Talk:Lizard Development

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Cite this page: Hill, M.A. (2021, May 15) Embryology Lizard Development. Retrieved from


Egg incubation temperature influences the growth and foraging behaviour of juvenile lizards

Behav Processes. 2019 Aug;165:9-13. doi: 10.1016/j.beproc.2019.06.003. Epub 2019 Jun 3.

Siviter H1, Deeming DC2, Wilkinson A3.

After laying their eggs, oviparous reptiles are reliant on the external environment to provide the required incubation conditions for successful embryonic development. Egg incubation temperature can impact the behaviour of various species of reptiles, but previous experiments have focused on the impact of incubation environment on hatchlings, with only a limited number of studies focussing on the longer-term behavioural consequences of incubation environment. This study investigated the effects of developmental environment on bearded dragon lizards (Pogona vitticeps) that were incubated at different temperatures within the natural range; half of them were incubated at a 'hot' temperature (30 ± 3 °C) and half at a 'cold' temperature (27 ± 3 °C). The growth and foraging behaviour of the lizards was then compared over 18 weeks of development. Although the lizards incubated at a cool temperatures grew more quickly, those incubated at the hotter temperature completed the foraging task more often and had significantly faster running speeds. These results show that egg incubation temperature impacts the foraging behaviour of juvenile lizards and suggest a potential trade-off between growth and foraging speed, which could influence an animal's life history trajectory. Copyright © 2019 Elsevier B.V. All rights reserved. KEYWORDS: Behaviour; Foraging; Growth; Incubation temperature; Lizard; Reptile PMID: 31170461 DOI: 10.1016/j.beproc.2019.06.003


Yolk sac development in lizards (Lacertilia: Scincidae): New perspectives on the egg of amniotes

J Morphol. 2017 Apr;278(4):574-591. doi: 10.1002/jmor.20656. Epub 2017 Feb 6. Stewart JR1, Thompson MB2.

Embryos of oviparous reptiles develop on the surface of a large mass of yolk, which they metabolize to become relatively large hatchlings. Access to the yolk is provided by tissues growing outward from the embryo to cover the surface of the yolk. A key feature of yolk sac development is a dedicated blood vascular system to communicate with the embryo. The best known model for yolk sac development and function of oviparous amniotes is based on numerous studies of birds, primarily domestic chickens. In this model, the vascular yolk sac forms the perimeter of the large yolk mass and is lined by a specialized epithelium, which takes up, processes and transports yolk nutrients to the yolk sac blood vessels. Studies of lizard yolk sac development, dating to more than 100 years ago, report characteristics inconsistent with this model. We compared development of the yolk sac from oviposition to near hatching in embryonic series of three species of oviparous scincid lizards to consider congruence with the pattern described for birds. Our findings reinforce results of prior studies indicating that squamate reptiles mobilize and metabolize the large yolk reserves in their eggs through a process unknown in other amniotes. Development of the yolk sac of lizards differs from birds in four primary characteristics, migration of mesoderm, proliferation of endoderm, vascular development and cellular diversity within the yolk sac cavity. Notably, all of the yolk is incorporated into cells relatively early in development and endodermal cells within the yolk sac cavity align along blood vessels which course throughout the yolk sac cavity. The pattern of uptake of yolk by endodermal cells indicates that the mechanism of yolk metabolism differs between lizards and birds and that the evolution of a fundamental characteristic of embryonic nutrition diverged in these two lineages. Attributes of the yolk sac of squamates reveal the existence of phylogenetic diversity among amniote lineages and raise new questions concerning the evolution of the amniotic egg. J. Morphol. 278:574-591, 2017. © 2017 Wiley Periodicals, Inc. KEYWORDS: embryonic nutrition; oviparity; vascular development PMID: 28168721 DOI: 10.1002/jmor.20656


Development of the hearts of lizards and snakes and perspectives to cardiac evolution

PLoS One. 2013 Jun 5;8(6):e63651. doi: 10.1371/journal.pone.0063651. Print 2013.

Jensen B, van den Berg G, van den Doel R, Oostra RJ, Wang T, Moorman AF. Source Department of Bioscience - Zoophysiology, Aarhus University, Aarhus, Denmark ; Department of Anatomy, Embryology & Physiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.


Birds and mammals both developed high performance hearts from a heart that must have been reptile-like and the hearts of extant reptiles have an unmatched variability in design. Yet, studies on cardiac development in reptiles are largely old and further studies are much needed as reptiles are starting to become used in molecular studies. We studied the growth of cardiac compartments and changes in morphology principally in the model organism corn snake (Pantherophis guttatus), but also in the genotyped anole (Anolis carolinenis and A. sagrei) and the Philippine sailfin lizard (Hydrosaurus pustulatus). Structures and chambers of the formed heart were traced back in development and annotated in interactive 3D pdfs. In the corn snake, we found that the ventricle and atria grow exponentially, whereas the myocardial volumes of the atrioventricular canal and the muscular outflow tract are stable. Ventricular development occurs, as in other amniotes, by an early growth at the outer curvature and later, and in parallel, by incorporation of the muscular outflow tract. With the exception of the late completion of the atrial septum, the adult design of the squamate heart is essentially reached halfway through development. This design strongly resembles the developing hearts of human, mouse and chicken around the time of initial ventricular septation. Subsequent to this stage, and in contrast to the squamates, hearts of endothermic vertebrates completely septate their ventricles, develop an insulating atrioventricular plane, shift and expand their atrioventricular canal toward the right and incorporate the systemic and pulmonary venous myocardium into the atria.

PMID 23755108


Identifying the evolutionary building blocks of the cardiac conduction system

PLoS One. 2012;7(9):e44231. doi: 10.1371/journal.pone.0044231. Epub 2012 Sep 11.

Jensen B, Boukens BJ, Postma AV, Gunst QD, van den Hoff MJ, Moorman AF, Wang T, Christoffels VM. Source Department of Anatomy, Embryology & Physiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.


The endothermic state of mammals and birds requires high heart rates to accommodate the high rates of oxygen consumption. These high heart rates are driven by very similar conduction systems consisting of an atrioventricular node that slows the electrical impulse and a His-Purkinje system that efficiently activates the ventricular chambers. While ectothermic vertebrates have similar contraction patterns, they do not possess anatomical evidence for a conduction system. This lack amongst extant ectotherms is surprising because mammals and birds evolved independently from reptile-like ancestors. Using conserved genetic markers, we found that the conduction system design of lizard (Anolis carolinensis and A. sagrei), frog (Xenopus laevis) and zebrafish (Danio rerio) adults is strikingly similar to that of embryos of mammals (mouse Mus musculus, and man) and chicken (Gallus gallus). Thus, in ectothermic adults, the slow conducting atrioventricular canal muscle is present, no fibrous insulating plane is formed, and the spongy ventricle serves the dual purpose of conduction and contraction. Optical mapping showed base-to-apex activation of the ventricles of the ectothermic animals, similar to the activation pattern of mammalian and avian embryonic ventricles and to the His-Purkinje systems of the formed hearts. Mammalian and avian ventricles uniquely develop thick compact walls and septum and, hence, form a discrete ventricular conduction system from the embryonic spongy ventricle. Our study uncovers the evolutionary building plan of heart and indicates that the building blocks of the conduction system of adult ectothermic vertebrates and embryos of endotherms are similar.

PMID 22984480

Tooth development in a model reptile: functional and null generation teeth in the gecko Paroedura picta

J Anat. 2012 Sep;221(3):195-208. doi: 10.1111/j.1469-7580.2012.01531.x. Epub 2012 Jul 11.

Zahradnicek O, Horacek I, Tucker AS. Source Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic.


This paper describes tooth development in a basal squamate, Paroedura picta. Due to its reproductive strategy, mode of development and position within the reptiles, this gecko represents an excellent model organism for the study of reptile development. Here we document the dental pattern and development of non-functional (null generation) and functional generations of teeth during embryonic development. Tooth development is followed from initiation to cytodifferentiation and ankylosis, as the tooth germs develop from bud, through cap to bell stages. The fate of the single generation of non-functional (null generation) teeth is shown to be variable, with some teeth being expelled from the oral cavity, while others are incorporated into the functional bone and teeth, or are absorbed. Fate appears to depend on the initiation site within the oral cavity, with the first null generation teeth forming before formation of the dental lamina. We show evidence for a stratum intermedium layer in the enamel epithelium of functional teeth and show that the bicuspid shape of the teeth is created by asymmetrical deposition of enamel, and not by folding of the inner dental epithelium as observed in mammals. © 2012 The Authors. Journal of Anatomy © 2012 Anatomical Society.

PMID 22780101


Patterns of interspecific variation in the heart rates of embryonic reptiles

PLoS One. 2011;6(12):e29027. Epub 2011 Dec 13.

Du WG, Ye H, Zhao B, Pizzatto L, Ji X, Shine R. Source Key Laboratory of Animal Ecology and Conservational Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.


New non-invasive technologies allow direct measurement of heart rates (and thus, developmental rates) of embryos. We applied these methods to a diverse array of oviparous reptiles (24 species of lizards, 18 snakes, 11 turtles, 1 crocodilian), to identify general influences on cardiac rates during embryogenesis. Heart rates increased with ambient temperature in all lineages, but (at the same temperature) were faster in lizards and turtles than in snakes and crocodilians. We analysed these data within a phylogenetic framework. Embryonic heart rates were faster in species with smaller adult sizes, smaller egg sizes, and shorter incubation periods. Phylogenetic changes in heart rates were negatively correlated with concurrent changes in adult body mass and residual incubation period among the lizards, snakes (especially within pythons) and crocodilians. The total number of embryonic heart beats between oviposition and hatching was lower in squamates than in turtles or the crocodilian. Within squamates, embryonic iguanians and gekkonids required more heartbeats to complete development than did embryos of the other squamate families that we tested. These differences plausibly reflect phylogenetic divergence in the proportion of embryogenesis completed before versus after laying.

PMID 22174948

Sex differences in sand lizard telomere inheritance: paternal epigenetic effects increases telomere heritability and offspring survival

PLoS One. 2011 Apr 22;6(4):e17473.

Olsson M, Pauliny A, Wapstra E, Uller T, Schwartz T, Blomqvist D. Source School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia.


BACKGROUND: To date, the only estimate of the heritability of telomere length in wild populations comes from humans. Thus, there is a need for analysis of natural populations with respect to how telomeres evolve. METHODOLOGY/PRINCIPAL FINDINGS: Here, we show that telomere length is heritable in free-ranging sand lizards, Lacerta agilis. More importantly, heritability estimates analysed within, and contrasted between, the sexes are markedly different; son-sire heritability is much higher relative to daughter-dam heritability. We assess the effect of paternal age on Telomere Length (TL) and show that in this species, paternal age at conception is the best predictor of TL in sons. Neither paternal age per se at blood sampling for telomere screening, nor corresponding age in sons impact TL in sons. Processes maintaining telomere length are also associated with negative fitness effects, most notably by increasing the risk of cancer and show variation across different categories of individuals (e.g. males vs. females). We therefore tested whether TL influences offspring survival in their first year of life. Indeed such effects were present and independent of sex-biased offspring mortality and offspring malformations. CONCLUSIONS/SIGNIFICANCE: TL show differences in sex-specific heritability with implications for differences between the sexes with respect to ongoing telomere selection. Paternal age influences the length of telomeres in sons and longer telomeres enhance offspring survival. PMID 21526170

Reptilian spermatogenesis: A histological and ultrastructural perspective

Spermatogenesis. 2011 Jul;1(3):250-269. Epub 2011 Jul 1.

Gribbins KM. Source Department of Biology; Wittenberg University; Springfield, OH USA.


Until recently, the histology and ultrastructural events of spermatogenesis in reptiles were relatively unknown. Most of the available morphological information focuses on specific stages of spermatogenesis, spermiogenesis, and/or of the mature spermatozoa. No study to date has provided complete ultrastructural information on the early events of spermatogenesis, proliferation and meiosis in class Reptilia. Furthermore, no comprehensive data set exists that describes the ultrastructure of the entire ontogenic progression of germ cells through the phases of reptilian spermatogenesis (mitosis, meiosis and spermiogenesis). The purpose of this review is to provide an ultrastructural and histological atlas of spermatogenesis in reptiles. The morphological details provided here are the first of their kind and can hopefully provide histological information on spermatogenesis that can be compared to that already known for anamniotes (fish and amphibians), birds and mammals. The data supplied in this review will provide a basic model that can be utilized for the study of sperm development in other reptiles. The use of such an atlas will hopefully stimulate more interest in collecting histological and ultrastructural data sets on spermatogenesis that may play important roles in future nontraditional phylogenetic analyses and histopathological studies in reptiles.

PMID 22319673


PMID 19645023

Table 1. Summary of embryonic staging data available for squamates
Species Embryonic series covered Source
Agama impalearis Pre- and post-oviposition Mouden et al. (2000)
Calotes versicolor Post-oviposition Muthukkaruppan et al. (1970)
Pre-oviposition Thapliyal et al. (1973)
Chamaeleo lateralis Pre- and post-oviposition Blanc (1974)
Chamaeleo bitaeniatus Post-oviposition Pasteels (1956)
Post-oviposition Milaire (1957)
Anolis sagrei Pre- and post-oviposition Sanger et al. (2008b)
Liolaemus t. tenuis Pre-oviposition Lemus and Duvauchelle (1966)
Post-oviposition Lemus et al. (1981)
Liolaemus gravenhorstii Pre- and post-oviposition Lemus (1967)
Lacerta viridis Post-oviposition Dhouailly and Saxod (1974)
Podarcis (Lacerta) agilis Pre- and post-oviposition Peter (1904)
Post-oviposition Rieppel (1994)
Podarcis (Lacerta) muralis Post-oviposition Dhouailly and Saxod (1974)
Podarcis (Lacerta) vivipara Intra-uterine Dufaure and Hubert (1961)
Mabuya megalura Intra-uterine Pasteels (1956)
Anguis fragilis Cleavage Nicolas (1904)
Gastrulation and neurulation Ballowitz (1905)
Neurulation to closure of the amnion Meyer (1910)
Python sebae Post-oviposition Boughner et al. (2007)
Natrix natrix Uncertain Krull (1906)
Uncertain Vielhaus (1907)
Natrix tesselata Uncertain Korneva (1969)
Thamnophis s. sirtalis Intra-uterine Zehr (1962)
Naja kaouthia Post-oviposition Jackson (2002)
Vipera aspis Intra-uterine Hubert and Dufaure (1968)
Hemiergis spp. Intra-uterine (incomplete coverage) Shapiro (2002)
Hemidactylus turcicus Post-oviposition (incomplete coverage) Werner (1971)
Paroedura picta Post-oviposition Noro et al. (2009)
Ptyodactylus hasselquistii guttatus Post-oviposition (incomplete coverage) Werner (1971)
Sphaerodactylus argus Post-oviposition (incomplete coverage) Werner (1971)