Moving beyond the surface: Comparative head and neck myology of threadsnakes (Epictinae, Leptotyphlopidae, Serpentes), with comments on the ‘scolecophidian’ muscular system

RESEARCH ARTICLE Moving beyond the surface: Comparative head and neck myology of threadsnakes (Epictinae, Leptotyphlopidae, Serpentes), with comments on the ‘scolecophidian’ muscular system Angele Martins ID1,2*, Paulo Passos1, Roberta Pinto1,3 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, 2 Departamento de Ciências Fisiológicas, Instituto de Biociências, Universidade de Brası́lia, Brası́lia, Distrito Federal, Brazil, 3 Museu de Arqueologia da Universidade Católica de Pernambuco, Universidade Católica de Pernambuco, Boa Vista, Recife, Pernambuco, Brazil * OPEN ACCESS Citation: Martins A, Passos P, Pinto R (2019) Moving beyond the surface: Comparative head and neck myology of threadsnakes (Epictinae, Leptotyphlopidae, Serpentes), with comments on the ‘scolecophidian’ muscular system. PLoS ONE 14(7): e0219661. https://doi.org/10.1371/journal. pone.0219661 Editor: Hector Escriva, Laboratoire Arago, FRANCE Received: March 13, 2019 Accepted: June 28, 2019 Published: July 18, 2019 Copyright: © 2019 Martins et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Funding: Angele Martins is grateful to the Smithsonian Institute for the Short-Term Fellowship Grant provided and to Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior (CAPES) for the scholarship (process 99999.010032/2014-02) provided during her PhD; and to K de Queiroz, D Johnson, A Nonaka, R McDiarmid and all USNM staff for the support Abstract Studies on the cephalic myology of snakes provide a series of relevant data on their biology and systematics. Despite the great amount of descriptive studies currently available for the group, much of the knowledge remains obscure for most scolecophidian taxa. This study aimed to describe in detail the cephalic (head and neck) myology of members of the tribe Epictinae, Leptotyphlopidae. We provide the first report of the presence of extrinsic ocular muscles, and a double Musculus pterygoideus acessorius in Leptotyphlopidae. A welldeveloped M. levator anguli oris is exclusive to the subtribes Renina and Epictina, being reduced in Tetracheilostomina species. Both inter- and intraspecific variations are reported for the head and neck muscles, and such results provide additional data and raise an interesting discussion on the neck-trunk boundaries in snakes. We also provide a discussion on the terminology of a few head muscles in Leptoyphlopidae in comparison to the other lineages of ´Scolecophidia´ (Anomalepididae and Typhlopoidea). Introduction The threadsnakes of the family Leptotyphlopidae currently comprise about 140 recognized species that occur in the sub-Saharan Africa (Leptotyphlopinae and Rhinoleptini) and in the New World (Americas and Antilles), with the subfamily Epictinae containing about 90 species allocated in nine currently recognized genera [1]. Despite the ancient cladogenesis event and the separation between these two main lineages of Leptotyphlopidae [2], all living species present an entirely fossorial lifestyle, actively eating on larvae or adults of social insects [3–5]. Leptotyphlopids fully ingest their prey through a very specialized food intake mechanism named mandibular raking [6], contrasting with the feeding mechanism of the alethinophidian snakes called pterygoidal walk (see [4]). The leptotyphlopid feeding mechanism most likely enables PLOS ONE | https://doi.org/10.1371/journal.pone.0219661 July 18, 2019 1 / 42 Comparative head and neck myology of Epictinae during the conduction of the project in the USA. Angele Martins was supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ, E-26/202.403/2017). Paulo Passos was supported by Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq processes 8256995713198058, 482086/ 2012-2, and 306227/2015-0) and Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ, E-26/110.434/2012 and E-26/111.636/2012). Competing interests: The authors have declared that no competing interests exist. relatively fast food intake compared to alethinophidian snakes, and possibly evolved due to the huge retaliatory response of social insects within their nests [7]. The differences in the leptotyphlopid feeding mechanism and their foraging pattern/diet is visible in the distinct phenotypes of, for example, head muscles and skull and jaw elements [4,7]. Such morphological changes might have played a fundamental role in the diversification of leptotyphlopid lineages and may be interpreted as an adaptation for feeding on social insects, considering the spectacular radiation of ants and termites during the Mesozoic age [8–10]. In this sense, the modification of the muscular-osteological system could represent a key innovation (or even an ecological break) leading potentially to the opening of a new niche for snakes. Despite the great amount of cephalic myology studies available for snakes (e.g., [11–17]), much of the knowledge remain obscure for several key taxa, with new muscles still being identifyied and described [18]. Some studies on the cephalic myology of snakes provide a series of relevant data regarding their biology (e.g., functional morphology), as well as several systematic issues [19]. Regarding scolecophidians (sensu lato, i.e., Anomalepididae + Leptotyphlopidae + Typhlopoidea; sensu Vidal et al. [20]), the main difficulties of providing comparative cephalic myology data and hypothesized primary homologies from muscular complexes are caused by the completely different muscular system and innervation patterns as compared to Alethinophidia (e.g., scolecophidian snakes lacking an aponeurotic system in adductor muscles; [21,22,23]). Additionally, the numerous terminologies utilized to describe the cephalic myology of ‘Scolecophidia’ hamper a precise comparative study amongst taxa of this infraorder. Studies on the post-cephalic muscles in snakes are extremely scarce in comparison to other anatomical complexes such as cephalic myology, cephalic glands, cranial and axial osteology, cartilaginous elements, hemipenes, external morphology, viscera, etc. Besides the classical descriptions of the trunk myology by Mosauer [24] and Gasc [25], very few additional studies are available, which are mostly focused on Alethinophidia (e.g., [26–31]). Descriptive and/or comparative studies of the craniovertebral myology in snakes have received even less attention in the past (e.g., [18,32–36]). Haas’ seminal studies on the head muscles of both leptotyphlopids and typhlopids [13,14,37] were the first contr (...truncated)