Skull Anatomy and Evolution in Scolecophidian Snakes (Squamata: Ophidia), with an Emphasis on the Role of Heterochrony

• Author / Creator

  Strong, Catherine R. C.

• Scolecophidians (‘blindsnakes’) form an assemblage of miniaturized and fossorial snakes, comprising three main lineages: Anomalepididae, Leptotyphlopidae, and Typhlopoidea. Scolecophidians have long been viewed as diverging basally among snakes, constituting the modern vestige of an ancestrally miniaturized, burrowing, vision-degenerate, and ‘microstomatan’ (small-mouthed) snake condition. However, despite their pivotal role in hypotheses of the anatomical, ecological, and phylogenetic origins of snakes, several aspects of scolecophidian anatomy and evolution remain poorly understood. In light of this uncertainty, my thesis re-examines the aforementioned paradigmatic view of this group. I focus particularly on the potential role of heterochrony (i.e., evolutionary changes in the rate and/or timing of developmental events)—and particularly paedomorphosis (i.e., juvenilization of morphology)—in influencing scolecophidian evolution.
  
  I first use the genus Atractaspis to assess the traditional hypothesis of a fundamental dichotomy between scolecophidians and alethinophidians (i.e., all other extant snakes). As a fossorial but non-miniaturized colubroid, deeply nested among snakes, Atractaspis presents an interesting basis for comparison to the miniaturized, fossorial, and assumedly ‘basal’ scolecophidians. This investigation of atractaspidid anatomy reveals a clear morphological continuum between scolecophidians and various fossorial alethinophidians, with miniaturization—and, concomitantly, extensive paedomorphosis—providing a reasonable mechanism linking these groups.
  
  I next examine the evolution of jaw mechanisms in squamates (i.e., lizards, including snakes). Snakes have traditionally been divided into two major groups based on feeding mechanics: ‘macrostomy’, the ability to ingest proportionally large prey items; and ‘microstomy’, the lack of this ability. ‘Microstomy’ is in turn generally viewed as a morphologically uniform condition shared by scolecophidians, early-diverging alethinophidians, and non-snake lizards. To investigate this paradigm, I formalize a new framework for conceptualizing and testing the homology of overall character complexes, or ‘morphotypes’. I analyze the morphology of the jaws and suspensorium across purported ‘microstomatan’ squamates, revealing 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 symplesiomorphy, I instead propose that non-snake lizards, early-diverging alethinophidians, anomalepidids, leptotyphlopids, and typhlopoids each exhibit a unique and non-homologous jaw morphotype: ‘minimal-kinesis microstomy’, ‘snout-shifting’, ‘axle-brace maxillary raking’, ‘mandibular raking’, and ‘single-axle maxillary raking’, respectively. I complement this qualitative approach with a quantitative assessment of squamate skull modularity. Anatomical network analysis of a broad range of squamates reveals that the jaw elements exhibit distinctive patterns of connectivity within each major ‘microstomatan’ group. These contrasting network structures in turn support the aforementioned hypothesis of a complex evolutionary history of ‘microstomy’. Morphospace-based analyses indicate convergence associated with both fossoriality and miniaturization, with their combined influence imposing further evolutionary constraint on skull architecture.
  
  Finally, I provide a preliminary phylogenetic re-assessment of snakes. I first revise the morphological dataset most commonly used in snake phylogenies, thus ameliorating the logical and operational inconsistencies affecting previous studies, as well as introducing several characters relevant to scolecophidian systematics. Maximum parsimony and Bayesian analyses of this revised dataset (which currently includes only extant taxa) recover the traditional topology of Scolecophidia and Alethinophidia as sister clades. However, a subsequent assessment of the phylogenetic impact of fossil snakes reveals that the position of Scolecophidia can change dramatically when extinct taxa are included. Similarly, an examination of the synapomorphies and symplesiomorphies of Scolecophidia as optimized on the revised-dataset cladogram reveals very few—if any—of them to be reliable, with several being highly susceptible to paedomorphosis- and/or fossoriality-related homoplasy. These results indicate that the inclusion of fossil snakes, alongside mitigation of the aforementioned sources of homoplasy, will be essential in reliably reconstructing the phylogeny of snakes.
  
  Ultimately, this thesis strongly rejects the traditional paradigm of scolecophidians as fundamentally ‘basal’ to other snakes. The miniaturization-related anatomical spectrum described above instead supports the controversial hypothesis of scolecophidians as ‘regressed alethinophidians’, reflecting paedomorphosis-driven derivation of the scolecophidian skull from a fossorial alethinophidian condition. Furthermore, the lack of synapomorphy among scolecophidian jaw mechanisms is inconsistent with the notion that they represent a homogenous and ancestral snake morphology; combined with the novel evidence of convergence presented herein, these results instead suggest the independent evolution of fossoriality, miniaturization, and ‘microstomy’ in each scolecophidian lineage. Altogether, I therefore advocate a hypothesis of scolecophidians as a highly convergent assemblage, marked by extensive paedomorphic ‘regression’ from a more typical snake-like bauplan.
  

• Subjects / Keywords

  • evolutionary development
  • fossoriality
  • heterochrony
  • micro-CT
  • miniaturization
  • functional morphology
  • homology
  • network analysis
  • phylogeny
  • paedomorphosis

• Graduation date

  Fall 2021

• Type of Item

  Thesis

• Degree

  Master of Science

• DOI

  https://doi.org/10.7939/r3-j4gc-k528

• License

  This thesis is made available by the University of Alberta Libraries with permission of the copyright owner solely for non-commercial purposes. This thesis, or any portion thereof, may not otherwise be copied or reproduced without the written consent of the copyright owner, except to the extent permitted by Canadian copyright law.