TABLE 2 - uploaded by Ricardo Montero
Content may be subject to copyright.
Source publication
An assemblage of amphisbaenian embryos has allowed us to characterize the external morphology of the developing embryos as well as the chondrification and ossification sequences of their skeletal elements. The external characterization of embryos serves as an incomplete developmental table. In contrast to the condition in other squamates, the prema...
Context in source publication
Context 1
... Tucumá n fe- male (FML 02605) laid five eggs (in the laboratory, on November 21, 1991), at a sur- prisingly constant interval of 25 minutes each (the last one appeared at the cloaca 25 minutes after the previous one, but was ex- pelled only after 15 more minutes; perhaps this delay reflected the absence of further oviductal eggs that could have pushed it out). The morphometry of the eggs after removal from the oviducts is given in Table 2. ...
Similar publications
An assemblage of amphisbaenian embryos has allowed us to characterize the external morphology of the developing embryos as well as the chondrification and ossification sequences of their skeletal elements. The external characterization of embryos serves as an incomplete developmental table. In contrast to the condition in other squamates, the prema...
Citations
... Our observations of A. brongersmianus skull ontogeny showed that the quadrate has an almost horizontal orientation in embryos and remains the same during postnatal development. Limb-reduced lizards and nonmacrostomous alethinophidian snakes have a vertically or slightly anteriorly oriented quadrate, and the lack of rotation along ontogeny was also reported for these groups (Montero et al., 1999;Roscito & Rodriguez, 2012;Werneburg et al., 2015;Scanferla, 2016). In contrast, the quadrate of macrostomous alethinophidians experiences a noteworthy counterclockwise rotation during ontogeny (Bellairs & Kamal, 1981;Rieppel, 1988;Palci et al., 2016;Scanferla, 2016). ...
Blind snakes represent the most basal group of extant snakes and include fossorial species with unusual skeletal traits. Despite their known phylogenetic position, little is known about their ontogeny and what it might reveal about the origin of their skull anatomy. Here we describe for the first time the ontogenetic transformations of the skull of a blind snake, the typhlopid Amerotyphlops brongersmianus, including embryos and postnatal individuals. Furthermore, we provide data on the size changes relative to skull growth of the main elements of the gnathic complex. We observed that the skull of this blind snake undergoes considerable morphological change during late ontogeny. Additionally, we detected delayed development of some traits (closure of the skull roof, opisthotic-exoccipital suture, ossification of the posterior trabeculae) simultaneously with clearly peramorphic traits (development of the crista circumfenestralis, growth of the pterygoid bar). Our analysis suggests that the unique skull anatomy of blind snakes displays plesiomorphic and highly autapomorphic features, as an outcome of heterochronic processes and miniaturization, and is shaped by functional constraints related to a highly specialized feeding mechanism under the selective pressures of a fossorial lifestyle.
... This leads to the deduction that their ossification likewise lags behind that of non-palatal dermatocranial elements. Delayed chondrocranial ossification is also seen in extant reptiles 21,[23][24][25][26][27][28] . The sequence of dermatocranial ossification is variable between taxa, but the skull roof often lags behind most other dermatocranial elements in ossification in sauropsids. ...
The availability of a large sample size from a range of ontogenetic stages makes Stenopterygius quadriscissus a good model to study ontogenetic variation in a fossil sauropsid. We qualitatively examined pre- and postnatal ontogenetic changes in the cranium of S. quadriscissus. The prenatal ossification sequence is similar to other diapsids, exhibiting delayed chondrocranial ossification compared to the dermatocranium. In the dermatocranium, the circumorbital area is more ossified earlier in development relative to other elements, especially those of the skull roof where ossification is comparatively weaker across prenatal stages. Perinatally all cranial elements are ossified, and many scarf and step joints are already closed. We propose four prenatal and three postnatal stages in S. quadriscissus on the basis of relative ossification, size and qualitative cranial characters pertaining to the jugal, parietal, frontal, pterygoid and surangular. These will provide a basis for determining ontogenetic stages in other ichthyosaurs. Moreover, our postnatal observations aid in refining ontogenetic characters for phylogenetic studies. Lastly, we observed that the antimeric sutures of the midline of the skull roof are open perinatally and that fusion of the midline only appears in the adult stage. We hypothesize that the loose connection of the midline functions as a fontanelle, limiting potential damage during birth.
... The opposite situation can be observed in the orbitotemporal region of the chondrocranium, which is well formed in the Archelosauria, but becomes more gracile in S. punctatus and tends to be reduced in squamates. 5,6,8,[65][66][67][68][69][70][71][72] ...
... From known evidence, only a few lizards possess an almost similar condition to the snake's trait, where the orbitotemporal part of the chondrocranium is almost completely missing. This can be found in Amphisbaenia 72,74 and Scincidae. 71 In addition, there is a complete absence of limbs in these lizards. ...
Background
In vertebrates, the skull evolves from a complex network of dermal bones and cartilage—the latter forming the pharyngeal apparatus and the chondrocranium. Squamates are particularly important in this regard as they maintain at least part of the chondrocranium throughout their whole ontogeny until adulthood. Anguid lizards represent a unique group of squamates, which contains limbed and limbless forms and show conspicuous variation of the adult skull.
Results
Based on several emboadryonic stages of the limbless lizards Pseudopus apodus and Anguis fragilis, and by comparing with other squamates, we identified and interpreted major differences in chondrocranial anatomy. Among others, the most important differences are in the orbitotemporal region. P. apodus shows a strikingly similar development of this region to other squamates. Unexpectedly, however, A. fragilis differs considerably in the composition of the orbitotemporal region. In addition, A. fragilis retains a paedomorphic state of the nasal region.
Conclusions
Taxonomic comparisons indicate that even closely related species with reduced limbs show significant differences in chondrocranial anatomy. The Pearson correlation coefficient suggests strong correlation between chondrocranial reduction and limb reduction. We pose the hypothesis that limb reduction could be associated with the reduction in chondrocrania by means of genetic mechanisms.
... Hugi et al. 2010;Jerez et al. 2015), lacertids (e.g. Rieppel, 1994), amphisbaenians (Montero et al. 1999), teiids (Arias and Lobo, 2006), gymnophthalmids (Hernandez-Jaimes et al. 2012; ...
... As the accounts differ from one another, however, in the number of stages analysed, and therefore in the degree of resolution offered, it can be difficult to compare the order of appearance of individual elements precisely. Two ossification stages were reported for Amphisbaena (Montero et al. 1999), with three for Ptychoglossus (Hernandez-Jaimes et al. 2012), four for Salvator (Tupinambis) (Arias and Lobo, 2006), seven for Varanus (Werneburg et al. 2015), and eight for Elgaria (Good, 1995) and Polychrus (Alvarez et al. 2005). ...
Tarentola annularis is a climbing gecko with a wide distribution in Africa north of the equator. In the present paper, we describe the development of the osteocranium of this lizard, from the first appearance of the cranial elements up to the point of hatching. This is based on a combination of histology and cleared and stained specimens. This is the first comprehensive account of gekkotan pre‐hatching skull development based on a comprehensive series of embryos, rather than a few selected stages. Given that Gekkota is now widely regarded as representing the sister group to other squamates, this account helps to fill a significant gap in the literature. Moreover, as many authors have considered features of the gekkotan skull and skeleton to be indicative of paedomorphosis, it is important to know whether this hypothesis is supported by delays in the onset of cranial ossification. In fact, we found the sequence of cranial bone ossification to be broadly comparable to that of other squamates studied to date, with no significant lags in development.
... Allometry, or shape changes associated with size variation, is a factor that can contribute substantially to the integration of morphological traits. As mentioned above, the influence of allometry was tested using a multivariate regression analysis of independent-contrasts of skull shape (Procrustes coordinates) on independent-contrasts of log-transformed centroid size 50 (Supplementary Tables 7-8); statistical significance was assessed using a permutation test (10000 permutations) against the null hypothesis of total independence. Allometric tests were also adjusted for phylogenetic signal 51 (see Results section of main text) based on phylogenetically independent contrasts 28 , which is equivalent to distance-based phylogenetic generalized least square (D-PGLS) regression 52 . ...
... DCL. ME y E.Montero et al. (1999) Boaedon fuliginosus 10 EE post-oviposición. DCL, 60 días. ...
In the life of an organism (ontogeny), phenotypic changes happen throughout the time. This contribution is a review of: a) terms and definitions used in studies of the ontogeny, b) the importance to distinguish between shape variation (development) and size variation (growth); and c) the need to consider the real time (age) in which the ontogeny takes place. Based on available information about the ontogeny among tetrapods with emphasis in anurans and nonavian sauropsids, it is outlined the need to increase the information about the ontogeny for comparative studies. We denote the relevancy to get tables of development to identify ontogenetic variation, the study of three fundamental components of ontogenies (it forms- size-time), and the processes that the age organizes (development and growth) to contribute the paradigm of the Evolution of the Development.
... 5. Sesamoids ossify, if at all, late in development (Chapman, 1972;Prokopec, Pfeiferova, & Josifko, 1997). The quadrate element does not ossify, remaining fibrocartilagous and only slightly mineralized in adult specimens and element X remains cartilaginous in late embryos of Amphisbaena heterozonata (Montero, Gans, & Lions, 1999), and ossifies only in adults (Gans & Montero, 2008). ...
Sesamoids are elements that originate as intratendinous structures due to genetic and epigenetic
factors. These elements have been reported frequently in vertebrates, although cranial sesamoids
have been recorded almost exclusively in non-tetrapod Osteichthyes. The only tetrapod cranial sesamoids
reported until now have been the transiliens cartilage (of crocodiles and turtles), and another
one located in the quadrate-mandibular joint of birds. Here, we examined seven squamate species
using histological sections, dissections of preserved specimens, dry skeletons, cleared and stained
specimens, computed tomographies (CT), and report the presence of other cranial sesamoids. One is
attached to the cephalic condyle of the quadrate, embedded in the bodenaponeurosis and jaw
adductor muscles of Ophiodes intermedius (Anguidae). The other sesamoid is found at the base of
the basicranium of several squamates, capping the sphenoccipital tubercle, on the lateral side of the
basioccipital–basisphenoid suture. This bone has previously been reported as “element X.” We reinterpret
it as a basicranial sesamoid, as it is associated with tendons of the cranio-cervical muscles.
This bone seems to have the function of resisting tension-compression forces generated by the
muscle during flexion the head. This element was previously known in several squamates, and we
confirmed its presence in three additional squamate families: Gymnophthalmidae, Gekkonidae, and
Pygopodidae. The evidence suggests that cranial sesamoids are a widespread character in squamates,
and it is possible that this feature has been present since the origin of the group.
... haje (Khannoon andEvans, 2014, 2015) and Psammophis sibilans (Khannoon and Zahradnicek, 2016). For amphisbaenians, the situation is much more precarious with only one incomplete staging series available for Amphisbaena darwini heterozonata (Montero et al., 1999). ...
The mouse, chicken, African clawed frog and zebrafish are considered “model organisms” due to their extensive embryological and genetic characterization. However they are far from representative of known diversity, impairing phylogenetic analyses of developmental patterns. Since squamates have historically received limited attention in developmental studies, we here describe the developmental sequence for Tropidurus torquatus, and provide the first post-ovipositional developmental series for the lizard family Tropiduridae. Fifteen developmental stages are described based on morphological traits such as the eye and accessory visual structures, pharyngeal arches, fusion of facial primordia, limb development, pigmentation and scales. Organogenesis is already in progression at oviposition (stage 28), with embryos continuing to develop at the incubation temperature of 30°C ± 1°C, and hatching after 75 ± 5 days, at stage 42. Comparisons with other lizards show a conserved embryonic sequence, however developmental timing differences were found in features such as the pharyngeal arches, endolymphatic sacs, pigmentation and scales. The development of the phallic and cranial lip of the cloaca anlages are compared with that of other lizards. The order of T. torquatus fore- and hindlimb formation differs from that most commonly observed in lizards. The abundance and close association of this species with urban environments, as well as the ease of capturing and managing females, makes T. torquatus an attractive source of developmental data for future experimental and ontogenetic studies. This article is protected by copyright. All rights reserved.
... Among temnospondyls, loss of skull bones appears to be preceded by a post-displacement of their timing in the developmental sequence, possibly due to a reduction in the overall relative size of these bones (Schoch 2002). Additionally, it has been hypothesized that within the skull, endochondral bones ossify later (Shaner 1926;Good 1995) and exhibit more variability in timing of ossification than dermal bones, and therefore may exhibit more heterochronic shifts (Smith 1997;Montero et al. 1999;Mabee et al. 2000;Sheil and Greenbaum 2005;Sánchez-Villagra et al. 2008). It is unclear if these observations are predictable patterns or even strict laws of heterochrony, and so they need to be empirically studied. ...
... Although some studies find no evidence for modularity of bone ossification in the skull (Goswami 2007;Koyabu et al. 2011), the idea that sets of skull bones belong to developmental modules is supported by common developmental origin (e.g., endochondral vs. dermal) and observations of sets of bones whose ossification appears to be linked (e.g., the facial bone series) (Hanken and Thorogood 1993;Rieppel 1994;Mabee et al. 2000;Schoch 2006;Piekarski et al. 2014). In fact, the data compiled and collected by this study supports the observation that dermal bones typically ossify before endochondral bones (Shaner 1926;Rieppel 1994;Good 1995;Abdala et al. 1997;Montero et al. 1999). The implication of modularity for studies of heterochrony is that shifts in timing of individual bones may be correlated among bones that represent discrete, developmentally-linked modules (e.g., the mandibular-, palatal-, circumorbital-, skull roof-, and neurocranial-modules; Schoch 2006). ...
... In a very general sense, there is some indication of modularity in these results, as dermal bones were generally found to begin ossification before endochondral bones (Shaner 1926;Rieppel 1994;Good 1995;Abdala et al. 1997;Montero et al. 1999), a pattern that likely is linked to their membrane versus cartilage origins, respectively. ...
The study of developmental systems may help to resolve the disagreement between morphological data and molecular data when it comes to the placement of Testudines among Amniota. Among other unique morphological adaptations, turtles possess an anapsid (unfenestrated) condition of the temporal region of the skull. If turtles are descended from diapsids, as molecular data suggests, this implies a rapid transformation of the temporal region from the diapsid condition to the anapsid condition. This study specifically addressed temporal bone heterochony among amniotes using the methods of Continuous Analysis (Germain and Laurin 2009) and Parsimov-based Genetic Inference (Harrison and Larsson 2008) to analyze cranial ossification sequences from representative taxa of all major orders of amniotes. In addition to the use of Continuous Analysis (Germain and Laurin 2009), this study recorded the internodal heterochronies reconstructed with this method. A smaller, complete dataset was analyzed by Continuous Analysis and PGi so that a direct comparison of the methods could be made. A larger dataset with missing data was also analyzed by PGi. Each analysis had three iterations for the three supported placements of Testudines within Amniota. With the data used in this study, I was also able to empirically assess the hypothesis that endochondral bones shift more often during evolution than dermal bones. Endochondral bones were not found to shift any more often than dermal bones during the course of evolution. The results of the analyses of the smaller dataset do not support any particular placement of turtles over another. However, the results of the analyses of the larger dataset support Testudines as sister to all of Diapsida.
... Accordingly, Amphisbaenia biology is poorly known and their reproductive habits stands as the most obscure aspect of their natural history. Most reports about reproduction in Amphisbaenia are restricted to the description of reproductive mode, i.e., oviparous or viviparous, and reports of embryos or eggs being found (Gans, 1978;Jared et al., 1997;Montero et. al., 1999;Webb et al., 2000;Barros-Filho and Nascimento, 2003). In most cases, the information provided is based on anedoctal and sparse observations, often included in taxonomic or more general studies (e.g., Bogert, 1964;Gans, 1966, 1 -Departamento de Zoologia, c. p. 199, Universidade Estadual Paulista, Rio Claro, SP, 13506-900, Brasil e-mail: d ...
... Similarly, the use of the egg tooth for opening the shell is also uncertain in L. infraorbitale, even though Jared et al. (1997) observed that the hatching sequence in this species starts by the opening of a small hole in the egg-shell. Montero et al. (1999) reported that the egg-tooth is absent in A. darwini heterozonata. ...
