random walk), random walk (URW, unbiased random walk), and stasis [113-116]. The evolutionary changes of each character are here evaluated by means of the maximum likelihood method of [116-119]. The method is recognized to perform well even when evolutionary sequences are incompletely sampled, which is likely for empirical palaeontological sequences as documented here [116]. It has been implemented as a package (paleoTS, [116]) in the freely available statistical environment R (http://www.r-project.org/ webcite). The method evaluates the maximum likelihood of producing the observed trends for three evolutionary modes (GRW, URW, and stasis). The relative support of each of these three models is assessed using well-established statistical means such as Akaike weights ([120]; for details, see [116-118]), which indicate the relative likelihood for each of the three evolutionary models (Figure 9). Since auguritids and pinacitids branched off from the same origin, the characters displaying directed trends shared by both lineages and supported by the statistical analysis can potentially participate to a case of parallel evolution (Figure 9).

thumbnailFigure 9. Evolutionary trajectories for Auguritidae and Pinacitidae and their Akaike weights for three evolutionary models. Standardized evolutionary trajectories of WSC, WER, UWI, and IZR and raw evolutionary trajectories of Dmx, FCI, NLb, and OLb for auguritids and pinacitids. The three tested evolutionary models are directed trends (GRW, general random walk), random trends (URW, unbiased random walk), and stasis (for details of the method, see text and [116]. Relative Akaike weights for models with more than minimal support are in bold, otherwise in italic. The most supported trends are those shared by both families (UWI, Dmx, and NLb) and characterize the parallel evolution of the two studied Devonian ammonoid lineages. For auguritids, the evolutionary changes for UWI initially weakly support the hypothesis of a directed trend, but if the outlier taxon (Weyeroceras angustus) is removed, this hypothesis is significantly supported (values in brackets).

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 [123]. 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 [121] 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 [121]). 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.

Results

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 [45]. 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 [78] 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 [92]. 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 [121]). 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 [116] 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.

Since auguritids and pinacitids originated from the same ancestor, had possible directional trends in UWI, Dmx and NLb, and finally ended with similar values for these three characters, auguritids and pinacitids may have a parallel evolution for three quantifiable traits (coiling, adult size, and suture complexity). There is, however, also the evolution of the umbilical lid, which is a presence/absence character and does not influence the quantitative results. The hypothesis of parallel evolution of the measurable characters is tested by two permutation methods based on the character subset made by UWI, Dmx and NLb (Figure 10). Using the trajectory approach of [123], it appears that there are no significant differences in the magnitude (MDsize = 0.103, Psize = 0.920) and in the direction (θdir = 14.735, Pdir = 0.087) of phenotypic evolution between the two lineages (Figure 10A). However, there are significant differences in the shape of the two evolutionary trajectories (Dshape = 0.586, Pshape = 0.001). This difference in the shape of the two trajectories is, however, expected because the taxa of each lineage are not truly equivalent and do not necessarily represent the same evolutionary steps.

thumbnailFigure 10. Evolutionary trajectories of Auguritidae and Pinacitidae in the morphological space defined by the three characters involved in the case of parallel evolution. A, Statistical evaluation of the parallel evolution by means of the trajectory approach of [123]. Plot of the first and second principal components estimated from the correlation matrix for auguritids and pinacitids based on the three standardized characters UWI, Dmx, and NLb. Statistical evaluation of the parallel evolution is indicated with and without the auguritid outlier taxon Weyeroceras angustus (dashed line). Parameters with more than minimal support are in bold. There are no significant differences in magnitude and direction of the trajectories, but they are different in shape. B, Statistical evaluation of the parallel evolution by means of the regression approach of [121]. The phylogenetic trajectory of each lineage is fitted by a linear total least square regression. The statistical evaluation is indicated without the auguritid outlier taxon. The p-value of the test (p = 0.0197) is low, but the hypothesis of parallel trajectories could not be rejected by the permutation test.

Using the regression approach of [121], 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).

Discussion

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, [135] 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.

Finally, both studied lineages evolved a peculiar morphological trait, the umbilical lid. This shell modification occurred only among the most derived species of both studied evolutionary lineages. This umbilical lid represents an extension of the lateral shell wall, passing across the umbilical shoulder toward the coiling axis and consequently more or less completely occludes the umbilicus of the ammonoid shell. This construction of the umbilical lid is a unique feature of the two studied lineages and is not known in this form from any younger ammonoid group, not even in groups having similar shell shapes. Other ammonoid groups do occasionally possess morphological features occluding the umbilicus [92,95,156], but in these cases, the structure is only superficially similar and results from a different origin (e.g., thickened umbilical walls and/or reduced umbilical width [92]). Since there are countless taxa with an overall shell shape (oxyconic shell with a very narrow umbilicus) roughly resembling that of auguritids and pinacitids, the appearance of this morphological structure (the umbilical lid) cannot be simply explained by covariation, thus making an adaptive explanation most likely. The parallel evolution of umbilical lids could be functionally explained by different, not mutually exclusive hypotheses.

(1) 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 [63]. 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.

(2) 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., [157]; 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 [158]. This is corroborated by the presence of a hyponomic sinus in our forms just like in Nautilus [146]. 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 [79].

thumbnailFigure 11. Reconstruction of Exopinacites singularis and of its possible swimming advantage involved by the presence of an umbilical lid. Speculative functional advantage of the umbilical lid, which was combined with a deep umbilical sinus in the aperture, allowing water to enter directly from the swimming direction into the mantle cavity. The position of the hyponome can be deduced from the hyponomic sinus.

(3) 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., [159]; for the description of such a case in the evolution of crustacean maxillipeds, see [7]) 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 [161]. 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 [166]. 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 [189], cameral liquid transfer [190], metabolic effect [191], developmental epiphenomena [175,192-194], and/or locomotion [195]. Nevertheless, the increase with size and through ontogeny is expected because septal formation behaves like a "viscous fingering" phenomenon (see review of [175]); 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").

Both studied lineages are no exception to this rule of covariation. The two lineages are characterized by the parallel and identical evolution toward an increasing number of lobes (Figure 5). In the case of pinacitids and auguritids, new lobes and saddles were especially inserted dorsally and ventrally, where the shell void was the narrowest (Figure 7). Note that in the two derived species Weyeroceras angustum (Auguritidae) and Exopinacites singularis (Pinacitidae) the siphuncle shifted to a subventral position causing the formation of an additional lobe [78,92]. Both lineages are also characterized by an increasing adult size and an increasing oxyconic character of the shell (more compressed shell and/or more acute venter; Figures 5 and 6). Hence, in the case of these Devonian ammonoids, the trends toward increasing number of suture line elements are likely to be induced by covariation as corroborated by the strong correlation of NLb with IZR, FCI and WSC (Figure 12). This covariation of NLb with WSC and FCI is not the indirect result of parallel evolution, because the two studied lineages display different trends for WSC and FCI (neither parallel, nor identical; Figures 5, 6, 9). Hence, both studied lineages experienced a parallel and identical trend toward more complex suture patterns, both by covariation with other evolutionary trends of the shell shape, but this is achieved differently in both lineages (mainly WSC for auguritids and FCI for pinacitids).

thumbnailFigure 12. Covariation of suture line geometry and shell geometry. Bivariate plots of IZR, FCI and WSC versus number of lobes (NLb); the number of lobes increased throughout the phylogeny of both lineages.

Conclusions

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 [200], 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 [2]. 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.

Authors' contributions

CK designed the study. CK and KDB collected the data (field, museum, literature) and made the morphometric measurements. CM performed the quantitative analyses and edited the text. CM, CK and KDB wrote the paper. All authors participated in the interpretation of the data. All authors read, discussed and approved the final manuscript.

Acknowledgements

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.

References

  1. 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. Publisher Full Text OpenURL

  2. Gould SJ: The structure of evolutionary theory. Cambridge, Harvard University Press; 2002. OpenURL

  3. 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. PubMed Abstract | Publisher Full Text OpenURL

  4. Palmer AR: Predation and parallel evolution: recurrent parietal plate reduction in balanomorph barnacles.

    Paleobiology 1982, 8:31-44. OpenURL

  5. Sheldon PR: Parallel gradualistic evolution of Ordovician trilobites.

    Nature 1987, 330:561-563. PubMed Abstract | Publisher Full Text OpenURL

  6. 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. Publisher Full Text OpenURL

  7. Averoff M, Patel NH: Crustacean appendage evolution associated with changes in Hox gene expression.

    Nature 1997, 388:682-686. PubMed Abstract | Publisher Full Text OpenURL

  8. 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. Publisher Full Text OpenURL

  9. Schluter D, Clifford EA, Nemethy M, McKinnon JS: Parallel evolution and inheritance of quantitative traits.

    American Naturalist 2004, 163:809-822. PubMed Abstract | Publisher Full Text OpenURL

  10. 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. PubMed Abstract | Publisher Full Text OpenURL

  11. Shapiro MD, Bell MA, Kingsley DM: Parallel genetic origins of pelvic reduction in vertebrates.

    Proc Natl Acad Sci USA 2006, 103:13753-13758. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  12. Tehler A, Irestedt M: Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales, Ascomycota).

    Cladistics 2007, 23:432-454. Publisher Full Text OpenURL

  13. Adams DC: Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders.

    BMC Evolutionary Biology 2010, 10:72. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  14. Gosliner TM, Ghiselin MT: Parallel evolution in opisthobranch gastropods and its implications for phylogenetic methodology.

    Systematic Zoology 1984, 33:255-274. Publisher Full Text OpenURL

  15. 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. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  16. 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. PubMed Abstract | Publisher Full Text OpenURL

  17. Cimino G, Ghiselin MT: Chemical defense and evolution in the Sacoglossa (Mollusca: Gastropoda: Opisthobranchia).

    Chemoecology 1998, 8:51-60. Publisher Full Text OpenURL

  18. Ponder WF, Lindberg DR: Phylogeny and evolution of the Mollusca. Berkeley, University of California Press; 2008. OpenURL

  19. 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. PubMed Abstract | Publisher Full Text OpenURL

  20. Simpson GG: The major features of evolution. New York, Columbia University Press; 1953. OpenURL

  21. Endler JA: Natural selection in the wild. Princeton, Princeton University Press; 1986. OpenURL

  22. Schluter D: The ecology of adaptive radiations. Oxford, Oxford University Press; 2000. OpenURL

  23. Zuckerkandl E: Molecular pathways to parallel evolution: I. Gene nexuses and their morphological correlates.

    J Molecular Evolution 1994, 39:661-678. Publisher Full Text OpenURL

  24. 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. Publisher Full Text OpenURL

  25. Haas O, Simpson GG: Analysis of some phylogenetic terms, with attempts at redefinition.

    Proceedings of the American Philosophical Society 1946, 90:319-349. PubMed Abstract OpenURL

  26. Donoghue MJ: Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny.

    Paleobiology 2005, 31:77-93. Publisher Full Text OpenURL

  27. Schindewolf OH: Konvergenz bei Korallen und bei Ammoniten.

    Fortschr Geol Paläontol 1940, 12:387-491. OpenURL

  28. Haas O: Recurrence of morphologic types and evolutionary cycles in Mesozoic ammonites.

    J Paleontol 1942, 16:643-650. OpenURL

  29. Kennedy WJ: Ammonoid evolution. In Patterns of evolution as illustrated by the fossil record. Edited by Hallam A. Amsterdam, Elsevier; 1977:251-302. OpenURL

  30. Kennedy WJ: Thoughts on the evolution and extinction of Cretaceous ammonites.

    Proc Geol Ass 1989, 100:251-279. Publisher Full Text OpenURL

  31. Bayer U, McGhee GR: Iterative evolution of Middle Jurassic ammonite faunas.

    Lethaia 1984, 17:1-6. Publisher Full Text OpenURL

  32. Dommergues JL: Ammonoids.

    In Evolutionary trends Edited by McNamara K. London. 1990, 162-187.

    Belhaven Press

    OpenURL

  33. Guex J: Origine des sauts évolutifs chez les ammonites.

    Bull Soc Vaud Sci Nat 1992, 82:117-144. OpenURL

  34. Guex J: Environmental stress and atavism in ammonoid evolution.

    Eclogae Geologicae Helveticae 2001, 94:321-328. OpenURL

  35. Guex J: Reinitialization of evolutionary clocks during sublethal environmental stress in some invertebrates.

    Earth Planetary Science Letters 2006, 243:240-253. OpenURL

  36. Saunders WB, Work DM, Nikolaeva SV: Evolution of complexity in Paleozoic ammonoid sutures.

    Science 1999, 286:760-763. PubMed Abstract | Publisher Full Text OpenURL

  37. Kiselev DN: Parallel evolution of the Arctic and central-Russian Paracadoceras (Cadoceratinae, Ammonoidea). In Contributions to current Cephalopod research: morphology, systematics, evolution, ecology and biostratigraphy. Edited by Leonova TB, Barskov IS, Mitta VV. Moscow, PIN RAS; 2009:41-46.

    [in Russian with English summary].

    OpenURL

  38. 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. Publisher Full Text OpenURL

  39. Monnet C, Bucher H, Guex J, Wasmer M: Large-scale evolutionary trends of Acrochordiceratidae Arthaber, 1911 (Ammonoidea, Middle Triassic) and Cope's rule.

    Palaeontology, in press. OpenURL

  40. 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. OpenURL

  41. Schindewolf OH: Grundfragen der Paläontologie. Geologische Zeitmessung. Organische Stammesentwicklung. Biologische Systematik. Stuttgart, Schweizerbart; 1950. OpenURL

  42. Landman NH: Heterochrony in ammonites. In Heterochrony in evolution. Edited by McKinney NL. New York, Plenum Press; 1988:159-182. OpenURL

  43. Korn D: Impact of environmental perturbations on heterochronic development in Palaeozoic ammonoids. In Evolutionary change and heterochrony. Edited by McNamara KJ. Chichester, Wiley & Sons; 1995:245-260. OpenURL

  44. Korn D: Typostrophism in Palaeozoic ammonoids. [http://www.springerlink.com/content/c536721013x67551/] webcite

    Paläont Zeit 2003, 77:445-470. OpenURL

  45. House MR: Juvenile goniatite survival strategies following Devonian extinction events. In Biotic recovery from mass extinction events. Volume 102. Edited by Hart MB. Geological Society Spec. Pub; 1996::163-185. OpenURL

  46. Guex J: A generalization of Cope's rule.

    Bull Soc géol France 2003, 174:449-452. Publisher Full Text OpenURL

  47. Korn D, Klug C: Morphological pathways in the evolution of Early and Middle Devonian ammonoids.

    Paleobiology 2003, 29:329-348. Publisher Full Text OpenURL

  48. 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. PubMed Abstract | Publisher Full Text OpenURL

  49. 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. PubMed Abstract | Publisher Full Text OpenURL

  50. De Baets K, Klug C, Korn D: Devonian pearls and ammonoid-endoparasite co-evolution.

    Acta Palaeontologica Polonica 2011, 56:159-180. Publisher Full Text OpenURL

  51. Seilacher A: Why are nautiloid and ammonoid sutures so different?

    N Jb Geol Paläont Abh 1988, 177:41-69. OpenURL

  52. Stanley SM: Macroevolution: pattern and process. San Francisco, W.H. Freeman; 1979. OpenURL

  53. Sepkoski JJ: Rates of speciation in the fossil record.

    Phil Trans R Soc London B 1998, 353:315-326. Publisher Full Text OpenURL

  54. Foote M, Sepkoski JJ: Absolute measures of the completeness of the fossil record.

    Nature 1999, 398:415-417. PubMed Abstract | Publisher Full Text OpenURL

  55. Bayer U, McGhee GR: Evolution in marginal epicontinental basins: the role of phylogenetic and ecological factors. In Sedimentary and evolutionary cycles. Volume 1. Edited by Bayer U, Seilacher A. Lecture Notes in Earth Sciences; 1985::164-220. OpenURL

  56. 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. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  57. 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. Publisher Full Text OpenURL

  58. Klug C, Korn D: The origin of ammonoid locomotion.

    Acta Palaeontologica Polonica 2004, 49:235-242. OpenURL

  59. Westermann GEG: Covariation and taxonomy of the Jurassic ammonite Sonninia adicra (Waagen).

    N Jb Geol Pal Abh 1966, 124:289-312. OpenURL

  60. Trueman AE: The meaning of orthogenesis.

    Transactions of the Geological Society of Glasgow 1940, 20:77-95. OpenURL

  61. Elmi S: Données expérimentales sur l'architecture fonctionelle de la coquille des ammonoïdes Jurassiques.

    Géobios, Mémoire Spécial 1991, 13:155-160. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  62. Jacobs DK: Shape, drag, and power in ammonoid swimming.

    Paleobiology 1992, 18:203-220. OpenURL

  63. Jacobs DK, Chamberlain JA: Buoyancy and hydrodynamics in ammonoids. In Ammonoid paleobiology. Volume 13. Edited by Landman NH, Tanabe K, Davis RA. New York, Plenum Press, Topics in Geobiology; 1996::169-223. OpenURL

  64. 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. Publisher Full Text OpenURL

  65. Nishiguchi MK, Mapes RH: Cephalopoda. In Phylogeny and evolution of the Mollusca. Edited by Ponder WF, Lindberg DR. Berkeley, University of California Press; 2008:163-199. OpenURL

  66. Erben HK: Primitive Ammonoidea aus dem Unterdevon Frankreichs und Deutschlands.

    N Jb Geol Pal Abh 1960, 110:1-128. OpenURL

  67. Erben HK: Die Evolution der ältesten Ammonoidea (Lieferung I).

    N Jb Geol Pal Abh 1964, 120:107-212. OpenURL

  68. Erben HK: Über den Ürsprung der Ammonoidea.

    Biological Reviews 1966, 41:641-658. PubMed Abstract | Publisher Full Text OpenURL

  69. Kröger B, Mapes RH: On the origin of bactritoids (Cephalopoda). [http://www.springerlink.com/content/m2010544527231rv/] webcite

    Paläont Zeit 2007, 81:316-327. OpenURL

  70. 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. Publisher Full Text OpenURL

  71. Barrande J: Systême Silurien du centre de la Bohême. I. Vol.II. Céphalopodes. Paris, Praha; 1865. PubMed Abstract OpenURL

  72. 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. OpenURL

  73. Bogoslovskji BI: Eyfelskie ammonoidei Urale i voprosy klassifikatsii agoniatitov.

    Paleontologicheskiy Zhurnal 1961, 60-70. OpenURL

  74. Bogoslovskji BI: Rannedevonskiye ammonoidei zeravchanskogo Khreta.

    Paleontologicheskiy Zhurnal 1980, 51-66. OpenURL

  75. Bogoslovskji BI: Novyy rod semeystva Auguritidae i soputstvuyushchie emu ammonoidei iz nizhnego Devona zeravshanskogo Khreta.

    Paleontologicheskiy Zhurnal 1984, 30-36. OpenURL

  76. Chlupáč I, Turek V: Devonian goniatites from the Barrandian area, Czechoslovakia.

    Rozpravy Ustředního ústavu geologického 1983, 46:1-159. OpenURL

  77. Klug C: Early Emsian ammonoids from the eastern Anti-Atlas (Morocco). [http://www.springerlink.com/content/2h2w51h10871814l/] webcite

    Paläont Zeit 2001, 74:479-515. OpenURL

  78. 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. OpenURL

  79. 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. Publisher Full Text OpenURL

  80. Nützel A, Frýda J: Paleozoic plankton revolution: evidence from early gastropod ontogeny.

    Geology 2003, 31:829-831. Publisher Full Text OpenURL

  81. Alberti GKB: Dacryoconaride und homoctenide Tentaculiten des Unter- und Miteldevons.

    Courier Forschungsinstitut Senckenberg 1993, 158:1-229. OpenURL

  82. 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. OpenURL

  83. Dzik J: Phylogeny of the Nautiloidea.

    Palaeontologia Polonica 1984, 45:1-219. OpenURL

  84. Kröger B: Adaptive evolution in Paleozoic coiled Cephalopods.

    Paleobiology 2005, 31:253-268. Publisher Full Text OpenURL

  85. 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. Publisher Full Text OpenURL

  86. 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. Publisher Full Text OpenURL

  87. Becker RT, House MR: International Devonian goniatite zonation, Emsian to Givetian, with new records from Morocco.

    Courier Forschungsinstitut Senckenberg 1994, 169:79-135. OpenURL

  88. 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. OpenURL

  89. Korn D: Morphometric evolution and phylogeny of Palaeozoic ammonoids. Early and Middle Devonian.

    Acta Geologica Polonica 2001, 51:193-215. OpenURL

  90. 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. OpenURL

  91. 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, in press. OpenURL

  92. Klug C, Korn D: Occluded umbilicus in the Pinacitinae (Devonian) and its palaeoecological implications.

    Palaeontology 2002, 45:917-931. Publisher Full Text OpenURL

  93. Bogoslovskji BI: Devonskie ammonoidei. I. Agoniatity.

    Trudy Paleontologicheskogo Instituta Akademiya Nauk SSSR 1969, 124:1-341. OpenURL

  94. 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. OpenURL

  95. Korn D, Klug C: Ammoneae Devonicae. In Fossilium Catalogus 1: Animalia. Volume 138. Edited by Riegraf W. Leiden, Backhuys; 2002::1-375. OpenURL

  96. Korn D: A key for the description of Palaeozoic ammonoids.

    Fossil Record 2010, 13:5-12. Publisher Full Text OpenURL

  97. Raup DM: Geometric analysis of shell coiling: general problems.

    J Paleont 1966, 40:1178-1190. OpenURL

  98. Raup DM: Geometrical analysis of shell coiling: coiling in ammonoids.

    J Paleont 1967, 41:43-65. OpenURL

  99. Saunders WB, Shapiro EA: Calculation and simulation of ammonoid hydrostatics.

    Paleobiology 1986, 12:64-79. OpenURL

  100. Korn D, Klug C: Conch form analysis, variability, and morphological disparity of a Frasnian (Late Devonian) ammonoid assemblage from Coumiac (Montagne Noire, France). In Cephalopods - Present and Past. Edited by Landman NH, Davis RA, Manger W, Mapes RH. New York, Springer; 2007:57-86. OpenURL

  101. Ruzhencev VE: Filogeneticheskaya sistema paleozoyskikh ammonoidey.

    Byulleten' Moskovskogo obshchestva ispytately prirody, novaya seriya, otdel geologicheskiy 1957, 31:49-64. OpenURL

  102. Wake DB: Homoplasy: the result of natural selection or evidence of design constraints?

    American Naturalist 1991, 138:543-567. Publisher Full Text OpenURL

  103. Stayton CT: Testing hypotheses of convergence with multivariate data: morphological and functional convergence among herbivorous lizards.

    Evolution 2006, 60:824-841. PubMed Abstract OpenURL

  104. Jackson JE: A user's guide to principal components. New York, John Wiley; PubMed Abstract | Publisher Full Text OpenURL

  105. Hammer Ø, Harper DAT, Ryan PD: PAST, Paleontological Statistics Software Package for Education and Data Analysis.

    Palaeontologia Electronica 2001, 4:1D. OpenURL

  106. Hammer Ø, Harper DAT: Paleontological data analysis. Oxford, Blackwell Publishing; 2005. OpenURL

  107. Raup DM, Crick RE: Evolution of single characters in the Jurassic ammonite Kosmoceras.

    Paleobiology 1981, 7:200-215. OpenURL

  108. Bookstein FL: Random walk and the existence of evolutionary rates.

    Paleobiology 1987, 13:446-464. OpenURL

  109. Bookstein FL: Random walk and the biometrics of morphological characters.

    Evolutionary Biology 1988, 9:369-398. OpenURL

  110. Raup DM: Stochastic models in evolutionary paleobiology. In Patterns of evolution as illustrated by the fossil record. Edited by Hallam A. Amsterdam, Elsevier; 1997:59-78. OpenURL

  111. Raup DM, Gould SJ: Stochastic simulation and evolution of morphology - towards a nomothetic paleontology.

    Systematic Zoology 1974, 23:305-322. Publisher Full Text OpenURL

  112. Roopnarine PD, Byars G, Fitzgerald P: Anagenetic evolution, stratophenetic patterns, and random walk models.

    Paleobiology 1999, 25:41-57. OpenURL

  113. Sheets HD, Mitchell CE: Why the null matters: statistical tests, random walks and evolution.

    Genetica 2001, 112-113:105-125. PubMed Abstract | Publisher Full Text OpenURL

  114. Gingerich PD: Quantification and comparison of evolutionary rates.

    American Journal of Science 1993, 293A:453-478. OpenURL

  115. Roopnarine PD: The description and classification of evolutionary mode: a computational approach.

    Paleobiology 2001, 27:446-465. Publisher Full Text OpenURL

  116. Hunt G: Fitting and comparing models of phyletic evolution: random walks and beyond.

    Paleobiology 2006, 32:578-601. Publisher Full Text OpenURL

  117. Hunt G: Phenotypic variation in fossil samples: modeling the consequences of time-averaging.

    Paleobiology 2004, 30:426-443. Publisher Full Text OpenURL

  118. Hunt G, Bell MA, Travis MP: Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage.

    Evolution 2008, 62:700-710. PubMed Abstract | Publisher Full Text OpenURL

  119. 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. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  120. Anderson DR, Burnham KP, Thompson WL: Null hypothesis testing: problems, prevalence, and an alternative.

    Journal of Wildlife Management 2000, 64:912-923. Publisher Full Text OpenURL

  121. 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. PubMed Abstract | Publisher Full Text OpenURL

  122. Webster M, Zelditch ML: Evolutionary modifications of ontogeny: heterochrony and beyond.

    Paleobiology 2005, 31:354-372. Publisher Full Text OpenURL

  123. Adams DC, Collyer ML: A general framework for the analysis of phenotypic trajectories in evolutionary studies.

    Evolution 2009, 63:1143-1154. PubMed Abstract | Publisher Full Text OpenURL

  124. Collyer ML, Adams DC: Analysis of two-state multivariate phenotypic change in ecological studies.

    Ecology 2007, 88:683-692. PubMed Abstract | Publisher Full Text OpenURL

  125. Klug C: Life-cycles of some Devonian ammonoids.

    Lethaia 2001, 34:215-233. Publisher Full Text OpenURL

  126. Newell ND: Phyletic size increase, an important trend illustrated by fossil invertebrates.

    Evolution 1949, 3:103-124. PubMed Abstract | Publisher Full Text OpenURL

  127. Rensch B: Evolution above the species level. New York, Columbia University Press; 1959. OpenURL

  128. Gould SJ: Allometry and size in ontogeny and phylogeny.

    Biological Reviews 1966, 41:587-640. PubMed Abstract | Publisher Full Text OpenURL

  129. Stanley SM: An explanation for Cope's rule.

    Evolution 1973, 27:1-26. Publisher Full Text OpenURL

  130. Kurten B: On the variation and population dynamics of fossil and Recent mammal populations.

    Acta Zool Fennica 1953, 76:1-122. OpenURL

  131. Brown JH, Maurer BA: Body size, ecological dominance and Cope's rule.

    Nature 1986, 324:248-250. Publisher Full Text OpenURL

  132. Hone DWE, Benton MJ: The evolution of large size: how does Cope's Rule work?

    Trends in Ecology & Evolution 2005, 20:4-6. PubMed Abstract | Publisher Full Text OpenURL

  133. Hallam A: Evolutionary size increase and longevity in Jurassic bivalves and ammonites.

    Nature 1975, 258:493-496. Publisher Full Text OpenURL

  134. Thierry J: Rythme d'évolution des caractères morphologiques chez les Macrocephalitidae (Cephalopoda, Ammonitina, Jurassique moyen). In Modalités, rythmes, mécanismes de l'évolution biologique. Volume 330. Edited by Chaline J. Paris, Editions du CNRS, Colloques Internationaux du Centre National de la Recherche Scientifique; 1982::211-218. OpenURL

  135. Dommergues JL, Montuire S, Neige P: Size patterns through time: the case of the Early Jurassic ammonite radiation.

    Paleobiology 2002, 28:423-434. Publisher Full Text OpenURL

  136. Hyatt A: Genesis of the Arietitidae.

    Smithsonian Contributions to Knowledge 1889, 673:1-238. OpenURL

  137. 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. OpenURL

  138. Guex J: Associations virtuelles et discontinuités dans la distribution des espèces fossiles: un exemple intéressant.

    Bull Soc Vaud Sci Nat 1981, 359:179-197. OpenURL

  139. Donovan DT: Ammonite shell form and transgression in the British Lower Jurassic. In Sedimentary and evolutionary cycles. Volume 1. Edited by Bayer U, Seilacher A. Lecture Notes in Earth Sciences; 1985::164-220. OpenURL

  140. Saunders WB, Work DM, Nikolaeva SV: The evolutionary history of shell geometry in Paleozoic ammonoids.

    Paleobiology 2004, 30:19-43. Publisher Full Text OpenURL

  141. 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. Publisher Full Text OpenURL

  142. Elmi S: Loi des aires, couche-limite et morphologie fonctionnelle de la coquille des cephalopods (ammonoïdes).

    Géobios, Mémoire Spécial 1993, 15:121-138. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  143. Seki K, Tanabe K, Landman NH, Jacobs DK: Hydrodynamic analysis of Late Cretaceous desmoceratine ammonites.

    Revue Paléobiologie, Volume spécial 2000, 8:141-155. OpenURL

  144. De Blasio FV: The role of suture complexity in diminishing strain and stress in ammonoid phragmocones.

    Lethaia 2008, 41:15-24. Publisher Full Text OpenURL

  145. Ward PD: In search of Nautilus. New York, Simon and Schuster; 1988. OpenURL

  146. Jacobs DK, Landman NH: Nautilus, a poor model for the function and behavior of ammonoids?

    Lethaia 1993, 26:101-111. Publisher Full Text OpenURL

  147. 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. Publisher Full Text OpenURL

  148. Batt RJ: Ammonite shell morphotype distributions in the Western Interior Greenhorn Sea and some paleoecological implications.

    Palaios 1989, 4:32-42. Publisher Full Text OpenURL

  149. Westermann GEG: Ammonoid life and habitat. In Ammonoid paleobiology. Volume 13. Edited by Landman NH, Tanabe K, Davis RA. New York, Plenum Press, Topics in Geobiology; 1996::607-707. OpenURL

  150. Westermann GEG, Tsujita CJ: Life habits of ammonoids. In Functional morphology of the invertebrate skeleton. Edited by Savazzi E. Chichester, John Wiley and Sons; 1999:299-325. OpenURL

  151. Neige P, Marchand D, Bonnot A: Ammonoid morphological signal versus sea-level changes.

    Geol Mag 1997, 134:261-264. Publisher Full Text OpenURL

  152. 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. OpenURL

  153. 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. In Advancing research on living and fossil cephalopods. Edited by Olóriz F, Rodríguez-Tovar FJ. New York, Kluwer/Plenum; 1999:273-293. OpenURL

  154. Olóriz F, Palmqvist P, Pérez-Claros A: Morphostructural constraints and phylogenetic overprint on sutural frilling in Late Jurassic ammonites.

    Lethaia 2002, 35:158-168. Publisher Full Text OpenURL

  155. 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. Publisher Full Text OpenURL

  156. Tozer ET: Observations on the shell structure of Triassic ammonoids.

    Palaeontology 1972, 15:637-654. OpenURL

  157. Packard A, Bone Q, Hignette M: Breathing and swimming movements in a captive Nautilus.

    J Marine Biol Assoc United Kingdom 1980, 60:313-327. Publisher Full Text OpenURL

  158. Engeser T: The Position of the Ammonoidea within the Cephalopoda. In Ammonoid paleobiology. Volume 13. Edited by Landman NH, Tanabe K, Davis RA. New York, Plenum Press, Topics in Geobiology; 1996::3-19. OpenURL

  159. 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. PubMed Abstract | Publisher Full Text OpenURL

  160. Lindsey CC: Experimental study of meristic variation in a population of threespine sticklebacks, Gasterosteus aculeatus.

    Can J Zool 1962, 40:271-312. Publisher Full Text OpenURL

  161. Minelli A: Perspectives in animal phylogeny and evolution. Oxford, Oxford University Press; 2009. OpenURL

  162. Seilacher A: Fabricational noise in adaptive morphology.

    Systematic Zoology 1973, 222:451-465. OpenURL

  163. Hammer Ø, Bucher H: Buckman's first law of covariation - a case of proportionality. [http://onlinelibrary.wiley.com/doi/10.1080/00241160510013196/abstract] webcite

    Lethaia 2005, 38:67-72. OpenURL

  164. 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. Publisher Full Text OpenURL

  165. 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. Publisher Full Text OpenURL

  166. Buckman SS: A monograph of the ammonites of the Inferior Oolite Series. London, Palaeontographical Society; 1892. OpenURL

  167. 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. Publisher Full Text OpenURL

  168. Yacobucci MM: Buckman's paradox: variability and constraints on ammonoid ornament and shell shape. [http://onlinelibrary.wiley.com/doi/10.1080/00241160410004755/abstract] webcite

    Lethaia 2004, 37:57-69. OpenURL

  169. 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. OpenURL

  170. Kennedy WJ, Cobban WA: Aspects of ammonite biology, biogeography, and biostratigraphy.

    Spec Pap Palaeontol 1976, 17:1-94. OpenURL

  171. 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. OpenURL

  172. Dagys A, Weitschat W: Intraspecific variation in Boreal Triassic ammonoids.

    Géobios 1993, 26:107-109. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  173. 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. OpenURL

  174. Morard A, Guex J: Ontogeny and covariation in the Toarcian genus Osperleioceras (Ammonoidea).

    Bull Soc géol France 2003, 174:607-615. Publisher Full Text OpenURL

  175. Checa AG, Garcia-Ruiz JM: Morphogenesis of the septum in ammonoids. In Ammonoid paleobiology. Edited by Landman NH, Tanabe K, Davies RA. New York, Plenum Press; 1996:253-296. OpenURL

  176. Kullmann J, Wiedmann J: Significance of sutures in phylogeny of Ammonoidea.

    University of Kansas Paleontological Contributions Paper 1970, 47:1-32. OpenURL

  177. Donovan DT: Evolution of the Arietitidae and their descendants. In Deuxième colloque du Centre International d'Etude du Lias (C.I.E.L.), Lyon 27-30 Mai 1996. Edited by Almeras Y, Rouget C. Lyon, Les Cahiers de l'Institut Catholique de Lyon, Série Sciences; 1987:123-138. OpenURL

  178. Donovan DT: Evolution in some early Jurassic ammonites: Asteroceratinae, Oxnoticeratidae and related forms. In Proceedings of the Third Pergola International Symposium ''Fossili, Evolution, Ambiente'' October 1990. Volume 1. Edited by Pallini G. Palaeopelagos Special Publication; 1994::383-396. OpenURL

  179. Korn D: A modified Balloon model for septa of early ammonoids.

    Lethaia 1997, 30:39-40. OpenURL

  180. 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. OpenURL

  181. 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. Publisher Full Text OpenURL

  182. 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. Publisher Full Text OpenURL

  183. Bockwinkel J, Becker RT, Ebbighausen V: Upper Givetian ammonoids from Dar Kaoua (Tafilalt, SE Anti-Atlas, Morocco).

    Berliner Paläobiologische Abhandlungen 2009, 10:61-128. OpenURL

  184. Brühwiler T, Bucher H, Goudemand N: Smithian (Early Triassic) ammonoids from Tulong, South Tibet.

    Géobios 2010, 43:403-431. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  185. Saunders WB: The ammonoid suture problem: relationships between shell and septum thickness and suture complexity in Paleozoic ammonoids.

    Paleobiology 1995, 21:343-355. OpenURL

  186. Checa AG: Fabrication and function of ammonite septa, comment on Lewy.

    J Paleont 2003, 77:790-791. Publisher Full Text OpenURL

  187. 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. OpenURL

  188. Hewitt RA, Westermann GEG: Mechanical significance of ammonoid septa with complex sutures.

    Lethaia 1997, 30:205-212. OpenURL

  189. Henderson RA: A muscle attachment proposal for septal function in Mesozoic ammonites.

    Palaeontology 1984, 27:461-486. OpenURL

  190. Daniel TL, Helmuth BS, Saunders WB, Ward PD: Septal complexity in ammonoid cephalopods increased mechanical risk and limited depth.

    Paleobiology 1997, 23:470-481. OpenURL

  191. Pérez-Claros JA: Allometric and fractal exponents indicate a connection between metabolism and complex septa in ammonites.

    Paleobiology 2005, 31:221-232. Publisher Full Text OpenURL

  192. Garcia-Ruiz JM, Checa A: A model for the morphogenesis of ammonoid septal sutures.

    Géobios, Mémoire Spécial 1993, 15:157-162. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  193. Garcia-Ruiz JM, Checa A, Rivas P: On the origin of ammonite sutures.

    Paleobiology 1990, 16:349-354. OpenURL

  194. Hammer Ø: The development of ammonoid septa: an epithelial invagination process controlled by morphogens?

    Historical Biology 1999, 13:153-171. Publisher Full Text OpenURL

  195. Seilacher A, LaBarbera M: Ammonites as Cartesian divers.

    Palaios 1995, 10:493-506. Publisher Full Text OpenURL

  196. Seilacher A: Arbeitskonzept zur Konstruktions-Morphologie.

    Lethaia 1970, 3:393-396. Publisher Full Text OpenURL

  197. Hewitt RA: Architecture and strength of the ammonoid shell. In Ammonoid paleobiology. Volume 13. Edited by Landman NH, Tanabe K, Davis RA. New York, Plenum Press, Topics in Geobiology; 1996::297-339. OpenURL

  198. Saunders WB, Work DM: Shell morphology and suture complexity in Upper Carboniferous ammonoids.

    Paleobiology 1996, 22:189-218. OpenURL

  199. Allen EG: Understanding ammonoid sutures. New insights into the dynamic evolution of Paleozoic suture morphology. In Cephalopods Present and Past: new insights and fresh perpsectives. Edited by Landman NH, Davis RA, Mapes RH. Dordrecht, Springer; 2007:159-180. OpenURL

  200. Willmer P: Convergence and homoplasy in the evolution of organismal form. In Origination of organismal form. Edited by Muller GB, Newman SA. Massachusetts, MIT Press, The Vienna series of theoretical biology; 2003:33-50. OpenURL

  201. Shigeno S, Sasaki T, Boletzky Sv: Origins of cephalopod body plans: A geometrical and developmental basis for the evolution of vertebrate-like organ systems. In Cephalopods Present and Past. Edited by Tanabe K, Shigeta Y, Sasaki T, Hirano H. Tokai University Press; 2010:23-34. OpenURL

  202. Lardeux H, Morzadec P, Bultynck P, Walliser OH: La Grange Limestone. In Massif Armoricain, Field Excursion Guidebook. Edited by Lardeux H, Morzadec P. International Subcommission on Devonian Stratigraphy; 1979:5-7. OpenURL

  203. Scotese CR: Digital Paleogeographic Map Archive on CD-ROM. Arlington, Texas, PALEOMAP Project; 2001. OpenURL