Deconstructing the Gestalt: New concepts and tests of homology, as exemplified by a re-conceptualization of “microstomy” in squamates

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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.

Original languageEnglish
JournalAnatomical Record
Volume304
Issue number10
Pages (from-to)2303-2351
Number of pages49
ISSN1932-8486
DOIs
Publication statusPublished - 2021
Externally publishedYes

Bibliographical note

Funding Information:
Funding for this research was provided via an Alexander Graham Bell Canada Graduate Scholarship awarded by the Natural Sciences and Engineering Research Council of Canada (NSERC) to Catherine R. C. Strong and an NSERC Discovery Grant (#23458) to Michael W. Caldwell This work was also performed in part at the Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Coordinated Infrastructure Network (NNCI) and part of Harvard University, which is supported by the National Science Foundation under NSF award no. 1541959. Copyright of all MCZ scans belongs to the Museum of Comparative Zoology, Harvard University, and the associated raw digital media are © President and Fellows of Harvard College, 2020, all rights reserved. These are used herein with permission. Several scans were obtained from DigiMorph.org , as provided by the University of Texas High‐Resolution X‐ray CT Facility (UTCT). Scans of YPM 14378 and YPM 14376 were originally collected under NSF grants DEB‐0132227, EF‐0334961, and IIS‐9874781. Scans of FMNH 58299, FRIM 0026, FMNH 216257, USNM 12378, FMNH 148589, FMNH 22468, and UMMZ 190285 were collected under NSF grants IIS‐0208675 and EF‐0334961. Scans of USNM 204078, FMNH 60958, FMNH 62204, FMNH 63117, FMNH 117833, FMNH 104800, and FMNH 148900 were collected under NSF grant EF‐0334961. Scans of TNHC 60638 and YPM 12871 were collected under NSF grants EF‐0334961 and IIS‐9874781. Scans of TMM M‐10006, YPM 6057, and TNHC 18483 were collected under NSF grant IIS‐9874781. Scans of TNHC 62769 were collected under NSF grant IIS‐0208675. Scans of FMNH 167048 and UTA 50569 were also obtained from DigiMorph. Scans of FMNH 179335, FMNH 30522, FMNH 58322, FMNH 62248, FMNH 259340, FMNH 31162, and FMNH 128304 were examined using images provided online by DigiMorph. Several other scans were downloaded from MorphoSource, Duke University. The University of Michigan Museum of Zoology provided access to the data for UMMZ 201901 (M39211‐70987) and UMMZ 174763 (M45443‐82778), the collection of which was funded by oVert TCN under NSF DBI‐1701714 and NSF DBI‐1701713. The University of Florida provided access to the data for UF 33488 (M33644‐62342), the collection of which was funded by oVert TCN under NSF DBI‐1701714. The University of Kansas Center for Research Inc provided access to the data for KUH 125976 (M41676‐75015), the collection of which was funded by oVert TCN under NSF DBI‐1701714, NSF DBI‐1701713, and NSF DBI‐1701932. The Field Museum of Natural History provided access to the data for FMNH 264702 (M27566‐52993), the collection of which was funded by oVert TCN under NSF DBI‐1701714 and NSF DBI‐1702421. oUTCT provided access to the data for FMNH 195924 (M53075‐96074), FMNH 22847 (M54489‐98383), FMNH 31182 (M54499‐98393), TCWC 45501 (M62793‐113753), CAS 126478 (M54497‐98391), CAS 134753 (M54498‐98392), CAS 26937 (M54605‐98507), FMNH 31774 (M54687‐98600), and FMNH 109462 (M54697‐98610), originally appearing in Gauthier et al. ( 2012 ), with data collection funded by NSF EF‐0334961 and data upload to MorphoSource funded by DBI‐1902242. Mark D. Scherz provided access to the data for ZSM 2194/2007 (M43873‐79510), originally appearing in Chretien et al. ( 2019 ). Finally, scans from the AMS, QM, and SAMA collections were provided courtesy of A. Palci, and scans of UAMZ specimens were provided courtesy of lab colleagues.

Funding Information:
National Science Foundation, Grant/Award Numbers: DBI‐1702421, DBI‐1701932, DBI‐1701713, DBI‐1701714, EF‐0334961, IIS‐0208675, IIS‐9874781, DEB‐0132227, 1541959; Natural Sciences and Engineering Research Council of Canada (NSERC), Grant/Award Number: (#23458) Funding information

Funding Information:
Funding for this research was provided via an Alexander Graham Bell Canada Graduate Scholarship awarded by the Natural Sciences and Engineering Research Council of Canada (NSERC) to Catherine R. C. Strong and an NSERC Discovery Grant (#23458) to Michael W. Caldwell This work was also performed in part at the Center for Nanoscale Systems (CNS), a member of the National Nanotechnology Coordinated Infrastructure Network (NNCI) and part of Harvard University, which is supported by the National Science Foundation under NSF award no. 1541959. Copyright of all MCZ scans belongs to the Museum of Comparative Zoology, Harvard University, and the associated raw digital media are ? President and Fellows of Harvard College, 2020, all rights reserved. These are used herein with permission. Several scans were obtained from DigiMorph.org, as provided by the University of Texas High-Resolution X-ray CT Facility (UTCT). Scans of YPM 14378 and YPM 14376 were originally collected under NSF grants DEB-0132227, EF-0334961, and IIS-9874781.

Publisher Copyright:
© 2021 American Association for Anatomy.

    Research areas

  • ancestral state reconstruction, functional morphology, homology, skull anatomy, snake evolution

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