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Slow and steady: the evolution of cranial disparity in fossil and recent turtles.

ABSTRACT: Turtles (Testudinata) are a diverse group of amniotes that have a rich fossil record that extends back to the Late Triassic, but little is known about global patterns of disparity through time. We here investigate the cranial disparity of 172 representatives of the turtle lineage and their ancestors grouped into 20 time bins ranging from the Late Triassic until the Recent using two-dimensional geometric morphometrics. Three evolutionary phases are apparent in all three anatomical views investigated. In the first phase, disparity increases gradually from the Late Triassic to the Palaeogene with only a minor perturbation at the K/T extinct event. Although global warming may have influenced this increase, we find the Mesozoic fragmentation of Pangaea to be a more plausible factor. Following its maximum, disparity decreases strongly towards the Miocene, only to recover partially towards the Recent. The marked collapse in disparity is likely a result of habitat destruction caused by global drying, combined with the homogenization of global turtle faunas that resulted from increased transcontinental dispersal in the Tertiary. The disparity minimum in the Miocene is likely an artefact of poor sampling.

SUBMITTER: Foth C

PROVIDER: S-EPMC5136591 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Slow and steady: the evolution of cranial disparity in fossil and recent turtles.

Foth Christian C Joyce Walter G WG

Proceedings. Biological sciences 20161101 1843

Turtles (Testudinata) are a diverse group of amniotes that have a rich fossil record that extends back to the Late Triassic, but little is known about global patterns of disparity through time. We here investigate the cranial disparity of 172 representatives of the turtle lineage and their ancestors grouped into 20 time bins ranging from the Late Triassic until the Recent using two-dimensional geometric morphometrics. Three evolutionary phases are apparent in all three anatomical views investiga ...[more]

PMID: 27903875

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Project description:BackgroundThe Notostraca is a small but ancient crustacean order with a contrasting combination of a conservative morphology and a wide range of reproductive modes. The tadpole shrimp Triops cancriformis, includes bisexual - the putatively ancestral state -, androdioecious and hermaphrodite populations. As hermaphroditism and androdioecy confer a colonisation advantage, we expect the postglacial colonisation of northern Europe to have been effected by lineages with such reproductive modes. Therefore, N European populations should be composed of closely related lineages reflecting a recent range expansion. In contrast, glacial refugia in the south should contain bisexual populations with high haplotype diversity and more population structuring. To test these hypotheses, we analysed the geographic distribution of reproductive modes based on new and published sex ratio data. In addition, we investigated the European phylogeography of T. cancriformis by sequencing over a 1000 bp of mitochondrial DNA (mtDNA) in individuals from a large sample of populations of the three recognised subspecies.ResultsBisexual populations were only found in the Iberian Peninsula, with the rest of European populations showing low male proportions or no males. Androdioecious populations were found in Central and Eastern Europe. Regarding mtDNA diversity, Spanish and Moroccan populations of T. c. mauritanicus were highly divergent, and showed strong population structure. In contrast, Triops c. cancriformis and T. c. simplex formed a single mtDNA lineage with low haplotype diversity. This diversity was structured into two phylogenetic clades (A, B), coexisting in E Germany. Basal haplotypes of both lineages were found in the Iberian Peninsula. Most of the populations in clade A and B are either hermaphroditic or androdioecious, with the only bisexual population in these clades found in the Iberian Peninsula. The genetic divergence between these two clades suggests a split in the Late Pleistocene and their geographic distribution reflects a complex evolutionary history of European Triops populations, with possibly two episodes of range expansions - one of them by clade A - involving androdioecious and hermaphroditic populations.ConclusionAs we predicted, N European populations of T. cancriformis are closely related, with few widely distributed haplotypes and indications of a recent range expansion involving hermaphroditic/androdioecious lineages. A possible second range expansion or long distance colonisation may have created the secondary contact zone between T. c. cancriformis/simplex clades A and B. The large haplotype diversity and strong genetic subdivision in the Iberian Peninsula, which is known to contain only bisexual populations, strongly suggest that this area was a Pleistocene refugium for T. cancriformis, although the occurrence of additional eastern refugia cannot be ruled out. Our data support the status of T. c. mauritanicus as a separate species and the colonisation of N Africa from the Iberian Peninsula. We suggest that hermaphroditism/androdioecy has evolved recently in T. cancriformis and has facilitated the postglacial colonisation of northern Europe.

Project description:Turtles are a successful clade of reptiles that originated in the Late Triassic. The group adapted during its evolution to different types of environments, ranging from dry land to ponds, rivers, and the open ocean, and survived all Mesozoic and Cenozoic extinction events. The body of turtles is characterized by a shell, which has been hypothesized to have several biological roles, like protection, thermal and pH regulation, but also to be adapted in its shape to the ecology of the animal. However, only few studies have investigated the relationships between shell shape and ecology in a global context or clarified if shape can be used to diagnose habitat preferences in fossil representatives. Here, we assembled a three-dimensional dataset of 69 extant turtles and three fossils, in particular, the Late Triassic Proganochelys quenstedtii and Proterochersis robusta and the Late Jurassic Plesiochelys bigleri to test explicitly for a relationship between shell shape and ecology. 3D models were obtained using surface scanning and photogrammetry. The general shape of the shells was captured using geometric morphometrics. The habitat ecology of extant turtles was classified using the webbing of their forelimbs as a proxy. Principal component analysis (PCA) highlights much overlap between habitat groups. Discriminant analyses suggests significant differences between extant terrestrial turtles, extant fully aquatic (i.e., marine and riverine) turtles, and an unspecialized assemblage that includes extant turtles from all habitats, mostly freshwater aquatic forms. The paleoecology of the three fossil species cannot be determined with confidence, as all three fall within the unspecialized category, even if Plesiochelys bigleri plots closer to fully aquatic turtles, while the two Triassic species group closer to extant terrestrial forms. Although the shape of the shell of turtles indeed contains an ecological signal, it is overall too weak to uncover using shell shape in paleoecological studies, at least with the methods we selected.

Dataset Information

Slow and steady: the evolution of cranial disparity in fossil and recent turtles.

Publications

Slow and steady: the evolution of cranial disparity in fossil and recent turtles.

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