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Embryonic Development of the Fossorial Gymnophthalmid Lizards Nothobachia

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Embryonic Development of the Fossorial Gymnophthalmid Lizards Nothobachia Zoology 115 (2012) 302–318 Contents lists available at SciVerse ScienceDirect Zoology jour nal homepage: www.elsevier.com/locate/zool Embryonic development of the fossorial gymnophthalmid lizards Nothobachia ablephara and Calyptommatus sinebrachiatus ∗ Juliana G. Roscito , Miguel T. Rodrigues Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Cidade Universitária, Rua do Matão, Trav. 14, no. 321, São Paulo, SP, CEP 05508-090, Brazil a r t i c l e i n f o a b s t r a c t Article history: The evolutionary history of the lizard family Gymnophthalmidae is characterized by several independent Received 7 December 2011 events of morphological modifications to a snake-like body plan, such as limb reduction, body elongation, Received in revised form 19 March 2012 loss of external ear openings, and modifications in skull bones, as adaptive responses to a burrowing and Accepted 20 March 2012 fossorial lifestyle. The origins of such morphological modifications from an ancestral lizard-like condition can be traced back to evolutionary changes in the developmental processes that coordinate the building Keywords: of the organism. Thus, the characterization of the embryonic development of gymnophthalmid lizards is Gymnophthalmidae an essential step because it lays the foundation for future studies aiming to understand the exact nature Lizards of these changes and the developmental mechanisms that could have been responsible for the evolution Fossorial lifestyle of a serpentiform (snake-like) from a lacertiform (lizard-like) body form. Here we describe the post- Limb reduction Staging system ovipositional embryonic development of the fossorial species Nothobachia ablephara and Calyptommatus sinebrachiatus, presenting a detailed staging system for each one, with special focus on the development of the reduced limbs, and comparing their development to that of other lizard species. The data provided by the staging series are essential for future experimental studies addressing the genetic basis of the evolutionary and developmental variation of the Gymnophthalmidae. © 2012 Elsevier GmbH. All rights reserved. 1. Introduction lacertiform genera Tretioscincus, Micrablepharus, Gymnophthalmus, Procellosaurinus, Vanzosaura and Psilophthalmus are lizard-like in Squamata is one of the most diverse groups among vertebrates, shape, have a tail that is longer than the body, and have well devel- comprising approximately 9500 species including lizards, snakes, oped limbs and digits, with 5 or 4 digits in the forelimb (the three amphisbaenians, turtles, crocodiles, and tuatara (Uetz, 2012) dis- former genera have 5 digits while the three latter have 4) and 5 dig- tributed along a wide range of habitats and niches (Vitt et al., 2003). its in the hindlimb. Nothobachia, Scriptosaura and Calyptommatus A common trait among squamate reptiles is the repeated evolution are fossorial and psammophilic (adapted to life on sand) and show of a snake-like morphology in distantly related groups (Wiens et al., morphological features related to this lifestyle, such as loss of exter- 2006; Brandley et al., 2008; Skinner et al., 2008), involving mor- nal ear openings, an elongated body, and reduced or absent limbs. phological changes associated with body elongation and with the Nothobachia has a styliform forelimb and a small hindlimb with 2 reduction or the complete loss of limbs. Such an evolutionary pat- digits, and Scriptosaura and Calytpommatus have no forelimbs and tern is clearly seen in the lizard group Gymnophthalmidae (Estes the hindlimb is styliform. et al., 1988), which is characterized by the convergent occurrence The origins of such morphological modifications that charac- of morphological adaptations to a fossorial lifestyle, such as reduc- terize the evolutionary history of the Gymnophthalmini can best tion and/or loss of limbs, body elongation, and loss of external ear be understood by studying the embryonic development of these openings. species, since changes in the developmental processes that coordi- The Gymnophthalmini, a monophyletic group of nine genera nate the patterning and growth of the embryos are the main sources (Rodrigues, 1991; Pellegrino et al., 2001; Rodrigues and dos Santos, of evolutionary variation in phenotypes (Raff, 2000). 2008; Rodrigues et al., 2009) within the Gymnophthalmidae, is The knowledge of how development is organized is fundamental one of the groups in which the evolutionary transition from a for understanding the causes underlying variation in the devel- lizard-like to a snake-like morphology is clearly recognizable. The opmental processes. Thus, detailed descriptions of the phases of embryonic development are essential references for evolutionary and developmental studies aiming to address how development ∗ evolves and how evolutionary processes are driven by changes in Corresponding author. E-mail address: [email protected] (J.G. Roscito). development. 0944-2006/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2012.03.003 J.G. Roscito, M.T. Rodrigues / Zoology 115 (2012) 302–318 303 Developmental biologists are more familiar with embryonic maintained in small rounded plastic boxes (20 cm diameter, 8 cm staging tables of vertebrates such as the chicken Gallus gal- high) containing slightly moist fine sand. Immediately after ovipo- lus (Hamburger and Hamilton, 1951), the frog Xenopus laevis sition, clutches were transferred to and maintained in photographic (Nieuwkoop and Faber, 1967), the fish Danio rerio (Kimmel et al., film tubes with moist sand to prevent drying, at environmental ◦ 1995), and the mouse Mus musculus (Kaufman, 1992), and to a lesser temperatures (28–35 C). As in all gymnophthalmids, clutch size degree, those of Eleutherodactylus coqui (Townsend and Stewart, was invariably two eggs (Rodrigues, 1991). Females were released 1985), Ambystoma mexicanum (Schreckenberg and Jacobson, back to the field after egg laying. 1975), and the medaka fish Oryzias latipes (Iwamatsu, 2004), for 52 eggs of C. sinebrachiatus and 13 eggs of N. ablephara were example. obtained and were opened at regular intervals throughout devel- As for turtles, lizards, and snakes, descriptions of embry- opment, which lasts approximately 45 days from oviposition to onic development are widespread in the literature (Dufaure and hatching in both species. The ontogenetic series of C. sinebrachia- Hubert, 1961; Zehr, 1962; Dhouailly and Saxod, 1974; Bellairs tus consists of two embryos representing each day of development, and Kamal, 1981; Guyot et al., 1994; Rieppel, 1992, 1994; el from the second day after laying up to the 34th day, and two older Mouden et al., 2000; Jackson, 2002; Shapiro, 2002; Greenbaum, embryos representing the pre-hatching stage. For N. ablephara, the 2002; Boughner et al., 2007; Sanger et al., 2008; Noro et al., 2009; ontogenetic series is distributed with two-day intervals through- Wise et al., 2009; Boback et al., 2012; among others) and pro- out development, from the second day after egg laying up to the vide valuable information on the ontogeny of these species. Also, 26th day, with only one embryo for each stage. These intervals over the last years a few studies addressing the regulation of were chosen in order to be able to observe early organogenesis, some aspects of developmental processes of lizards and snakes which is the period where most features are appearing or rapidly (Raynaud et al., 1998; Cohn and Tickle, 1999; Shapiro et al., 2003; changing shape; later on in development, growth is the dominant Gomez et al., 2008; Vonk and Richardson, 2008; Vonk et al., 2008) process (Andrews, 2004). Developmental time, measured in days, have enriched the knowledge on the evolution of the processes was counted from the moment of egg laying. involved in the formation of new body forms within squamate Embryos were removed from the egg, carefully dissected from groups. However, the data available is still unsatisfactory consider- the embryonic membranes and fixed immediately in 100% ethanol ing the diversity of forms and habitats occupied, and the adaptive or 10% neutral-buffered formalin; after a week, the fixed embryos responses in body form, reproduction, locomotion, physiology and were transferred to 70% ethanol. behavior. The material was examined with an Olympus SZX12 stereomi- Given the evolutionary history of the Gymnophthalmini and croscope (Olympus, Tokyo, Japan), and digital pictures were taken their well-established phylogenetic relationships (see Pellegrino with a digital camera attached to it. et al., 2001; Castoe et al., 2004; but for further discussion on the relationships within the gymnophthalmids, see Castoe et al., 2004; 2.1. Staging criteria Rodrigues et al., 2007, 2009), the group has the potential to become a good model for researchers aiming to comprehend the variation The phases of development were determined based on key diag- in developmental pathways that could have led to the modifica- nostic features of external morphology, such as those defined by tion of a lacertiform to a serpentiform body form. Therefore, in this the Standard Event System (SES; Werneburg, 2009); this system paper we present a detailed description of the post-ovipositional establishes morphological criteria for staging embryos and facili- embryonic development of Nothobachia ablephara and of Calyptom- tates comparisons between taxa, allowing more reliable analysis matus sinebrachiatus, and thus establish a working ground for future of variation of developmental
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