Figure 11 - uploaded by Alessandro Palci
Content may be subject to copyright.
'Regressed alethinophidian' hypothesis of scolecophidian evolution. (A) Example of how 'regression' from a 'typical' or non-fossorial alethinophidian skull (represented by the colubroid Thamnophis radix, UAMZ R636), to a fossorial alethinophidian (represented by Atractaspis irregularis, FMNH 62204), to a typhlopoid skull morphology (Indotyphlops braminus, UAMZ R363) could easily occur due to fossorial adaptations, paedomorphosis, and miniaturization. (B) Example of how the leptotyphlopid skull (Leptotyphlops dulcis, TNHC 60638) could easily be derived from that of a basal alethinophidian (Cylindrophis ruffus, FMNH 60958) through accumulation of fossorial adaptations, paedomorphosis, and miniaturization. In this scenario, Anomochilus leonardi (FRIM 0026) would represent an ideal morphological intermediate between the two endpoint skull types. We propose that miniaturization in scolecophidians further superimposes unique features overtop an ancestral fossorial alethinophidian morphotype. Note that these are only examples of morphological grades and do not imply phylogenetic relationships, only that the scolecophidian skull typology could be derived from an ancestral alethinophidian condition. Elements of the jaws and suspensorium affected by paedomorphosis are highlighted. Colouration of bones is consistent throughout panels. Specimens not to scale. Abbreviations: cb, compound bone; d, dentary; ecp, ectopterygoid; mx, maxilla; pal, palatine; pt, pterygoid; q, quadrate; st, supratemporal.
Source publication
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 gr...
Similar publications
The early Permian Richards Spur locality of Oklahoma has produced abundant material of numerous terrestrial fossil tetrapods, including various “microsaurs,” several of which are considered to belong to the clade Recumbirostra. We present a new partial skull of the recumbirostran “microsaur” Nannaroter mckinziei; through computed tomography (CT) an...
Citations
... Among snakes, extreme cases of miniaturization are found in blind snakes, threadsnakes, and worm snakes traditionally known as "Scolecophidia." Recent works have hypothesized that several characteristics of the group are a result from miniaturization possibly driven by paedomorphosis, including the loss/reduction of several skull bones in comparison to alethinophidian snakes (Strong et al. 2020). ...
... The preference for a largely secretive way Sunandan Das and Jonathan Brecko have contributed equally and should be considered joint first authors. terms of both the number of taxa assigned and their morphology, aparallactines have not received as much attention from anatomists and functional morphologists as Atractaspis (e.g., Deufel & Cundall, 2003;Strong et al., 2020). Strong et al. (2020) described the cranial osteology thoroughly and discussed the evolution of burrowing adaptations in Atractaspis irregularis, but a similar detailed bone-bybone description does not exist for any aparallactines. ...
... terms of both the number of taxa assigned and their morphology, aparallactines have not received as much attention from anatomists and functional morphologists as Atractaspis (e.g., Deufel & Cundall, 2003;Strong et al., 2020). Strong et al. (2020) described the cranial osteology thoroughly and discussed the evolution of burrowing adaptations in Atractaspis irregularis, but a similar detailed bone-bybone description does not exist for any aparallactines. Bourgeois (1968) described the crania of some aparallactines and atractaspidines in her landmark contribution of African snake cranial osteology. ...
... were obtained from MorphoSource (https://www.morphosource.org/) and Digimorph (http://digimorph.org/index.phtml) databases and from Strong et al. (2020) (an Atractaspis irregularis, the scan of which is also available on Digimorph). We also obtained scans of the skull of Boaedon fuliginosus as an outgroup for phylogenetic analyses, and some fossorial basal alethinophidians as comparative materials to study fossorial adaptations from MorphoSource and Digimorph, respectively. ...
Fossoriality evolved early in snakes, and has left its signature on the cranial morphology of many extinct Mesozoic and early Caenozoic forms. Knowledge of the cranial osteology of extant snakes is indispensable for associating the crania of extinct lineages with a particular mode of life; this applies to fossorial taxa as well. In the present work, we provide a detailed description of the cranium of Hypoptophis wilsonii, a member of the subfamily Aparallactinae, using micro‐computed tomography (CT). This is also the first thorough micro‐CT‐based description of any snake assigned to this African subfamily of predominantly mildly venomous, fossorial and elusive snakes. The cranium of Hypoptophis is adapted for a fossorial lifestyle, with increased consolidation of skull bones. Aparallactines show a tendency towards reduction of maxillary length by bringing the rear fangs forward. This development attains its pinnacle in the sister subfamily Atractaspidinae, in which the rear fang has become the ‘front fang’ by a loss of the part of the maxilla lying ahead of the fang. These dentitional changes likely reflect adaptation to subdue prey in snug burrows. An endocast of the inner ear of Hypoptophis shows that this genus has the inner ear typical of fossorial snakes, with a large, globular sacculus. A phylogenetic analysis based on morphology recovers Hypoptophis as a sister taxon to Aparallactus. We also discuss the implications of our observations on the burrowing origin hypothesis of snakes.
This article is protected by copyright. All rights reserved.
... Among snakes, extreme cases of miniaturization are found in blind snakes, threadsnakes, and worm snakes traditionally known as "Scolecophidia." Recent works have hypothesized that several characteristics of the group are a result from miniaturization possibly driven by paedomorphosis, including the loss/reduction of several skull bones in comparison to alethinophidian snakes (Strong et al. 2020). ...
... The "scolecophidian" snakes have long been regarded as miniaturized lineages, although-as far as we are aware-only very few studies have addressed this matter with the discussion of phenotypic consequences driven by this phenomenon (e.g., Chretien, Wang-Claypool, Glaw, & Scherz, 2019;Hedges, 2008;Strong, Palci, & Caldwell, 2021). Recent works (Kley, 2006;Rieppel & Maisano, 2007;Strong et al., 2021) hypothesize that several "typical" scolecophidian characteristics might represent a result of paedomorphosis, such as the lack of medial frontal pillars, of a laterosphenoid, the reduction of palatal and lower jaw elements, and the lack of crests and ridges in the braincase. ...
... The "scolecophidian" snakes have long been regarded as miniaturized lineages, although-as far as we are aware-only very few studies have addressed this matter with the discussion of phenotypic consequences driven by this phenomenon (e.g., Chretien, Wang-Claypool, Glaw, & Scherz, 2019;Hedges, 2008;Strong, Palci, & Caldwell, 2021). Recent works (Kley, 2006;Rieppel & Maisano, 2007;Strong et al., 2021) hypothesize that several "typical" scolecophidian characteristics might represent a result of paedomorphosis, such as the lack of medial frontal pillars, of a laterosphenoid, the reduction of palatal and lower jaw elements, and the lack of crests and ridges in the braincase. These authors also reinforce the hypothesis that the autapomorphic conditions found in scolecophidians are indeed related to the specialized miniaturized and fossorial nature of this group. ...
... Because miniaturization can occur in confluence with fossoriality (Lee, 1998;Rieppel, 1984;Rieppel, 1996;Strong et al., 2021) several traits that will be discussed herein might also be a result of headfirst fossorial habits found in both Mitophis and Tetracheilostoma (as well as all other known "scolecophidians"). Previous works on squamates that are headfirst burrowers indicate that some characteristics of miniaturization might also be associated with fossoriality (e.g., Hanken & Wake, 1993;Lee, 1998;Rieppel, 1996;Roscito & Rodrigues, 2010), since they generate convergent reinforced skulls with reduced mobility. ...
The genera Mitophis and Tetracheilostoma comprise two extant lineages of small‐sized threadsnakes that exclusively inhabit several islands of the West Indies. Even though leptotyphlopids are known for their extremely reduced size, miniaturization has only been hypothesized to reflect insular dwarfism for the genus Tetracheilostoma. Herein, we aim to describe the comparative osteology and visceral morphology of both genera, investigating and discussing their several internal morphological simplifications and novelties. Our results indicate that these taxa exhibit several autapomorphies mostly concentrated in the dorsoposterior skull elements and maxillae, as well as in their axial skeleton and viscera. These novelties and simplifications are most likely a result of extreme miniaturization driven by the evolutionary constraints or ecological opportunities possibly imposed by the “island rule.” Both Mitophis and Tetracheilostoma distinguish from all other Epictinae in lacking a dentigerous process in the maxillae, by having the prootic fused to the otooccipital, and by the lack (except in comparison to a few Epictia) of a cervical vertebrae intercentrum I. Additionally, Mitophis can be distinguished from other Epictinae by the participation of the unpaired supraoccipital in the dorsal border of the foramen magnum, by the absence of the pleurapophyses in the caudal vertebrae, by a higher number of liver segments, and by the extreme degeneration of the pelvic rudiments. Tetracheilostoma differs from other Epictinae by lacking a distinct supraoccipital, which is fused to the parietal. Thus, our results reinforce that morphological characters are extremely valuable for leptotyphlopid systematics given their extremely conserved external morphology.
... Miniaturized species often encounter physiological and ecological challenges (Glaw et al., 2021), and thus extreme body size reduction is often accompanied by profound structural modifications that maintain functionality and facilitate their survival. For example, miniaturization is often associated with organ reduction, tissue loss, and other structural reorganizations (Daza et al., 2008;Hanken & Wake, 1993;Ocampo et al., 2018;Rieppel, 1996;Strong et al., 2020). Additionally, miniaturization can result in other distinctive features, such as enlarged sensory organs and braincases relative to body size (Hanken, 1983;Perez-Martinez & Leal, 2021;Rieppel, 1996), and changes to the nervous system (Faisal, 2005;Niven & Farris, 2012), which are crucial for navigating in complex microenvironments. ...
The evolution of miniaturization can result in dramatic alterations of morphology, physiology and behavior; however the effects of miniaturization on sexual dimorphism remain largely unknown. Here we investigate how miniaturization influences patterns of sexual size dimorphism (SSD) in geckos. Measuring 1,875 individuals from 131 species, we character-ized patterns of SSD relative to body size across two families. We found that miniaturized species were more female-biased than non-miniaturized species. Additionally, one family which contained many miniaturized species (Sphaerodactylidae) displayed allometric pat- terns in SSD with body size, where larger species were male-biased and smaller species were more female-biased. Smaller species in this lineage also produced proportionally larger eggs. By contrast, another family containing few miniaturized species (Phyllodactylidae) displayed a more isometric trend. Together, these observations are consistent with the hypothesis that selection for increased reproductive success in small species of Sphaerodactylidae results in female-biased SSD in these taxa, which in turn drives the positive SSD allometry observed in this lineage. Thus, selection for increased miniaturization in the clade may be offset by selection on maintaining a female size in smaller taxa that ensures reproductive success.
The arrangement and morphology of the vertebrate skull reflect functional and ecological demands, making it a highly adaptable structure. However, the fundamental developmental and macroevolutionary mechanisms leading to different vertebrate skull phenotypes remain unclear. Here we exploit the morphological diversity of squamate reptiles to assess the developmental and evolutionary patterns of skull variation and covariation in the whole head. Our geometric morphometric analysis of a complex squamate ontogenetic dataset (209 specimens, 169 embryos, 44 species), covering stages from craniofacial primordia to fully ossified bones, reveals that morphological differences between snake and lizard skulls arose gradually through changes in spatial relationships (heterotopy) followed by alterations in developmental timing or rate (heterochrony). Along with dynamic spatiotemporal changes in the integration pattern of skull bone shape and topology with surrounding brain tissues and sensory organs, we identify a relatively higher phenotypic integration of the developing snake head compared with lizards. The eye, nasal cavity and Jacobson’s organ are pivotal in skull morphogenesis, highlighting the importance of sensory rearrangements in snake evolution. Furthermore, our findings demonstrate the importance of early embryonic, ontogenetic and tissue interactions in shaping craniofacial evolution and ecological diversification in squamates, with implications for the nature of cranio-cerebral relations across vertebrates.
Background
Sexual dimorphism in size and shape is widespread among squamate reptiles. Sex differences in snake skull size and shape are often accompanied by intersexual feeding niche separation. However, allometric trajectories underlying these differences remain largely unstudied in several lineages. The sea krait Laticauda colubrina (Serpentes: Elapidae) exhibits very clear sexual dimorphism in body size, with previous studies having reported females to be larger and to have a relatively longer and wider head. The two sexes also differ in feeding habits: males tend to prey in shallow water on muraenid eels, whereas females prey in deeper water on congerid eels.
Methods
I investigated sexual dimorphism in skull shape and size as well as the pattern of skull growth, to determine whether males and females follow the same ontogenetic trajectories. I studied skull characteristics and body length in 61 male and female sea kraits.
Results
The sexes differ in skull shape. Males and females follow distinct allometric trajectories. Structures associated with feeding performance are female-biased, whereas rostral and orbital regions are male-biased. The two sexes differ in allometric trajectories of feeding-related structures (female biased) that correspond to dietary divergence between the sexes.
Conclusions
Sea kraits exhibit clear sexual dimorphism in the skull form that may be explained by intersexual differences in the feeding habits as well as reproductive roles. The overall skull growth pattern resembles the typical pattern observed in other tetrapods.
Background
Dipsadine snakes represent one of the most spectacular vertebrate radiations that have occurred in any continental setting, with over 800 species in South and Central America. Their species richness is paralleled by stunning ecological diversity, ranging from arboreal snail-eating and aquatic eel-eating specialists to terrestrial generalists. Despite the ecological importance of this clade, little is known about the extent to which ecological specialization shapes broader patterns of phenotypic diversity within the group. Here, we test how habitat use and diet have influenced morphological diversification in skull shape across 160 dipsadine species using micro-CT and 3-D geometric morphometrics, and we use a phylogenetic comparative approach to test the contributions of habitat use and diet composition to variation in skull shape among species.
Results
We demonstrate that while both habitat use and diet are significant predictors of shape in many regions of the skull, habitat use significantly predicts shape in a greater number of skull regions when compared to diet. We also find that across ecological groupings, fossorial and aquatic behaviors result in the strongest deviations in morphospace for several skull regions. We use simulations to address the robustness of our results and describe statistical anomalies that can arise from the application of phylogenetic generalized least squares to complex shape data.
Conclusions
Both habitat and dietary ecology are significantly correlated with skull shape in dipsadines; the strongest relationships involved skull shape in snakes with aquatic and fossorial lifestyles. This association between skull morphology and multiple ecological axes is consistent with a classic model of adaptive radiation and suggests that ecological factors were an important component in driving morphological diversification in the dipsadine megaradiation.
Braincase descriptions of lepidosaurian clades (Rhynchocephalia and Squamata) are scarce, and paleoneurological studies are even scarcer when compared to other reptiles. Regarding paleoneurology sensu stricto, so far mosasauroids and snakes (the latter by means of a single published study) remain the better known lepidosaur groups. Further comparisons among extinct and living lepidosaurs – along with their evolutive history starting in the early Triassic– are not possible due to the lack of neuroanatomical information in most families. Here we provide a revision of the published literature on endocranial anatomy and paleoneurology in Lepidosauria, including an overview of the comparative braincase and neuroanatomy of living representatives of the clade. We hope that this information will have an impact on future studies in the field of comparative neuroanatomy in both living and extinct species. Micro-CT and diceCT data are currently facilitating neuroanatomical comparisons among living species, preparing the background for a potential rise of paleoneurological studies of non-marine extinct lepidosaurs.
