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The ecological origins of snakes as revealed by skull evolution.

ABSTRACT: The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial. Here we use a geometric morphometric approach integrating ecological, phylogenetic, paleontological, and developmental data for building models of skull shape and size evolution and developmental rate changes in squamates. Our large-scale data reveal that whereas the most recent common ancestor of crown snakes had a small skull with a shape undeniably adapted for fossoriality, all snakes plus their sister group derive from a surface-terrestrial form with non-fossorial behavior, thus redirecting the debate toward an underexplored evolutionary scenario. Our comprehensive heterochrony analyses further indicate that snakes later evolved novel craniofacial specializations through global acceleration of skull development. These results highlight the importance of the interplay between natural selection and developmental processes in snake origin and diversification, leading first to invasion of a new habitat and then to subsequent ecological radiations.

SUBMITTER: Da Silva FO

PROVIDER: S-EPMC5785544 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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The ecological origins of snakes as revealed by skull evolution.

Da Silva Filipe O FO Fabre Anne-Claire AC Savriama Yoland Y Ollonen Joni J Mahlow Kristin K Herrel Anthony A Müller Johannes J Di-Poï Nicolas N

Nature communications 20180125 1

The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial. Here we use a geometric morphometric approach integrating ecological, phylogenetic, paleontological, and developmental data for building models of skull shape and size evolution and developmental rate changes in squamates. Our large-scale data reveal that whereas the most recent common ancestor of crown snakes had a small skull with a sha ...[more]

PMID: 29371624

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Project description:BackgroundFossil evidence suggests that extant North American lizard genera (north of Mexico) evolved during the Miocene. Although fossils of the clade Phrynosomatidae (spiny lizards and sand lizards) have been reported, there have been no previously described fossils of the fringe-toed sand lizards (Uma). In the extant biota, Uma inhabit arid deserts, and members of the western clade of Uma are restricted to sand dunes or other habitats containing fine-grained sand.ResultsI describe the first known fossil of Uma and refer the fossil to the total clade of Uma with an apomorphy-based diagnosis. The fossil is a partial premaxilla that was found in the Miocene strata of the Dove Spring Formation of southern California, dating to 8.77 Ma. The paleoenvironment of the Dove Spring Formation was semiarid and contained ephemeral streams that facilitated deposition, and there is no evidence of sand dune deposits in the strata containing the locality from which the Uma fossil was found. Divergence time analyses of a concatenated molecular dataset with four fossil calibrations support a Neogene origin of the total clade of Uma and of the crown clade of Uma. Those analyses also estimated a Neogene divergence between Uma scoparia and the Uma notata complex. Multispecies coalescent analyses with one fossil calibration inferred a Paleogene origin for the total clade of Uma and a Pliocene or Pleistocene divergence between Uma scoparia and the Uma notata complex. The fossil and the total and crown clades of Uma precede the evolution of modern desert ecosystems in the southwestern United States and northern Mexico by millions of years.ConclusionsThe total clade and the crown clade of Uma were not restricted to arid deserts throughout their evolutionary histories. I demonstrate that an apomorphy-based diagnosis can be used to identify fossils of isolated skeletal elements for at least one clade of phrynosomatid lizard, and suggest exercising caution when using environmental tolerances of extant taxa to hypothesize paleoecological reconstructions.

Project description:Uropeltids form a diverse clade of highly derived, fossorial snakes that, because of their phylogenetic position among other alethinophidian lineages, may play a key role in understanding the early evolution of cranial morphology in snakes. We include detailed osteological descriptions of crania and mandibles for eight uropeltid species from three nominal genera (Uropeltis, Rhinophis, and Brachyophidium) and emphasize disarticulated elements and the impact of intraspecific variation on previously proposed morphological characters used for phylogenetic analysis. Preliminary analysis of phylogenetic relationships strongly supports a clade composed exclusively of species of Plectrurus, Uropeltis, and Rhinophis. However, monophyly of each of those genera and Melanophidium is not upheld. There is moderate support that Sri Lankan species (e.g., Rhinophis and Uropeltis melanogaster) are monophyletic with respect to Indian uropeltids. Previously proposed characters that are phylogenetically informative include the shape of the nasals, length of the occipital condyle, level of development of the posteroventral process of the dentary, and participation of the parietal in the optic foramen. Additionally, thirty new features that may be systematically informative are identified and described, but were not verified for their utility. Such verification must await availability of additional disarticulated cranial material from a larger sample of taxa. All characters require further testing through increased focus on sources and patterns of intraspecific variation, inclusion of broader taxonomic samples in comparative studies, and exploration of skeletal development, sexual dimorphism, and biogeographic patterns. Additionally, trends in the relative enlargement of the sensory capsules, reduction in cranial ossification and dentition, fusion of elements, and the appearance of novel morphological conditions, such as the structure and location of the suspensorium, may be related to fossoriality and miniaturization in some uropeltid taxa, and may complicate analysis of relationships within Uropeltidae and among alethinophidian snakes.

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The ecological origins of snakes as revealed by skull evolution.

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The ecological origins of snakes as revealed by skull evolution.

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