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This indicates that the recovered overall disparity pattern is dominated by the observations and relationships of the extant species, whereas the fossils seem to have a stronger influence on the uncertainty of the disparity estimates, which is augmented by the uncertainty in the topology. In all cases, the curves are much smoother than the original graph produced by Foth and Joyce [ 6 ], as should be expected from the use of interpolated ancestors.

As in the original analyses, the cranial disparity of pan-cryptodires exceeds that of pan-pleurodires over most of the time figure 1 b , solid lines. Pan-cryptodires show a steady increase in cranial disparity throughout the Cretaceous until achieving their maximum around the border of the Early and Late Cretaceous.

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Although a number of ups and downs are apparent throughout the Cenozoic, pan-cryptodires overall show a moderate decline until the Oligocene, before their disparity increase towards the Recent, again. Pan-pleurodires also show a steady increase throughout the Cretaceous and reach their first maximum during the Late Cretaceous. The cranial disparity of the group declines during the Eocene, but recovers in the Recent time bin, surpassing the level of the Maastrichtian. The cranial disparity of pan-pleurodires surpasses that of pan-cryptodires since the Late Cretaceous see electronic supplementary material S1, Table S1.

Like in the previous study, the relationship between skull shape disparity and climate is rather weak. In addition, a specific comparison between changes in temperature and cranial disparity across successive time bins found no relationship, too. Although our new analysis broadly recovers results similar to those of our initial analysis, some notable differences are apparent that confirm that a fuller use of phylogenetic data has a broad impact on disparity analyses.

As in our initial study, turtles show a slow but steady increase in cranial disparity throughout the Mesozoic, which opposes the near explosive achievement of high disparity levels in other groups of animals [ 28 , 29 ]. Such delayed peak of disparity was interpreted to indicate a concordance between morphological and taxonomic diversification which shows an exponential-like shape through time, figure 1 g , and thus implies neither constraints on morphological evolution nor trends in morphological step size during the prolonged period of increase [ 30 ].

In contrast to our initial analysis, however, our revised analysis reveals that turtles maintained a high level of disparity in skull shape throughout the Cenozoic, instead of showing a strong decline towards the Miocene, followed by a recovery towards the Recent.

This result confirms our previous suspicion that our initial Cenozoic curve was negatively affected by poor sampling and that this sampling bias might be overcome by including ghost lineages. We initially hypothesized that the decrease of cranial disparity throughout the Cenozoic may have been caused by the loss of morphospace that occurred through the extinction of more basal groups e. Based on the simulations undertaken by Foote [ 31 ], the overall course of the disparity curve indicates that during the Mesozoic the morphological step size was relatively high, but constant with no temporal changes see above.

In contrast, the more or less constant level of cranial disparity during the Cenozoic indicates that the number of morphological steps was significantly reduced compared with the Mesozoic. As this pattern is also evident for the two subclades, it is evident that pan-cryptodires and pan-pleurodires underwent similar evolutionary patterns. As we thought a climatological control of disparity to be biologically implausible, we hypothesized following our initial analysis [ 6 ] that cranial disparity may be correlated with biogeography.

In particular, as most turtle groups populate different parts of the available morphospace [ 32 ], the increasing fragmentation of Pangaea over the course of the late Mesozoic may had led to the formation of increasing amounts of endemism. This trend was only reversed during the Cenozoic when the extinction of basally branching turtle groups, perhaps caused by the global spread of cryptodires made possible by emerging continental bridges, offset gains in cranial disparity [ 7 , 8 ].

This hypothesis can now be supported by a correlation between cranial disparity and number of major landmasses through time, although we lack an understanding of the underlying biological processes. Interestingly, the revised analysis still shows an overall poor correlation with temperature, thereby indicating once again that climate does not appear to directly control the disparity of turtle skulls. However, this does not necessarily mean that the general morphological diversity of turtles was completely unaffected by global temperature, especially as their geographical dispersal seems to show such a correlation [ 33 ].

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Thus, to fully embrace how turtle anatomy may be affected by climate change over time, further studies are necessary focusing on different body parts, including the shell and limbs. Although the use of ancestral lineages resulted in disparity curves that are much more gradual than ones we initially retrieved, some notable steps still remain, particularly in the curves of the two primary clades of extant turtles. Here, the skull shape disparity of pan-pleurodires seems to suffer a loss during the Palaeogene, probably due to the loss of marine-adapted lineages at that time e.

Interestingly, although pleurodires represent only about a quarter of all extant turtles [ 34 ], their sum of variance, a disparity measure that takes diversity into account, is greater than that of cryptodires for the whole Cenozoic.

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We noted following our initial analysis [ 6 ] that the outcome strongly depends on phylogenetic relationships, the algorithm of time-scaling [ 35 ] and, potentially, the method of ancestral reconstruction [ 36 , 37 ]. This is even more true for the current analysis, where we measured disparity exclusively from phylogenetically interpolated shape variables. Consequently, the new curves are characterized by much smoother trajectories than the previous one figure 1 a. Furthermore, the resolution of the polytomies in the supertree has a significant effect on the sum of variances measured from interpolated traits figure 1.

Despite these uncertainties, we are confident regarding the robustness of our results for the following reasons. This and the previous analysis found disparity curves showing overall similar trends that are apparently independent from the particular topology use see Material and methods , the ages of fossils, the use of branch interpolations or the addressing of topological uncertainty.

The only major difference is the presence of a Cenozoic plateau in the present analysis. This confirms that the Miocene dip found in the original analysis indeed is a sampling artefact that can be addressed through the usage of branch interpolations. We nevertheless see room for improvement, especially in regard to sampling. This is not a trivial concern, considering the often-bizarre morphology of numerous fossil turtle skulls not included in our study because of poor preservation e. While this sampling bias is inherent to any study of morphological or taxonomic diversity, we here identify another bias that may be overcome partially using phylogenetic data.

As implemented herein, phylogenetic data allow sampling time bins not represented by fossil by including ghost lineages. However, we note that many time bins still remain unsampled, because the fossil sampled is not necessarily the last representative of its lineage. For example, we compensate for the absence of adocids in the majority of Cretaceous time bins, as the sole representative of the group in our sample, Adocus lineatus , only samples the latest Cretaceous time bin Maastrichtian.

However, the adocid lineage actually persists into the Eocene of Asia [ 39 ] and the unusual morphology of this lineage is therefore not accounted for in the Palaeogene time bins. In summary, the interpolation of traits along branches is a useful method to minimize the effect of artefacts related to sampling gaps in the fossil record. Following Wilberg [ 9 ], it should be noted that reconstructed ancestors and interpolated traits are not meant to represent true ancestral shapes, but placeholders in the absence of sampled specimens.

Indeed, the extensive use of phylogenetic interpolation implies that the results can be highly sensitive to the method of ancestral trait reconstruction. Regardless, in our appreciation, the use of such estimated morphologies for a given time bin is better than treating an absence of sampled data as actual absence of shape. Along those lines, the Miocene dip in the cranial disparity curves of turtles we retrieved in our original study [ 6 ] turns out to be a gap in the fossil record rather than a natural event.

As a consequence, the new analysis is still compatible with our original hypothesis that the cranial disparity of turtles could be driven by biogeographic factors, while climate played only a secondary role. We thank Anieli Pereira for freely sharing her data with us. This manuscript was improved considerably by thoughtful comments provided by three anonymous reviewers. All authors gave final approval for publication.

National Center for Biotechnology Information , U. R Soc Open Sci.

Swati Rajoria

Published online Nov Author information Article notes Copyright and License information Disclaimer. Electronic supplementary material is available online at https: Received Jul 13; Accepted Oct Abstract In a previous study, we estimated the cranial disparity of turtles Testudinata through time using geometric morphometric data from both terminal taxa and hypothetical ancestors to compensate for temporal gaps in the fossil record. Introduction Over the course of the last decades, the combination of geometric morphometrics with phylogenetic comparative methods has become a promising resource for the study of macroevolutionary dynamics, including the evolution of disparity, which quantifies morphological diversity as opposed to taxonomic, functional or phylogenetic diversity [ 1 — 5 ].

Open in a separate window. Material and methods The materials and methods in general follow Foth and Joyce [ 6 ] see electronic supplementary material, S1—S4 of [ 6 ] with the exception of the following modifications. Discussion and conclusion 4. Comparisons with previous analysis Although our new analysis broadly recovers results similar to those of our initial analysis, some notable differences are apparent that confirm that a fuller use of phylogenetic data has a broad impact on disparity analyses.

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Limitation of results We noted following our initial analysis [ 6 ] that the outcome strongly depends on phylogenetic relationships, the algorithm of time-scaling [ 35 ] and, potentially, the method of ancestral reconstruction [ 36 , 37 ]. Click here to view. Acknowledgements We thank Anieli Pereira for freely sharing her data with us. Data accessibility Additional results supporting this article have been uploaded as part of the electronic supplementary material.

Competing interests The authors declare no competing interests. Villier L, Eble GJ.



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Insights from the cranial morphometrics and evolutionary history of Pterosauria Diapsida: Unappreciated diversification of stem archosaurs during the Middle Triassic predated the dominance of dinosaurs. Foth C, Joyce WG. B , doi: Multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. A toothed turtle from the Late Jurassic of China and the global biogeographic history of turtles.

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