skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.

Title: Insights into skull evolution in fossorial snakes, as revealed by the cranial morphology of Atractaspis irregularis (Serpentes: Colubroidea)

Comparative osteological analyses of extant organisms provide key insight into major evolutionary transitions and phylogenetic hypotheses. This is especially true for snakes, given their unique morphology relative to other squamates and the persistent controversy regarding their evolutionary origins. However, the osteology of several major snake groups remains undescribed, thus hindering efforts to accurately reconstruct the phylogeny of snakes. One such group is the Atractaspididae, a family of fossorial colubroids. We herein present the first detailed description of the atractaspidid skull, based on fully segmented micro‐computed tomography (micro‐CT) scans ofAtractaspis irregularis. The skull ofAtractaspispresents a highly unique morphology influenced by both fossoriality and paedomorphosis. This paedomorphosis is especially evident in the jaws, palate, and suspensorium, the major elements associated with macrostomy (large‐gaped feeding in snakes). Comparison to scolecophidians—a group of blind, fossorial, miniaturized snakes—in turn sheds light on current hypotheses of snake phylogeny. Features of both the naso‐frontal joint and the morphofunctional system related to macrostomy refute the traditional notion that scolecophidians are fundamentally different from alethinophidians (all other extant snakes). Instead, these features support the controversial hypothesis of scolecophidians as regressed alethinophidians, in contrast to their traditional placement as the earliest‐diverging snake lineage. We propose thatAtractaspisand scolecophidians fall along a morphological continuum, characterized by differing degrees of paedomorphosis. Altogether, a combination of heterochrony and miniaturization provides a mechanism for the derivation of the scolecophidian skull from an ancestral fossorial alethinophidian morphotype, exemplified by the nonminiaturized and less extreme paedomorphAtractaspis.

more » « less
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Journal of Anatomy
Page Range / eLocation ID:
p. 146-172
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We compared the head skeleton (skull and lower jaw) of juvenile and adult specimens of five snake species [Anilios(=Ramphotyphlops)bicolor,Cylindrophis ruffus,Aspidites melanocephalus,Acrochordus arafurae, andNotechis scutatus] and two lizard outgroups (Ctenophorus decresii,Varanus gilleni). All major ontogenetic changes observed were documented both qualitatively and quantitatively. Qualitative comparisons were based on high‐resolution micro‐CTscanning of the specimens, and detailed quantitative analyses were performed using three‐dimensional geometric morphometrics. Two sets of landmarks were used, one for accurate representation of the intraspecific transformations of each skull and jaw configuration, and the other for comparison between taxa. Our results document the ontogenetic elaboration of crests and processes for muscle attachment (especially for cervical and adductor muscles); negative allometry in the braincase of all taxa; approximately isometric growth of the snout of all taxa exceptVaranusandAnilios(positively allometric); and positive allometry in the quadrates of the macrostomatan snakesAspidites,AcrochordusandNotechis, but also, surprisingly, in the iguanian lizardCtenophorus. Ontogenetic trajectories from principal component analysis provide evidence for paedomorphosis inAniliosand peramorphosis inAcrochordus. Some primitive (lizard‐like) features are described for the first time in the juvenileCylindrophis. Two distinct developmental trajectories for the achievement of the macrostomatan (large‐gaped) condition in adult snakes are documented, driven either by positive allometry of supratemporal and quadrate (in pythons), or of quadrate alone (in sampled caenophidians); this is consistent with hypothesised homoplasy in this adaptive complex. Certain traits (e.g. shape of coronoid process, marginal tooth counts) are more stable throughout postnatal ontogeny than others (e.g. basisphenoid keel), with implications for their reliability as phylogenetic characters.

    more » « less
  2. Abstract Scolecophidian snakes have long posed challenges for scholars interested in elucidating their anatomy. The importance, and relative paucity, of high‐quality anatomical data pertaining to scolecophidians was brought into sharp focus in the late 20 th century as part of a controversy over the phylogeny and ecological origin of snakes. The basal position of scolecophidians in the phylogeny of snakes makes their anatomy, behavior, ecology, and evolution especially important for such considerations. The depauperate fossil record for the group meant that advances in understanding their evolutionary history were necessarily tied to biogeographic distributions and anatomical interpretations of extant taxa. Osteological data, especially data pertaining to the skull and mandible, assumed a dominant role in shaping historical and modern perspectives of the evolution of scolecophidians. Traditional approaches to the exploration of the anatomy of these snakes relied heavily upon serial‐sectioned specimens and cleared‐and‐stained specimens. The application of X‐ray computed tomography (CT) to the study of scolecophidians revolutionized our understanding of the osteology of the group, and now, via diffusible iodine‐based contrast‐enhanced computed tomography (diceCT), is yielding data sets on internal soft anatomical features as well. CT data sets replicate many aspects of traditional anatomical preparations, are readily shared with a global community of scholars, and now are available for unique holotype and other rare specimens. The increasing prevalence and relevance of CT data sets is a strong incentive for the establishment and maintenance of permanent repositories for digital data. 
    more » « less
  3. Abstract

    A snake‐like body plan and burrowing lifestyle characterize numerous vertebrate groups as a result of convergent evolution. One such group is the amphisbaenians, a clade of limbless, fossorial lizards that exhibit head‐first burrowing behavior. Correlated with this behavior, amphisbaenian skulls are more rigid and coossified than those of nonburrowing lizards. However, due to their lifestyle, there are many gaps in our understanding of amphisbaenian anatomy, including how their cranial osteology varies among individuals of the same species and what that reveals about constraints on the skull morphology of head‐first burrowing taxa. We investigated intraspecific variation in the cranial osteology of amphisbaenians using seven individuals of the trogonophidDiplometopon zarudnyi. Variation in both skull and individual skull element morphology was examined qualitatively and quantitatively through three‐dimensional (3D) models created from microcomputed tomography data. Qualitative examination revealed differences in the number and position of foramina, the interdigitation between the frontals and parietal, and the extent of coossification among the occipital complex, fused basioccipital and parabasisphenoid (“parabasisphenoid‐basioccipital complex”), and elements X. We performed 3D landmark‐based geometric morphometrics for the quantitative assessment, revealing shape differences in the skull, premaxilla, maxilla, frontal, and parietal. The observed intraspecific variation may be the result of different stages of ontogenetic development or biomechanical optimization for head‐first burrowing. For example, variation in the coossification of the occipital region suggests a potential ontogenetic coossification sequence. Examination of these areas of variation across other head‐first burrowing taxa will help determine if the variation is clade‐specific or part of a broader macroevolutionary pattern of head‐first burrowing.

    more » « less
  4. Abstract

    Amphisbaenians are a poorly understood clade of fossorial lizards. Because of their derived anatomy and relative scarcity, the systematics of the clade and its placement within squamates has long been controversial. Traditional approaches grouped species into four assemblages according to burrowing behavior and cranial morphology, resulting in the recognition of “shovel‐headed,” “round‐headed,” “keel‐headed,” and “spade‐headed” morphotypes. Recent phylogenetic analyses do not support the monophyly of the taxa that share those morphotypes. Detailed analyses of cranial osteology were previously accomplished using high‐resolution x‐ray computed tomography (HRXCT) for the “shovel‐headed”Rhineura hatcherii(Rhineruidae) and the “spade‐headed”Diplometopon zarudnyi(Trogonophidae). A detailed description of the “round‐headed”Amphisbaena albawas previously completed based upon traditional “dry” skeletal specimens. Seven species of the “round‐headed”Blanus(Blanidae) were also analyzed using HRXCT. The goal of that project was a comparative analysis of all extant species ofBlanusrather than a detailed, bone‐by‐bone description of one species, but certainly is useful for comparison with another “round‐headed” taxon. The “round‐headed” morphotype is by far the most common among amphisbaenians and is much in need of further documentation. We use HRXCT imagery to provide additional data about the disparity in cranial morphology among amphisbaenians. Those data allow us to provide another detailed description of a “round‐headed” amphisbaenian, the poorly known southern African speciesZygaspis quadrifrons. HRXCT is ideal for this relatively rare and diminutive species. We are able to visualize and describe a detailed reconstruction of the entire skull as well as individual cranial elements. Comparisons with other species that were described in similar detail—D.zarudnyi,Spathorhynchus fossorium,R.hatcherii, andA.alba—and to a lesser degree withBlanus, reveal a complex mosaic of morphological features of the skull inZygaspis. Preliminary data suggest that intraspecific variation is present withinZ.quadrifrons, and interspecific variation among other species ofZygaspismay be sufficient for species‐level recognition based on cranial osteology. Our description is, therefore, also intended to serve as a baseline for comparative analysis of other specimens ofZ.quadrifronsand of other species within the genus.

    more » « less
  5. Abstract

    Snakes—a subset of lizards—have traditionally been divided into two major groups based on feeding mechanics: “macrostomy,” involving the ingestion of proportionally large prey items; and “microstomy,” the lack of this ability. “Microstomy”—considered present in scolecophidian and early‐diverging alethinophidian snakes—is generally viewed as a symplesiomorphy shared with non‐snake lizards. However, this perspective of “microstomy” as plesiomorphic and morphologically homogenous fails to recognize the complexity of this condition and its evolution across “microstomatan” squamates. To challenge this problematic paradigm, we formalize a new framework for conceptualizing and testing the homology of overall character complexes, or “morphotypes,” which underlies our re‐assessment of “microstomy.” Using micro‐computed tomography (micro‐CT) scans, we analyze the morphology of the jaws and suspensorium across purported “microstomatan” squamates (scolecophidians, early‐diverging alethinophidians, and non‐snake lizards) and demonstrate that key components of the jaw complex are not homologous at the level of primary character state identity across these taxa. Therefore, rather than treating “microstomy” as a uniform condition, we instead propose that non‐snake lizards, early‐diverging alethinophidians, anomalepidids, leptotyphlopids, and typhlopoids each exhibit a unique and nonhomologous jaw morphotype: “minimal‐kinesis microstomy,” “snout‐shifting,” “axle‐brace maxillary raking,” “mandibular raking,” and “single‐axle maxillary raking,” respectively. The lack of synapomorphy among scolecophidians is inconsistent with the notion of scolecophidians representing an ancestral snake condition, and instead reflects a hypothesis of the independent evolution of fossoriality, miniaturization, and “microstomy” in each scolecophidian lineage. We ultimately emphasize that a rigorous approach to comparative anatomy is necessary in constructing evolutionary hypotheses that accurately reflect biological reality.

    more » « less