Picking up the threads: Comparative osteology and associated cartilaginous elements for members of the genus Trilepida Hedges, 2011 (Serpentes, Leptotyphlopidae) with new insights on the Epictinae systematics

Abstract

The threadsnakes of the family Leptotyphlopidae have been historically neglected in terms of their natural history, ecology, systematics, and morphology. Given the relevance of morphological data for resolving systematic, evolutionary, and functional issues, we aimed to provide a detailed comparative description of osteology and associated cartilaginous elements for members of the genus Trilepida. Data were obtained through high-resolution computed tomography images, cleared and stained specimens, and radiography images of a total of 47 specimens and 12 species. Both cranial and axial osteology characters exhibited a relevant degree of intraspecific variation regarding qualitative and quantitative data associated with skull and vertebrae foramina and the shape of bony sutures and processes. The high representativeness of examined species and specimens allows us to provide a comprehensive discussion on the inter-and intraspecific osteological variation, as well as a compelling osteological diagnosis for the entire genus. Trilepida spp. differ from all Epictinae by the presence of the following combination of characters: paired nasals, fused supraoccipitals (distinct from parietal, prootics, and otooccipitals), a single (fused) parietal without a dorsal fontanelle, and the basioccipital participating in the foramen magnum (except in Trilepida nicefori). Our results reinforce the need for integration of detailed anatomical traits to usually conserved external morphological data to provide accurate diagnostic features for Epictinae. In addition, new phylogenetic hypotheses or even taxonomic re-allocations may broadly benefit from these detailed comparative studies.

An evolutionary paradox on threadsnakes: Phenotypic and molecular evidence reveal a new and remarkably polymorphic species of Siagonodon (Serpentes: Leptotyphlopidae: Epictinae) from Amazonia

“…The fossorial snakes of the Family Leptotyphlopidae (approximately 140 nominal extant species; Uetz et al 2022) usually exhibit an extremely conserved external morphology (Martins et al 2021a) and are among the least known terrestrial vertebrates (Marin et al 2013). Although molecular evidence has helped in determining their higher-level relationships (Adalsteinsson et al 2009), such data have rarely been useful for unambiguous diagnosis among genera (Martins et al 2019a), which were defined based on general resemblance (i.e., external morphology) of traditional species groups (see Orejas-Miranda 1967;Peters and Orejas-Miranda 1970).…”

“…Thus, we examined the skull of one paratype of S. acutirostris (CHUNB 35648; Fig. 2), and noticed that the putative osteological diagnostic data of Trilepida proposed by Martins et al (2021a): i.e., (i) the basioccipital participating in the formation of the foramen magnum, (ii) paired nasals and (iii) fused supraoccipitals are present in S. acutirostris. These data contrast with skull data from Siagonodon spp.…”

“…6; n = 3; holotype condition indicated with asterisk). Premaxilla wide, expanded anterolaterally, roughly rectangular (n = 2*) or trapezoidal (n = 1) in anterior view; and triangular in ventral view, edentulous, pierced by seven (n = 2) or eight (n = 1*) foramina; nasal process of premaxilla reduced and tapered toward apex, transverse process absent and vomerian process tapered and single; premaxilla with internal septum composed of two laminae that support the septum nasi dorsally, expanding posteriorly and contacting septomaxilla ventrally; nasals paired, elongated, expanded anterolaterally, with convex anterior limit, and undulated dorsoposterior suture with frontals; being pierced by pair of foramina in posterolateral border of contact with prefrontals and frontals (foramen for the apicalis nasi); additional pair of foramina pierce on the medial contact within both nasals; nasal septum descending as double medial vertical flanges that contact premaxilla and septomaxilla ventrally (internally); prefrontals paired, irregular in shape, in contact with septomaxilla midventrally, and separated by short gap (n = 2*) from maxilla ventrolaterally or in contact with it (n = 1); each prefrontal perforated by two (n = 2*) or three (n = 1*) foramina; septomaxillae paired, complex in shape, expanding dorsoanteriorly and comprising posterior limit of naris; conchal invagination absent; ascending process of premaxilla pierced by single large foramen (n = 2*) or by two foramina (n = 1); internally, dorsal surface of each septomaxilla pierced by single foramen (n = 3 sides*) or two foramina (n = 3 sides*), and with medial inconspicuous sulcus (n = 2*), or sulcus absent (n = 1); vomers paired, located midventral to vomeronasal cupola, transversal arms absent, with posterior arms in contact with each other posteriorly (n = 2*) or not (n = 1); pair of foramina pierce the ventral lamina of each vomer; frontals paired, elongated, approximately twice longer than wide, both elements bearing short anterolateral projections to attach to prefrontals; frontal pillars absent; optic nerve foramen paired (n = 2*) or single (n = 1), restricted to lateral descending surface of frontals; maxilla edentulous, irregular in shape, pierced by four (n = 1*) or six (n = 2) foramina; posterior process of maxilla reaching (n = 1) or not reaching (n = 2*) level of anteriormost optic nerve foramen in lateral view; posterior orbital element absent; parietal single, wide, representing largest bone of braincase; parietal internal pillars (sensu Martins et al 2021a) present; parabasisphenoid arrow-like, with tapered anterior tip lying dorsally to palatine, and fitting in medial line of vomeronasal cupola; posterior limit of parabasisphenoid convex medially; internal (dorsal) face of parabasisphenoid with inconspicuous lateral sulci; anterior opening for palatine artery indistinct or absent, internal carotid artery foramen and abducens nerve foramen present; opening for palatine ramus of facial nerve formed by lateral edge of parabasisphenoid and ventral edge of parietal; basioccipital single and approximately triangular in ventral view, lateral process for attachment of tendons for nuchal muscles (Martins et al 2019b) absent; basioccipital does not participate in formation of foramen magnum; supraoccipitals fused into single unit, approximately twice wider than long; prootics fused to otooccipitals; prootics+otooccipitals forming trigeminal nerve foramen together with parietal and parabasisphenoid (on one side of one specimen parabasisphenoid does not participate in it); prootics pierced medially (internally) by single acoustic nerve foramen; two statolythic masses present in cavum vestibuli (n = 2*) or statolythic mass absent; stapedial footplate apparently not co-ossified with prootic; otooccipitals dorsally fo...…”

“…Pinto and Curcio (2011) described Siagonodon acutirostris based on a combination of morphological characters, including a new character for the diagnosis of the genus. Martins (2021a) proposed the following osteologically diagnostic characters for the genus Trilepida based on a high sample of species: (i) the basioccipital participating in the formation of the foramen magnum, (ii) paired nasals and (iii) fused supraoccipitals. Based on the combination of morphological characters proposed by Adalsteisson et al (2009), Pinto and Curcio (2011), and Martins (2016, 2021a, and the molecular data provided herein, we propose a new combination and new diagnosis for S. acutirostris and regard the presence of fused caudals as a homoplastic character.…”

“…These snakes have long posed challenges for researchers interested in elucidating their taxonomy, systematics, and consequently biogeography and evolution (Bell et al 2021). However, recent contributions-most of them boosted by the use of high resolution digital images (Rieppel et al 2009;Reis 2018, 2019;Koch et al 2019;Martins et al 2019a;Koch et al 2021;Lira and Martins 2021;Deolindo et al 2021;Martins et al 2021aMartins et al , 2021b-have repeatedly highlighted morphological data (mostly osteological) as fundamental for elucidating longstanding unresolved or disputed issues in the literature (see Miralles et al 2018). For instance, several studies (e.g., Koch et al 2019Koch et al , 2021Martins et al 2019a) have taken advantage of µCT data to overcome the challenges imposed by the overall highly conserved external morphology of scolecophidians, demonstrating the informativeness of skull and lower jaw characters for systematic studies .…”