Morphological evolution of the skull roof in extinct temnospondyl amphibians mirrors conservative ontogenetic patterns

Celeste M. Pérez-Ben1*, Ana M. Báez1, 2, and Rainer R. Schoch3

1CONICET. Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y

Naturales, Universidad de Buenos Aires, Buenos Aires 1428 Argentina

2Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires 1405

Argentina.

3Staaliches Museum für Naturkunde, Stuttgart, Baden-Württemberg 70191 Germany

and Staaliches Museum für Naturkunde, Stuttgart, Baden-Württemberg 70191

Germany.

* E-mail: [email protected] Abstract.—Understanding the evolution of development is essential to unravel how morphological evolution proceeds in phenotypic space and how the resulting morphological disparity originates. In particular, the study of ontogenetic allometric patterns and their evolution is relevant because allometry is thought to constrain morphological evolution to specific directions and to promote morphological change by producing pronounced phenotypic differences along phenotypic lines of least evolutionary resistance. The extinct clade of temnospondyl amphibians enables a unique opportunity to investigate the interplay between developmental and morphological evolution in deep time because individuals of different growth stages are known for numerous species. Temnospondyls lived during the Paleozoic and

Mesozoic in a wide range of habitats and had different life cycles (e.g., metamorphosing, neotenic). In spite of this, cranial morphology is markedly conserved within the clade. Herein, we investigate whether the ontogenetic allometric patterns of the skull roof in temnospondyls are also conserved or reflect the variety of their ecological adaptations and life-cycles and examine the extent to which the ontogenetic allometry may account for the adult cranial morphology. Using geometric morphometric techniques, we computed the ontogenetic allometries of 13 temnospondyl species and the evolutionary allometry of the clade. A conserved pattern of morphological change during ontogeny not associated to phylogeny or life- style is recovered across the clade. Furthermore, the evolutionary allometry strongly resembles the conserved ontogenetic changes of shape. These results suggest strong ancestral constraints in cranial development, which, in turn, may explain the low morphological disparity in the group.

Introduction Understanding the evolution of development is essential to unravel how morphological evolution moves in phenotype space (Hall, 2000; Wilson, 2013) and how the resulting morphological disparity originates. Morphology results from development (Zeldtich et al., 2016) and, thus, developmental pathways affect both the direction and extent of morphological evolution (Adams and Nistri 2010; Wagner and

Altenberg, 1996; Gerber, 2014). Variational properties of development affect the propensity of traits to vary thus reducing the evolutionary response to external selective forces to certain directions of phenotype space and, consequently, also reducing the likely morphological outcomes.

Among the multiple aspects that drive and characterize developmental pathways, the study of ontogenetic allometric patterns and their evolution is particularly relevant because allometry (i.e., the statistical relationship between size and shape, Mitteroecker et al., 2013) is thought to constrain evolution to specific directions of shape change by integration (i.e., covariation among traits) but at the same time to facilitate phenotypic differentiation along lines of least evolutionary resistance (Cardini and Polly, 2013). Therefore, establishing the ontogenetic component of allometric transformations is key to understand the diversification in size and shape.

Ontogenies of fossil taxa, in contrast to those of extant taxa, offer a deep-time perspective on this topic by making it possible to study the evolution of ontogenetic allometry over a geological time-span. In this regard, extinct temnospondyl amphibians enable a unique opportunity to investigate the interplay between developmental and morphological evolution in deep time because numerous species are represented by individuals of different growth stages, including exquisitely preserved gill-bearing larvae (Boy and Sues, 2002). Temnospondyls constitute a specious clade of amphibians (about 300 species) known from the Visean (Early Carboniferous, 330 myr) through the Aptian (Early

Cretaceous, 115 myr) (Schoch, 2014a). Although still a topic of ongoing debate, a widely accepted hypothesis considers that modern amphibians (i.e., frogs, salamanders, and caecilians) originated from a clade of Paleozoic temnospondyls, the dissorophoids (e.g., Maddin et al., 2012), making the study of temnospondyls particularly relevant among the diverse extinct amphibian groups. Temnospondyls

(henceforth the non-lissamphibians) lived in a wide range of habitats – lakes, rivers, marine and terrestrial environments – and had different life history strategies, including species with aquatic larvae that transformed gradually into aquatic adults, others with aquatic larvae that suffered a drastic metamorphosis that led to fully terrestrial adults, and neotenic species (Schoch, 2014b). The diversity in ecologies and life-cycles is reflected in a wide range of morphotypes and body sizes, including large aquatic predators with body lengths up to six meters (many stereospondylomorphs), heavily armored terrestrial forms (dissorophids), tiny lizard-like taxa (terrestrial amphibamids), and aquatic perennibranchiates (micromelerpetontids and branchiosaurids) (Schoch, 2014a; Witzmann et al., 2009). Despite this diversity, the dermal skull roof of temnospondyls is strikingly conserved over geological time, showing the identical set of dermal bones in conserved relative positions, with only few exceptions (e.g., some plagiosaurids; Schoch and Milner, 2014).

Temnospondyls have already been the focus of morphogeometric studies at both the macroevolutionary (e.g., Stayton and Ruta, 2006; Angielczyk and Ruta,

2012) and ontogenetic levels (Witzmann et al., 2009). However, to our knowledge, no work has addressed the two levels comparatively and the only comparative study on shape change through ontogeny –Witzmann et al., 2009- was based on a methodology that assumed a conserved allometric pattern among species without testing whether this is the case (discussed below). Taking this into account, the present study aims to complement previous work by: 1) assessing the cranial ontogenetic allometric patterns in temnospondyls; 2) exploring the factors that might explain these patterns; and 3) examining the extent to which the ontogenetic allometry may account for the disparity of adult cranial morphologies.

Materials and methods

Phylogenetic Relationships.— An explicit phylogenetic context is essential to analyze morphological and ontogenetic evolution rigorously and to calculate the evolutionary allometry using phylogenetic general least squares (PGLS, see below).

Because our taxonomic sampling included species of many different temnospondyl groups, we constructed a synthetic tree combining previous phylogenetic hypotheses

(Fig. 1). We used the topology recovered by Schoch (2013) in his study of major temnospondyl clades as a backbone tree. For the non-stereospondyl

Stereospondylomorpha section of the phylogeny, we replaced the topology of Schoch

(2013) by the one recovered by Schoch and Witzmann (2009a) because the latter included more taxa and the two species of Glanochthon considered in our ontogenetic analyses. The only discrepancy between the two topologies is that in the preferred tree of Schoch (2013), Archegosaurus and Glanochthon were recovered as a clade, whereas these taxa formed a grade towards Stereospondyli in the study of Schoch and

Witzmann (2009a). However, Schoch also recovered the latter topology in some alternative scenarios. The clade Dissorophoidea recovered by Schoch (2013) was also replaced by the more detailed topology used in Pérez-Ben et al. (2018). Ontogenetic patterns.—We calculated the ontogenetic allometry (i.e., how shape changes through ontogeny) of the skull roof in 13 temnospondyl species representing different major clades and life-styles (Supplementary Material) using geometric morphometric techniques. In the analyses we included every temnospondyl taxon represented by at least two relatively well-preserved skulls of different ontogenetic stages available to us. Because of the lack of age data, we used skull length as a proxy of ontogenetic stage to select the specimens and, when available, qualitative features whose changes throughout ontogeny are known, such as the degree of ornamentation of dermal bones (see Boy and Sues, 2000 for a discussion on the matter). Given that skull length is a continuous variable, establishing the differences in this variable that represent different stages instead of within-stage variation was inevitably arbitrary when no qualitative-proxies were available. We limited the analyses to the skull roof because it is the part of the cranium usually best preserved and, besides, is completely formed at a very early ontogenetic stage in most temnospondyls (Witzmann et al., 2009). Moreover, we only considered the medial region of the skull roof because the lateral bones are not well preserved in many specimens and, in addition, those with a vertical component are not preserved in natural position in species that are two-dimensionally preserved (e.g.,

Micromelerpeton, Sclerocephalus, Glanochthon).

We used images of the skull roof in dorsal view consisting of photographs of fossil specimens studied by first hand and photographs, interpretative drawings, or reconstructions from the literature in the case of relevant taxa to which we could not have direct access (Supplementary Material). Regarding the fossil material studied by first hand, specimens with minor deformations were included after having been partially reconstructed digitally. Only interpretative drawings and reconstructions whose accuracy could be checked were included.

On each image we digitized 11 landmarks (Fig. 2; Table 1) using TPSDIG2

(Rohlf, 2006). The selection of landmarks was based on the trade-off between capturing the cranial shape in detail and maximizing the number of individuals on which the landmarks could be digitized confidently. Landmarks were digitized in the best-preserved cranial half. The landmark configurations of the hemi-crania were reflected on the plane of sagittal symmetry (defined by landmarks 1 to 5, Table 1) to avoid putative artefacts of the Procrustes aligment by using the R-function AMP.r written by Annat Haber (available at http://life.bio.sunysb.edu/morph/morphmet/AMP.R).

The following analyses were performed in R using the Geomorph package

(Adams and Otarola-Castillo 2013). We superimposed the landmark configurations of all individuals by a Generalized Procrustes Analysis (GPA). We further worked with the aligned coordinates of one half of the skull. Centroid sizes (CS) were calculated and regressions of shape coordinates on ln CS were carried out separately for each species represented by three or more individuals to determine their ontogenetic allometries. Because of the low number of specimens of most species, we did not test for allometry statistically. Shape changes during ontogeny are obvious to the naked eye and any non-rejection of the null hypothesis of isometry (i.e., the slope coefficients of the regression vector are not different from cero) might be an artefact of the small sample size and not meaningful biologically. We visualized the shape changes through ontogeny by deformations grids depicting deformations from the species mean shape to the shapes predicted on the regression vector (i.e., allometric vector) corresponding to different values of ln CS. For Cacops, which was represented by two individuals only, the deformation grid was generated to visualize changes from the smallest to the largest specimen.

In order to compare the ontogenetic allometries among the species, we used the “allometric space” approach, which has been proved to provide a better understanding of the evolution of ontogenetic trajectories and its relationship with morphological disparity (Gerber and Hopkins, 2011; Streling et al., 2017). An allometric space is a multivariate ordination of taxa based on the slope coefficients of multivariate regressions of shape on size (Gerber and Hopkins, 2011), where each ontogenetic trajectory is represented by a single point. To construct the allometric space, the coefficient vectors obtained from the regressions were standardized to unit length and subjected to a PCA (Mitteroecker et al., 2013) to help visualize the ordination of taxa in a reduced space (Gerber and Hopkins, 2011). Because we found that Gerrothorax was an outlier in the allometric space, we performed a second PCA excluding this taxon. Using this PCA, we analyzed whether the distribution of taxa in the allometric space was related to their life-styles and /or clade in two ways: 1) qualitatively by observing possible groups in the reduced allometric space formed by the first three PCs, and 2) by a cluster analysis of the matrix of Euclidean distances between each pair of taxa using UPGMA. We differentiated the taxa according to three ecological habits of the adults: fully aquatic, terrestrial, and amphibian. Among the aquatic taxa, we further distinguished neotenic species from non-neotenic ones. In summary, we defined four groups based on habitat and life cycle. To simplify the nomenclature, we refer to these categories (i.e., neotenic fully aquatic, non-neotenic fully aquatic, terrestrial, and amphibian) as life-styles. The assignments to the groups were based on the literature (Supplementary Material). We did not test for grouping statistically because of the low number of species and unbalanced group sizes. Macroevolutionary patterns.—In order to assess the diversity in adult cranial shape of temnospondyls, we digitized the same set of landmarks of the ontogenetic section in 50 species, each represented by a single specimen. We used the same type of images and reflected the landmark configurations as before. We selected the taxa to be included in the study so as to represent the major temnospondyl clades and capture the morphological diversity of the group. Only taxa represented by well-preserved material and whose phylogenetic placements are reasonably known were included.

Given the lack of age data, we used individuals that are large according to the size range known for their respective species. It is noteworthy that we considered non- stereospondyl stereospondylomorphs as a clade, in spite of they being actually a paraphyletic group. We did this because they formed a monophyletic group before the

Triassic radiation of stereospondyls according the phylogenetic hypothesis used in this study.

We performed a GPA of the landmark configurations and a PCA of the resulting shape coordinates of one half of the skull. Because we found that

Gerrothorax was an outlier in the morphospace, we performed a second PCA excluding it. The following analyses were carried out considering the latter PCA. To evaluate the influence of life-style on skull shape variation, we fitted the life-style variable to the first three PCs scores, which account for the 84% of the variance, using

PGLS. PGLS is a method that deals with the phylogenetic non-independence of interspecific data (Rohlf, 2001; Garland et al., 2005) and is implemented in the

ProcD.pgls function of Geomorph. Given that PGLS requires specifications of branch lengths and the topologies used to construct the supertree lack this information because they are the result of cladistic analyses, we set all branch lengths to one, which corresponds to a speciational model of evolution (Garland et al., 1992), following previous evolutionary allometric analyses (e.g., Yeh, 2002; Kimmel et al.,

2009; Pérez-Ben et al., 2018). The statistical significance was estimated by a permutation test using 10000 random permutations.

The same four adult life-styles (i.e., neotenic fully aquatic, non-neotenic fully aquatic, terrestrial, and amphibian) of the ontogenetic analysis were used; assignments to the groups were based on the literature (Supplementary Material). We performed a second test grouping the amphibian and both fully aquatic (i.e., neotenic and non- neotenic) life-styles together due to the low number of amphibian and neotenic species and because some taxa were alternatively described as fully or semi-aquatic

(e.g., most individuals of Sclerocephalus haeuseri have been described as fully aquatic, but some others show morphological features consistent with a semiaquatic ecology; Schoch, 2009).

Evolutionary allometry was calculated by regressing the shape coordinates of all the taxa excluding Gerrothorax on ln CS using PGLS. Allometry was tested by

10000 permutations. We visualized the evolutionary allometry by deformation grids in the same way as for the ontogenetic allometry.

Results

Ontogenetic allometry.—Three patterns of shape change throughout ontogeny are recovered for every species sampled, excepting Gerrothorax: 1) the snout elongates; 2) the orbits become shorter; and 3) parietals and postparietals become narrower (Figs. 3). By contrast, in Gerrothorax the snout shortens throughout ontogeny. Other extended trends are the shortening of postparietals (in branchiosaurids, Acanthostomatops, Archegosaurus, Glanochthon angusta, Sclerocephalus, and Micromelerpeton; opposite trend in Cacops, Mastodonsaurus, and Gerrothorax; no change in the remaining taxa) and the extension of the area between the posterior edge of the orbit and the anterior margin of the tabular (in A. caducus, Cochleosaurus, Archegosaurus, G. angusta, G. latirostris, Sclerocephalus,

Micropholis, Cacops, and Gerrothorax; no change in the remaining taxa). The length of the suture between the supratemporal and the tabular also changes markedly through ontogeny, but with opposite trends: whereas it increases in branchiosaurids,

Acanthostomatops, G. latirostris, and Gerrothorax, the suture becomes shorter in

Cochleosaurus, Archegosaurus, G. angusta, Sclerocephalus, Micromelerpeton, and

Mastodonsaurus.

Allometric space.—Gerrothorax was recovered as an outlier in the allometric space, so the following results correspond to analyses excluding this taxon. The first three principal components of the PCA of the standardized regression vectors account for the 66.8% of the variance (PC1: 28.5%; PC2: 23.7%; PC3: 14.6%). In the reduced allometric spaces formed by PC1-PC2 and PC1-PC3 (Fig. 4), it is not clear whether taxa group according to their life-style or clade because they partially do so by both factors. The cluster analysis confirms that there are no clear groupings (Fig. 4).

Adult shapes in the morphospace.— Gerrothorax was also recovered as an outlier in the morphospace, so it was excluded from subsequent analyses. When all the species are taken into account except Gerrothorax, PC1, PC2 and PC3 account for the 84.2% of the variance (PC1: 60.4%; PC2: 15.1%; PC3: 8.7%). The ordination of taxa in the morphospace and deformation grids corresponding to extreme values of

PC1 are shown in Figure 5. Positive values of PC1 indicate shorter snouts, longer orbits, and slightly longer and wider postorbital skull tables than the consensus configuration. Positive values of PC2 also indicate longer orbits and wider postorbital regions, but, in contrast to PC1, slightly longer snouts and markedly shorter postorbital skull tables than the consensus. Positive values of PC3 correlate with longer orbits and frontals and shortening of the area between the posterior margin of the orbits and the anterior margin of tabulars.

Clades group in the reduced morphospace PC1-PC2. An exception is

Batrachosuchus, which lies far from its sister taxon, Laidleira, and the other stereospondylomorphs. In this reduced morphospace, some clades overlap, such as non-stereospondyl stereospondylomorphs and capitosaurs, or trematosaurs and dvinosaurs. In the reduced morphospace PC1-PC3, the clades also group, but the overlaping changes: non-stereospondyl stereospondylomorphs and capitosaurs lay apart, whereas dissorophoids are closer to each other and more overlapped to other clades.

The only life-style that occupies a distinctive (i.e., non-overlapping) region of the morphospace is the non-neotenic aquatic one, laying apart from the other styles along the PC2. The PGLS shows a non-significant relationship between shape and life-style.

Evolutionary allometry–Evolutionary allometric regression is statistically significant (p<0.05) and the evolutionary allometric vector explains 10.8% of the variance. Evolutionary allometric changes of shape consist of elongation of the snout, shortening of orbits, elongation of postorbital region with longer postparietals, and diminishing skull width when the CS increases (Fig. 5).

Discussion There is a conserved pattern of cranial shape change through ontogeny in temnospondyls, which consists of the elongation of the snout, the shortening of the orbits, and the diminishing width of parietals and postparietals. The same general pattern has been previously recognized by qualitative comparisons of ontogenetic stages of different temnospondyl species (e.g., Steyer, 2003 in Watsonisuchus madagascariensis) and in studies based on linear morphometrics in Micromelerpeton credneri (Witzmann and Pfretzschner, 2003) and Archegosaurus decheni (Witzmann and Scholz, 2007), although the width of the postparietals was not evaluated.

Witzmann et al. (2009), in their comparative geometric morphometric study of temnospondyl ontogenies, recovered a similar pattern. However, in our opinion their results are based on the misinterpretation of the first PC of a PCA performed on all the ontogenetic stages of all species considered together. Hence PC1 represents the axis of global major variance of the sample, which does not correspond to any biological variance and not necessarily points in the same direction than those of the different ontogenetic trajectories. In other words, by doing this PCA, it is not possible to visualize the potentially different directions of the particular ontogenetic trajectories and, therefore, to test for conserved or divergent patterns. Taking this into account, in the present study we address comparatively the ontogenetic trajectories in temnospondyls from a morphometric point of view.

Why the ontogenetic allometric patterns listed above were conserved in the evolution of temnospondyls merits consideration. Parietals and postparietals overlie the braincase and the otic capsules, which are rarely completely ossified in temnospondyls. Consequently the proportionally wider parietals and postparietals of the younger developmental stages might be related to constraints on the sizes of the brain and the inner ear due to functional needs. Likewise, constraints related to functional eye size and attached musculature might explain the large orbits of early stages. On the other hand, the trend of larger braincases in early stages fits the repetitive pattern observed across vertebrates, where braincase size scales negatively with body size intra and inter-specifically (Emerson and Bramble, 1993). This pattern has been explained biomechanically: to keep constant the masticatory power when the body size increases, the transversal area of masticatory muscles needs to scale positively. A negative allometry of the braincase results in a larger space to accommodate this musculature in larger animals (Emerson and Bramble, 1993). In temnospondyls, this represents a larger adductor chamber (sensu Witzmann and

Schoch, 2013). Regarding the ontogenetic elongation of the snout, it is consistent with what has been documented in different mammalian clades (Cardini and Polly, 2013); therefore, this pattern might be plesiomorphic for tetrapods.

In spite of some adaptive explanations driven by external selective pressures

(sensu Schwenk and Wagner 2004) may be proposed for the ontogenetic patterns recovered, such as the need to maintain a functional feeding musculature, the fact that these patterns were conserved over millions of years and in species with radically different life-styles and from phylogenetically distant temnospondyl subclades (e.g., filter-feeding branchiosaurid Apateon pedestris and top predator capitosaur

Mastodonsaurus) suggests a complementary explanation: the presence of developmental constraints inherited from the earliest temnospondyls. Such constraints often result from internal selection pressures that derive from the internal dynamics of a functioning organism and lead to a stabilizing selection, and not from external (i.e., environmentally related) forces persisting over millions of years (Schwenk and

Wagner, 2004). Other ontogenetic transformations are variable, even in closely related and morphologically very similar species, such as tabulars becoming wider in

Glanochthon angusta vs. the narrowing of the same bones in G. latirostris.

Apparently, these transformations are not associated to life-style and, therefore, they might not represent an adaptive advantage.

The qualitative comparisons of ontogenetic allometries, which show that some ontogenetic patterns are extensively conserved and some others vary independently from phylogeny and life-styles, is also observed in the allometric space given that the ontogenetic trajectories do not group clearly for clade or life-style.

At the macroevolutionary level, shape diversification related to size seems to have played a key role in the morphological evolution in temnospondyls because shape changes over the major axis of variation in the morphospace (i.e., PC1) are very similar to the ones explained by the major axis of variation related to size change among species (i.e., the evolutionary allometric vector). In particular, the allometric vector explains more than 10% of the shape variance in the clade.

Evolutionary allometries can be explained by two hypotheses (which form extreme cases of a continuum): one related to the functional adaptation between traits and the other based on developmental constraints on the evolution of the traits (Voje et al., 2013). Two results of the present study support the hypothesis of developmental constraints: 1) cranial shape change over the evolutionary allometric vector is similar to the conserved ontogenetic allometric pattern and 2) the adult shape of the skull roof is consistent with phylogeny rather than life-style.

In this scenario, developmental constraints canalized the evolution of adult cranial shape along pathways patterned by ontogenetic shape change. Diversification of size and shape might have been achieved by heterochrony: changes in the length of the ancestral ontogenetic pathway resulted in evolutionary changes in size and shape, which are coupled by ontogenetic allometry.

Gerrothorax, a non-metamorphosing and bottom-dwelling form (Schoch and

Witzmann, 2012), seems to have somehow “escaped” from the developmental constraints mentioned above considering that it was the only species in our sample that does not follow the general pattern of ontogenetic change; this, in turn, explains its outlier position in both the allometric space and adult morphospace. As discussed for temnospondyls in general, the ontogeny of Gerrothorax may be a guide in understanding intraspecific morphological evolution. The ontogeny of Gerrothorax has been described as remarkably stable, with the youngest known specimens closely resembling the adults (Schoch and Witzmann, 2012). This ontogenetic stability is consistent with a remarkable evolutionary stability, as Gerrothorax exemplifies evolutionary stasis over a time span of almost 35 Myr (Schoch and Witzmann, 2012).

In conclusion, developmental constraints led to stereotyped ontogenetic shape changes in temnospondyls, with notable exceptions such as Gerrothorax. These conserved developmental pathways, in turn, might have acted as a line of least resistance for the evolution of cranial shape and might be the reason for the relatively low cranial disparity of the clade.

Acknowledgements

The authors thank U. Göhlich (NHMW), H. Hagdorn (MHI), H. Lutz

(NHMM), M. A. Norell (AMNH), K. Padian (UCMP), S. E. Pierce (MCZ), O. W. M.

Rauhut (BSM), D. Vasilyan (GPIT), and F. Witzmann (MB) for specimen access. C. P.-B. also thanks J. Fotuny, G. Cassini, and M. Ramírez for fruitful comments on the doctoral thesis on which this work is based. This work was funded by doctoral fellowships from CONICET, DAAD together with the Ministry of Education of

Argentina, and the Konrad Lorenz Institute awarded to C.P.-B.

Literature Cited

Adams, D. C. and A. Nistri. 2010. Ontogenetic convergence and evolution of foot

morphology in European cave salamanders (Family: Plethodontidae). BMC

Evolutionary Biology 10:216.

Adams, D. C. and E. Otarola–Castillo. 2013. geomorph: an R package for the

collection and analysis of geometric morphometric forma data. Methods in

Ecology and Evolution 4:393–399.

Angielczyk, K. D. and M. Ruta. 2012. The roots of amphibian morphospace: a

geometric morphometric analysis of Paleozoic temnospondyls. Fieldiana Life

and Earth Sciences 5:40–58.

Boy, J. A. and H.–D. Sues. 2000. Branchiosaurs: larvae, metamorphosis and

heterochrony in temnospondyls and seymouriamorphs. Pp. 1150–1197 in H.

Heatwole y R. L. Carroll (eds.). Amphibian Biology vol. 4: Palaeontology.

Surrey Beatty, Chipping Norton, Australia.

Cardini, A. and P. D. Polly. 2013. Larger mammals have longer faces because of

size–related constraints on skull form. Nature Communications 4:2452. Davidson, E. H. 2006. The Regulatory Genome: Gene Regulatory Networks In

Development And Evolution. Academic Press, London.

Emerson, S. B. and D. M. Bramble. 1993. Scaling, allometry, and skull design. Pp.

384–421 in Hanken, J. y B. K. Hall (eds.). The skull, Volume 3. University of

Chicago Press, Chicago, USA.

Garland, T. Jr., A. F. Bennett, and E. L. Rezende. 2005. Phylogenetic approaches in

comparative physiology. Journal of Experimental Biology 208:3015–3035.

Garland, T. Jr., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of

comparative data using phylogenetically independent contrasts.

SystematicBiology 41:18–32.

Gerber, S. 2014. Not all roads can be taken: development induces anisotropic

accessibility in morphospace. Evolution and Development 16:373–381.

Gerber, S. and M. J. Hopkins. 2011. Mosaic heterochrony and evolutionary

modularity: the trilobite genus Zacanthopsis as a case study. Evolution 65:

3241–3252.

Gould, S. J. and R. C. Lewontin. 1979. The spandrels of San Marco and the

Panglossial paradigm: a critique of the adaptationist programme. Proceedings of

the Royal Society of London 205:581–598.

Hall, B. K. 2000. Guest editorial: evo–devo or devo–evo – does it matter?

Evolutionary Development 2:177–178.

Kimmel, C. B., B. Sidlauskas, and J. A. Clack. 2009. Linked morphological changes

during palate evolution in early tetrapods. Journal of Anatomy 215:91–109. Maddin, H. C., F. A. Jenkins Jr. y J. S. Anderson. 2012. The braincase of Eocaecilia

micropodia (Lissamphibia, Gymnophiona) and the origin of caecilians. PLoS

One 7: e50743.

Mitteroecker, P., P. Gunz, S. Windhager and K. Schaefer. 2013. A brief review of

forma, form, and allometry in geometric morphometrics, with applications to

human facial morphology. Hystrix, the Italian Journal of Mammology 24:59–

66.

Pérez-Ben, C. M., R. R. Schoch, and A. M. Báez. 2018. Miniaturization and

morphological evolution in Paleozoic relatives of living amphibians: a

quantitative approach. Paleobiology 44:58–75.

Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables:

geometric interpretations. Evolution 55:2143–2160.

Rohlf, F. J. 2006. TPSDIG 2.1. Department of Ecology and Evolution, State

University of New York at Stony Brook, Stony Brook, Nueva York.

Schoch, R. R. 2009. Evolution of life cycles in early amphibians. Annual Review of

Earth and Planetary Sciences 37:135–162.

Schoch, R. R. 2013. The evolution of major temnospondyl clades: an inclusive

phylogenetic analysis. Journal of Systematic Palaeontology 11:673–705.

Schoch, R. R. 2014a. Amphibian evolution: the life of early land vertebrates. John

Wiley, Nueva York, USA.

Schoch, R. R. 2014b. Life cycles, plasticity and palaeoecology in temnospondyl

amphibians. Palaeontology 57:517–529. Schoch, R. R. and A. R. Milner. 2014. Handbook of Paleoherpetology–

Temnospondyli I. Dr. Friedrich Pfeil, Munich, Germnay.

Schoch, R. R. and F. Witzmann. 2009a. The temnospondyl Glanochthon from the

Permian Meisenheim Formation of Germany. Special Papers in Palaeontology

81:121–136.

Schoch, R. R. and F. Witzmann. 2012. Cranial morphology of the plagiosaurid

Gerrothorax pulcherrimus as an extreme example of evolutionary stasis.

Lethaia 45:371–385.

Schwenk, K. and G. P. Wagner. 2004. The relativism of constraints on phenotypic

evolution; pp. 390 – 408 in: M. Pigliucci and K. Preston (eds). Phenotypic

integration. Studying the ecology and Evolution of Complex Phenotypes.

Stayton, C. T. and M. Ruta. 2006. Geometric morphometrics of the skull rook of

stereospondyls (Amphibia: Temnospondyli). Palaeontology 49:307–337.

Steyer, J. S. 2003. A revision of the Early Triassic “Capitosaurs” (Stegocephali,

Stereospondyli) from Madagascar, with remarks on their comparative ontogeny.

Journal of Vertebrate Paleontology 23:544–555.

Strelin, M. M., S. M. Benitez–Vieyra, J. Fornoni, C. P. Klingenberg and A. A.

Cocucci. 2017. The evolution of floral ontogenetic allometry in the Andean

genus Caiophora (Loasaceae, subfam. Loasoideae). Evolution and

Development: advance online, DOI: 10.1111/ede.12246.

Voje, K., T. F. Hansen, C. K. Egset, G. H. Bolstad and C. Pelabon. 2013. Allometric

constraints and the evolution of allometry. Evolution 68:866–885. Wagner, G. P. and L. Altenberg. 1996. Perspective: complex adaptations and the

evolution of evolvability. Evolution 50:967–976.

Wilson, L. A. B. 2013. Allometric disparity in rodent evolution. Ecology and

Evolution 3:971–984.

Witzmann, F. and H–U Pfretzschner. 2003. Larval ontogeny of Micromelerpeton

credneri (Temnospondyli, Dissorophoidea). Journal of Vertebrate Paleontology

23:750–768.

Witzmann, F. and R. R. Schoch. 2013. Reconstruction of cranial and hyobranchial

muscles in the Triassic temnospondyl Gerrothorax provides evidence for

akinetic suction feeding. Journal of morphology 274: 525–542.

Witzmann, F. and H. Scholz. 2007. Morphometric study of allometric skull growth in

the temnospondyl Archegosaurus decheni from the Permian/Carboniferous of

Germany. Geobios 40:641–554.

Witzmann, F., H. Scholz, and M. Ruta. 2009. Morphospace occupation of

temnospondyl growth series: a geometric morphometric approach. Alcheringa

33:237–255.

Yeh, J. 2002. The effect of miniaturized body size on skeletal morphology in

frogs.Evolution 56:628–641.

Zeldtich, M. L., Z. T. Calamari, and D. L. Swiderski. 2016. Disparate postnatal

ontogenies do not add to the forma disparity of infants. Evolutionay Biology

43:188–207. Figure captions

FIGURE 1. Phylogenetic hypothesis used in the present study. FIGURE 2. Landmarks of the skull roof used in the geometric morphometric analyses (image modified from Schoch and Milner, 2014). FIGURE 3. Visualization of the ontogenetic allometry of the skull roof of selected species estimated by regressions of Procrustes shape coordinates on ln CS. The grids show the deformation between the consensus configuration of each species and the shapes corresponding to different multiples of standard deviation of ln CS. A-B, Acanthostomatops vorax (terrestrial); C-D, Apateon caducus (neotenic aquatic); E-F, Sclerocephalus haeuseri (non-neotenic aquatic); G-H, Gerrothorax pulcherrimus (non-neotenic aquatic). FIGURE 4. A-B, allometric space constructed by a principal component analyses on the ontogenetic allometric vectors standardized (A, PC1 and PC2; B, PC1 and PC3); C, cluster analysis of the same vectors. Life-styles are indicated by colors and symbols indicate the clade to which the species belong. FIGURE 5. A-B, morphospace constructed by a principal component analyses on the Procrustes shape coordinates of adult specimens (A, PC1 and PC2; B, PC1 and PC3); C-D, grids showing the deformation between the consensus configuration and (C) the maximum and (D) minimum values of PC1; F-G, Visualization of the evolutionary allometry of the skull roof estimated by regressions of Procrustes shape coordinates on ln CS. The grids show the deformation between the consensus configuration and the shapes corresponding to different multiples of standard deviation of ln CS.