A staging table of embryonic development for a viviparous (live-bearing) lizard Eremias multiocellata (Squamata: Lacertidae)
Zhaocun Lin
A # , Kaiming Yu A # , Leyao Shen A , Yu Zhang B , Yutian Liu C , Mei Hou A , Zhennan Peng A , Xiaolong Tang A * and Qiang Chen A
+ Author Affiliations
- Author Affiliations
A Institute of Biochemistry and Molecular Biology, School of Life Science, Lanzhou University, 222 Tianshui South Road, Lanzhou 730000, China.
B School of Medicine, Tsinghua University, Beijing, China.
C College of Life Science, Shaanxi Normal University, Xi’an, China.
* Correspondence to: tangxl@lzu.edu.cn
# These authors contributed equally to this paper
Handling Editor: Andrew Pask
Reproduction, Fertility and Development 33(14) 782-797 https://doi.org/10.1071/RD21082
Published online: 19 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
As the only viviparous reptile in China that has both temperature-dependent sex determination (TSD) and genetic-dependent sex determination (GSD) mechanisms, Eremias multiocellata is considered as an ideal species for studying the sex determination mechanism in viviparous lizards. However, studies on embryonic stage of viviparous lizards and morphological characteristics of each stage are limited. In the present study, the embryonic development process of E. multiocellata is divided into 15 stages (stages 28–42) according to the morphology of embryos. Embryos sizes are measured and continuous dynamic variation of some key features, including limbs, genitals, eyes, pigments, and brain scales are color imaged by a stereoscopic microscope. Furthermore, based on these morphological characteristics, we compare the similarities and differences in the embryonic development of E. multiocellata with other squamate species. Our results not only identified the staging table of E. multiocellata with continuous changes of external morphological characteristics but also developed a staging scheme for an important model species that provides a necessary foundation for study of sex determination in a viviparous lizard.
Keywords: amniotic animals, developmental stages, embryos, Eremias multiocellata, morphological characteristics, reptile, temperature-dependent sex determination, viviparity.
References
Andrews, RM, Brandley, MC, and Greene, VW (2013). Developmental sequences of squamate reptiles are taxon specific. Evolution & Development 15, 326–343.| Developmental sequences of squamate reptiles are taxon specific.Crossref | GoogleScholarGoogle Scholar |
Davidson, D (1989). The house mouse: atlas of embryonic development. By K. Theiler. Second printing, 1989. New York: Springer-Verlag. 178 pages. DM 168.00. ISBN 3 540059407. Genetics Research 54, 240–241.
| The house mouse: atlas of embryonic development. By K. Theiler. Second printing, 1989. New York: Springer-Verlag. 178 pages. DM 168.00. ISBN 3 540059407.Crossref | GoogleScholarGoogle Scholar |
de Queiroz, K (1982). The scleral ossicles of sceloporine iguanids: a reexamination with comments on their phylogenetic significance. Herpetologica 38, 302–311.
Duench, K, and Franz-Odendaal, TA (2012). BMP and Hedgehog signaling during the development of scleral ossicles. Developmental Biology 365, 251–258.
| BMP and Hedgehog signaling during the development of scleral ossicles.Crossref | GoogleScholarGoogle Scholar | 22370003PubMed |
Dufaure, J, and Hubert, J (1961). Zootocavivipara Jacquin Archives d’Anatomie Microscopique et de Morphologie Expérimentale 50, 309–328.
El Mouden, E, Bons, J, Pieau, C, Renous, S, Znari, M, and Boumezzough, A (2000). Table de développement embryonnaire d’un lézard agamidé, Agama impalearis Boettger, 1874. Annales des Sciences Naturelles - Zoologie et Biologie Animale 21, 93–115.
| Table de développement embryonnaire d’un lézard agamidé, Agama impalearis Boettger, 1874.Crossref | GoogleScholarGoogle Scholar |
Ferrandino, I, and Grimaldi, MC (2004). Immunohistochemical study of adenohypophysial cells during embryonic development in the reptile Chalcides chalcides (Squamata, Scincidae). Journal of Molecular Histology 35, 55–61.
| Immunohistochemical study of adenohypophysial cells during embryonic development in the reptile Chalcides chalcides (Squamata, Scincidae).Crossref | GoogleScholarGoogle Scholar | 15323349PubMed |
Franz-Odendaal, TA (2006). Intramembranous ossification of scleral ossicles in Chelydra serpentina. Zoology 109, 75–81.
| Intramembranous ossification of scleral ossicles in Chelydra serpentina.Crossref | GoogleScholarGoogle Scholar | 16377163PubMed |
Fyfe, DM, and Hall, BK (1981). A scanning electron microscopic study of the developing epithelial scleral papillae in the eye of the embryonic chick. Journal of Morphology 167, 201–209.
| A scanning electron microscopic study of the developing epithelial scleral papillae in the eye of the embryonic chick.Crossref | GoogleScholarGoogle Scholar | 7241598PubMed |
Gao, W, Sun, Y-B, Zhou, W-W, Xiong, Z-J, Chen, L, Li, H, Fu, T-T, Xu, K, Xu, W, Ma, L, Chen, Y-J, Xiang, X-Y, Zhou, L, Zeng, T, Zhang, S, Jin, J-Q, Chen, H-M, Zhang, G, Hillis, DM, Ji, X, Zhang, Y-P, and Che, J (2019). Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity. Proceedings of the National Academy of Sciences of the United States of America 116, 3646–3655.
| Genomic and transcriptomic investigations of the evolutionary transition from oviparity to viviparity.Crossref | GoogleScholarGoogle Scholar | 30808754PubMed |
Gredler, ML, Sanger, TJ, and Cohn, MJ (2015). Development of the cloaca, hemipenes, and hemiclitores in the green anole, Anolis carolinensis. Sexual Development 9, 21–33.
| Development of the cloaca, hemipenes, and hemiclitores in the green anole, Anolis carolinensis.Crossref | GoogleScholarGoogle Scholar | 24960313PubMed |
Gregorovicova, M, Zahradnicek, O, Tucker, AS, Velensky, P, and Horacek, I (2012). Embryonic development of the monitor lizard, Varanus indicus. Amphibia-Reptilia 33, 451–468.
| Embryonic development of the monitor lizard, Varanus indicus.Crossref | GoogleScholarGoogle Scholar |
Guerra-Fuentes, RA, Daza, JD, and Bauer, AM (2014). The embryology of the retinal pigmented epithelium in dwarf geckos (Gekkota: Sphaerodactylinae): a unique developmental pattern. BMC Developmental Biology 14, 29.
| The embryology of the retinal pigmented epithelium in dwarf geckos (Gekkota: Sphaerodactylinae): a unique developmental pattern.Crossref | GoogleScholarGoogle Scholar | 24974837PubMed |
Hall, BK (1981). Specificity in the differentiation and morphogenesis of neural crest-derived scleral ossicles and of epithelial scleral papillae in the eye of the embryonic chick. Development 66, 175–190.
| Specificity in the differentiation and morphogenesis of neural crest-derived scleral ossicles and of epithelial scleral papillae in the eye of the embryonic chick.Crossref | GoogleScholarGoogle Scholar |
Hamburger, V, and Hamilton, HL (1951). A series of normal stages in the development of the chick embryo. Journal of Morphology 88, 49–92.
| 24539719PubMed |
Hamburger, V, and Hamilton, HL (1992). A series of normal stages in the development of the chick embryo. Developmental Dynamics 195, 231–272.
| A series of normal stages in the development of the chick embryo.Crossref | GoogleScholarGoogle Scholar | 1304821PubMed |
Hopwood, N (2007). A history of normal plates, tables and stages in vertebrate embryology. The International Journal of Developmental Biology 51, 1–26.
| A history of normal plates, tables and stages in vertebrate embryology.Crossref | GoogleScholarGoogle Scholar | 17183461PubMed |
Khannoon, ER (2015). Developmental stages of the climbing gecko Tarentola annularis with special reference to the claws, pad lamellae, and subdigital setae. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 324, 450–464.
| Developmental stages of the climbing gecko Tarentola annularis with special reference to the claws, pad lamellae, and subdigital setae.Crossref | GoogleScholarGoogle Scholar |
Kimmel, CB, Ballard, WW, Kimmel, SR, Ullmann, B, and Schilling, TF (1995). Stages of embryonic development of the zebrafish. Developmental Dynamics 203, 253–310.
| Stages of embryonic development of the zebrafish.Crossref | GoogleScholarGoogle Scholar | 8589427PubMed |
Lemus, D (1967). Contribution to the study of embryology in Chilean reptiles. II. Table of development of the viviparous lizard Liolaemus gravenhorti (Reptilia-Squamata-Iguanidae). Biologica 40, 39–61.
| 5627967PubMed |
Lemus, D, Illanes, J, Fuenzalida, M, De La Vega, YP, and Garcia, M (1981). Comparative analysis of the development of the lizard, Liolaemus tenuis tenuis. II. A series of normal postlaying stages in embryonic development. Journal of Morphology 169, 337–349.
| Comparative analysis of the development of the lizard, Liolaemus tenuis tenuis. II. A series of normal postlaying stages in embryonic development.Crossref | GoogleScholarGoogle Scholar | 30111005PubMed |
Murakami, A, Hasegawa, M, and Kuriyama, T (2018). Developmental mechanisms of longitudinal stripes in the Japanese four‐lined snake. Journal of Morphology 279, 27–36.
| Developmental mechanisms of longitudinal stripes in the Japanese four‐lined snake.Crossref | GoogleScholarGoogle Scholar | 28922458PubMed |
Muthukkaruppan, VR, Kanakambika, P, Manickavel, V, and Veeraraghavan, K (1970). Analysis of the development of the lizard, Calotes versicolor. I. A series of normal stages in the embryonic development. Journal of Morphology 130, 479–489.
| Analysis of the development of the lizard, Calotes versicolor. I. A series of normal stages in the embryonic development.Crossref | GoogleScholarGoogle Scholar |
Neaves, L, Wapstra, E, Birch, D, Girling, JE, and Joss, JM (2006). Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus. Journal of Experimental Zoology Part A Comparative Experimental Biology 305, 74–82.
| Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus.Crossref | GoogleScholarGoogle Scholar |
Noro, M, Uejima, A, Abe, G, Manabe, M, and Tamura, K (2009). Normal developmental stages of the Madagascar ground gecko Paroedura pictus with special reference to limb morphogenesis. Developmental Dynamics 238, 100–109.
| Normal developmental stages of the Madagascar ground gecko Paroedura pictus with special reference to limb morphogenesis.Crossref | GoogleScholarGoogle Scholar | 19097047PubMed |
Pinto, CB, and Hall, BK (1991). Toward an understanding of the epithelial requirement for osteogenesis in scleral mesenchyme of the embryonic chick. Journal of Experimental Zoology 259, 92–108.
| Toward an understanding of the epithelial requirement for osteogenesis in scleral mesenchyme of the embryonic chick.Crossref | GoogleScholarGoogle Scholar |
Pyron, RA, and Burbrink, FT (2014). Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecology Letters 17, 13–21.
| Early origin of viviparity and multiple reversions to oviparity in squamate reptiles.Crossref | GoogleScholarGoogle Scholar | 23953272PubMed |
Rapp Py-Daniel, T, Kennedy Soares De-Lima, A, Campos Lima, F, Pic-Taylor, A, Rodrigues Pires Junior, O, and Sebben, A (2017). A staging table of post‐ovipositional development for the South American collared lizard Tropidurus torquatus (Squamata: Tropiduridae). The Anatomical Record 300, 277–290.
| A staging table of post‐ovipositional development for the South American collared lizard Tropidurus torquatus (Squamata: Tropiduridae).Crossref | GoogleScholarGoogle Scholar | 27741560PubMed |
Raynaud A, Pieau C (1985) Embryonic development of the genital system. In ‘Biology of the reptilia. Vol. 15’. (Eds Gans C, Billett F) pp. 149–300. (John Wiley and Sons: New York, NY, USA)
Sanger, TJ, Losos, JB, and Gibson‐Brown, JJ (2008). A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. Journal of Morphology 269, 129–137.
| A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology.Crossref | GoogleScholarGoogle Scholar | 17724661PubMed |
Tang, X-L, Yue, F, Yan, X-F, Zhang, D-J, Xin, Y, Wang, C, and Chen, Q (2012). Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude. Journal of Thermal Biology 37, 438–444.
| Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude.Crossref | GoogleScholarGoogle Scholar |
Wald G (1944) ‘The vertebrate eye and its adaptive radiation’. (JSTOR: New York, NY, USA)
Wang, C, Tang, X, Xin, Y, Yue, F, Yan, X, Liu, B, An, B, Wang, X, and Chen, Q (2015). Identification of sex chromosomes by means of comparative genomic hybridization in a lizard, Eremias multiocellata. Zoological Science 32, 151–156.
| Identification of sex chromosomes by means of comparative genomic hybridization in a lizard, Eremias multiocellata.Crossref | GoogleScholarGoogle Scholar | 25826063PubMed |
Wang, Y, Zeng, Z-G, Li, S-R, Bi, J-H, and Du, W-G (2016). Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction. Oecologia 182, 961–971.
| Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction.Crossref | GoogleScholarGoogle Scholar | 27638182PubMed |
Werneburg, I (2009). A standard system to study vertebrate embryos. PLoS One 4, e5887.
| A standard system to study vertebrate embryos.Crossref | GoogleScholarGoogle Scholar | 19521537PubMed |
Wise, PAD, Vickaryous, MK, and Russell, AP (2009). An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko. The Anatomical Record 292, 1198–1212.
| An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko.Crossref | GoogleScholarGoogle Scholar |
Yan, X-F, Tang, X-L, Yue, F, Zhang, D-J, Xin, Y, Wang, C, and Chen, Q (2011). Influence of ambient temperature on maternal thermoregulation and neonate phenotypes in a viviparous lizard, Eremias multiocellata, during the gestation period. Journal of Thermal Biology 36, 187–192.
| Influence of ambient temperature on maternal thermoregulation and neonate phenotypes in a viviparous lizard, Eremias multiocellata, during the gestation period.Crossref | GoogleScholarGoogle Scholar |
Yanes, C, Batista, MAP, Trujillo, JMM, Monzon, M, and Marrero, A (1987). Anterior dorsal ventricular ridge in the lizard: embryonic development. Journal of Morphology 194, 55–64.
| Anterior dorsal ventricular ridge in the lizard: embryonic development.Crossref | GoogleScholarGoogle Scholar | 29898567PubMed |
Zhang, D-J, Tang, X-L, Yue, F, Chen, Z, Chen, Q, Li, R-D, and Chen, Q (2010). Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata. Journal of Thermal Biology 35, 129–133.
| Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata.Crossref | GoogleScholarGoogle Scholar |
Zhao E-M, Adler K (1993) ‘Herpetology of China’. (Society for the Study of Amphibians and Reptiles: Oxford, OH, USA)
