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RBP Ch 6.Indd 144 Reproductive Biology and Phylogeny of Lizards and Tuatara CHAPTER 6 Female Reproductive Anatomy: Cloaca, Oviduct and Sperm Storage Dustin S. Siegel,1,* Aurélien Miralles,2 Justin L. Rheubert 3 and David M. Sever 4 6.1 OVERVIEW The following chapter is a review of the female reproductive anatomy of lizards. We limit our discussions to the anatomy of the cloacae, oviducts, and sperm storage receptacles in female lizards, as other chapters focus attention toward topics such as ovarian development/ovarian cycle (Ramirez-Pinilla et al. Chapter 8, this volume and placental morphology/ eggs shelling (Stewart and Blackburn Chapter 15, this volume). 1 Department of Biology, Southeast Missouri State University, Cape Girardeau, MO 63701, USA. 2 CNRS-UMR5175 CEFE, Centre d’Ecologie Functionnelle et Evolutive, 1919 route de mende, 34293 Montpellier cedex 5. 3 College of Sciences, The University of Findlay, Findlay, Ohio 45840, USA. 4 Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402, USA. * Corresponding author Female Reproductive Anatomy: Cloaca, Oviduct and Sperm Storage 145 6.2 THE CLOACA 6.2.1 Overview Few investigators have surveyed the morphology of the lizard cloaca by means of histological examination. Prominent previous studies were accomplished by Gabe and Saint-Girons (1965), Whiting (1969), Hardy and Cole (1981), Trauth et al. (1987), Sánchez-Martínez et al. (2007), Gharzi et al. (2013), and Siegel et al. (2013). As Siegel et al. (2011a) indicated in a review on the cloacal anatomy of snakes, gross examination of snake cloacae that pre-dated histological studies (e.g., Gadow 1887) confused many of the distinct cloacal regions and their orientation. Thus, we focus the majority of our review on historical literature that utilized histological examination. Although not technically lizards, details of the cloacal anatomy of Sphenodon will also be reviewed (i.e., Gabe and Saint-Girons 1964, 1965), as in depth details on the cloacal anatomy of the closest extant relative to squamates may be pertinent to the understanding of cloaca evolution in lizards (e.g., out-group comparison; see also Cree Chapter 16, this volume). Considering many historical studies provide inadequate details on the morphology of the cloaca of lizards, we examined cloacae from three individuals of Yarrow’s Spiny Lizard (Sceloporus jarrovi; collected from Cochise and Pima counties, Arizona, April, 2013; permit #M587954). Specimens were euthanased via a lethal injection of MS-222 and urogenital tracts were removed, fi xed in buffered formalin, dehydrated in ascending concentrations of ethanol, cleared in toluene, embedded in paraffin, sectioned sagittally or transversely, affi xed to albumenized slides, stained with hematoxylin and eosin for general histological examination, and examined with light microscopy. This novel collection was used to construct detailed micrographs to aid in the visualization of the female lizard cloaca, and confi rm anatomical accounts from previous assessments. 6.2.2 Sceloporus jarrovi Cloaca The vent of female Sceloporus jarrovi opens dorsally through the ventral body wall and into the proctodaeum (Fig. 6.1a). Sagittaly, the proctodaeum proceeds dorsal and slightly caudal before its dorsal extreme, at which point the proctodaeum abruptly bends cranial to a horizontal plane and then slightly ventral (Fig. 6.1a-d). Transversely, the lumen of the proctodaeum is dorso-laterally fl attened (Fig. 6.2A,B). The lumen of the proctodaeum is lined by a conspicuous stratifi ed squamous epithelium (~6 cell layers thick) with a keratinized superfi cial cell layer. A large ventral gland complex empties into the lumen of the proctodaeum cranial to the bend of the proctodaeum 146 Reproductive Biology and Phylogeny of Lizards and Tuatara Fig. 6.1 Representative sagittal sections of the cloaca of female Sceloporus jarrovi. a-e. Sections from the mid-sagittal plane of the cloaca (a) to the left periphery (e) of the cloaca (hematoxylin and eosin; scale bar [top right horizontal line] = 1,000 μm). Sections are orientated so that their left extreme represents the caudal extreme of the cloacal apparatus and the right extreme represents the cranial extreme of the cloacal apparatus. See text for description of fi gure. Amp, ampullary papilla; Aur, ampulla ureter; Aur/ur, ampulla ureter/ureter communication; Bs, bladder stalk; Int, intestine; Kd, kidney; Op, oviducal papilla; Ov, oviduct; Pr, proctodaeum; Skm, skeletal muscle; Ug, urodaeal gland; Uro, urodaeum; Us, urodaeal sphincter; Vt, vent; Wd, Wolffi an duct. Color image of this fi gure appears in the color plate section at the end of the book. Female Reproductive Anatomy: Cloaca, Oviduct and Sperm Storage 147 Fig. 6.2 Representative transverse sections from the cloaca of female Sceloporus jarrovi. Sections are organized from most caudal (A) to most cranial (H). Individual micrograph lettering represents the capital lettering on Fig. 9.1, as demonstrative of the approximate location that each representative transverse section originated (hematoxylin and eosin; scale bar = 500 μm). See text for description of fi gure. Ap, ampullary papilla; Aur, ampulla ureter; Csm, circular smooth muscle; Ep, epithelium; Kd, kidney; Lp, lamina propria; Lsm, longitudinal smooth muscle; Pr, proctodaeum; Skm, skeletal muscle; Ug, urodaeal gland; U/p, urodaeal/ proctodaeal transition; Ur, ureter; Uro, urodaeum; Vg, ventral gland; Wd, Wolffi an duct. Color image of this fi gure appears in the color plate section at the end of the book. 148 Reproductive Biology and Phylogeny of Lizards and Tuatara to a horizontal plane (Fig. 6.1a; 6.2A,B). This gland complex rests in the submucosa space of the proctodaeum between skeletal muscle and the lamina propria and is complex tubular in morphology. The epithelium lining the gland tubules is simple columnar with the cytoplasm of tubular ends of the glandular cells containing numerous eosinophilic granules (Fig. 6.2A,B). The histology of the lamina propria of the proctodaeum is consistent with that of a loose areolar connective tissue, and the dorsal projection of the proctodaeum is encompassed exteriorly by skeletal muscle (Fig. 6.1c). As the proctodaeum bends cranially, skeletal muscle dorsal to the proctodaeum terminates and is replaced by smooth muscle fi bers circulating around the cloaca (Fig. 6.2A-D). As the proctodaeum persists cranially, the dorso-ventrally fl attened appearance decreases, and internal folding of the mucosa increases and results in rugae extension into the lumen (Fig. 6.2C,D). The epithelium lining the lumen remains stratifi ed (~3 cell layers thick), however, the superfi cial cell lining transitions to cuboidal with eosinophilic epithelial cell cytoplasm. Notably, the mucosa is fi lled with simple and branched tubular glands emptying onto the surface of the epithelium (Fig. 6.1b; Fig. 6.2C,D). These glands are lined by a simple columnar epithelium with eosinophilic granules scattered in individual epithelial cell cytoplasm. At this plane of section, the cloaca is now entirely encompassed by a thick muscularis of mainly circular muscle fi bers, but also contains longitudinal fi bers dorsally and laterally (Fig. 6.2C,D). We consider this region a transitional region between the proctodaeum and urodaeum; however, the majority of the charateristics of this region are more similar to that of the urodaeum. More cranially, the lumen of the cloaca expands dramatically (Fig. 6.1a,b; Fig. 6.2E), and this expansion delineates the urodaeum proper. At this juncture of the cloaca, urodaeal mucosal glands are numerous and the epithelium lining the lumen of the urodaeum is stratifi ed (~3 cell layers thick) with a columnar superfi cial cell layer. Individual epithelial cell cytoplasm stains eosinophilic, as observed in the transition between the proctodaeum and urodaeum. A thick layer of circular smooth muscle encompasses the entire urodaeum, and a thinner layer of longitudinal smooth muscle covers the circular layer externally (Fig. 6.2E). Just cranial to the transition to the urodaeum proper, two ampullary papilla carry the ampullae ureters to the lumen of the urodaeum from a dorsolateral position (Fig. 6.1b-d; Fig. 6.2F-H). The ampullary papillae project cranially into the cloaca and, thus, the ureters and Wolffi an ducts travel caudal to their point of communication with the urodaeum (Fig. 6.2H) and then travel cranially through the ampullary papilla (Fig. 6.1b-d). Before traveling through the ampullary papillae, the ureters and Wolffi an ducts unite (Fig. 6.1d; Fig. 6.2H), forming the ampullae ureters. The lumina of the ampullae ureters and ureters are both lined by a simple and highly basophilic columnar Female Reproductive Anatomy: Cloaca, Oviduct and Sperm Storage 149 epithelium, whereas, the lumina of the Wolffi an ducts are lined by a simple cuboidal epithelium that stains eosinophilic. Immediately cranial to the communication of the ampullae ureters with the urodaeum, the distal tips of the oviducal papillae are observed, through which the oviducts communicate with the urodaeum (Fig. 6.1d; Fig. 6.3I,H). The distal extremities of the oviducal papillae are free from the wall of the urodaeum, but more cranially they are embedded in the urodaeal wall through a dorso-lateral invasion into the urodaeum (Fig. 6.1d,e; Fig. 6.3J-L). Cranial to the invasion of the oviducal papillae, the urodaeum is not bifurcated, and the lumen decreases in size dramatically (Fig. 6.3L). At this plane of section, the cloaca still possesses numerous urodaeal glands in the mucosa lining the dorsal wall of the cloaca, but not the ventral (Fig. 6.3L). More cranially, the lumen of the urodaeum decreses in size and the bladder stalk, with a simple columnar and eosinophilic epithelium, can be observed branching from the ventral wall of the urodaeum (Fig. 6.1a; Fig. 6.3M,N). Cranial to the branching of the bladder stalk, the cloaca transitions to a sphincter lined solely by circular muscle, with a very thin mucosa and no urodaeal glands (Fig.
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