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The Sexual Segment of Hemidactylus Turcicus and the Evolution of Sexual Segment Location in Squamata

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The Sexual Segment of Hemidactylus Turcicus and the Evolution of Sexual Segment Location in Squamata JOURNAL OF MORPHOLOGY 272:802–813 (2011) The Sexual Segment of Hemidactylus turcicus and the Evolution of Sexual Segment Location in Squamata Justin L. Rheubert,1* Christopher M. Murray,1 Dustin S. Siegel,1,2 Johnathan Babin,1 and David M. Sever1 1Department of Biological Sciences, Southeastern Louisiana University, SLU 10736, Hammond, Louisiana 70402 2Department of Biological Sciences, Saint Louis University, St. Louis, Missouri 63103 ABSTRACT The kidneys of the Mediterranean Gecko, snake, Natrix natrix, and termed the ‘‘segment Hemidactylus turcicus (Gekkonidae), were investigated sexuel’’ by Regaud and Policard (1903), who noted using light and electron microscopy with the primary focus the SSK occurred only in male snakes. Subse- placed on morphology of the sexual segment of the kidney. quently, the SSK has been found in the kidney The nephrons of male H. turcicus are composed of five dis- ducts of all male snakes and lizards (Squamata) tinct regions: 1) a renal corpuscle and glomerulus, 2) a proxi- mal convoluted tubule, 3) an intermediate segment, 4) a that have been examined and is considered a sec- distal convoluted tubule, and 5) the sexual segment of the ondary sexual characteristic (reviews by Saint kidney/collecting duct. Female H. turcicus is similar but Girons, 1972; Fox, 1977; Aldridge et al., in press). lack a sexual segment of the kidney. The sexual segment of Research has been conducted investigating the the kidney is hypertrophied during the months of March morphology and physiology of the sexual segment through August, which corroborates previous reports of in many squamates, but only nine studies have reproductive activity. During inactive months, the sexual investigated ultrastructural characteristics of the segment of the kidney is nondiscernable from the collecting SSK, five on snakes (Ku¨ hnnel and Krisch, 1974; ducts. The sexual segment consists of tall columnar epithe- Sever et al., 2002; Krohmer, 2004; Sever et al., lial cells with basally positioned nuclei. Perinuclear Golgi 2008; Siegel et al., 2009), and four on lizards complexes and rough endoplasmic reticulum are present. Secretory granules, which fill the apices of the epithelial (Furieri and Lanzavecchia, 1959; Del Conte and cells, are electron dense and released into the lumen by a Tamayo, 1973; Gabri 1983; Sever and Hopkins, merocrine secretory process. Narrow intercellular canaliculi 2005). separate each epithelial cell and are sealed by tight junc- Previous studies regarding the sexual segment tions at the luminal aspect. Basally, leukoctyes are observed vary in depth of coverage. For lizards, Furieri and within the intercellular canaliculi and outside the basal lam- Lanzavecchia (1959) were concerned only with the ina. Mast cells can be found just outside the basal lamina in effects of castration on the ergastoplasm (endo- close association with renal capillaries. The sexual segment plasmic reticulum conditions) of the sexual seg- of the kidney of H. turcicus is similar to that of three unre- ment of Italian wall lizards, Lacerta sicula (Lacer- lated lizards for which ultrastructure was investigated with tidae). Del Conte and Tamayo (1973) compared the secretion mode being the major difference Also, H. turcicus is similar to most other lizards in that complete regression sexual segment of males of rainbow whiptails, occurs during reproductive inactivity, but differs in this trait Cnemidophorus lemniscatus (Teiidae), with a ho- from the skink, Scincella lateralis, and most snakes which mologous area that undergoes some differentiation display a hypertrophied sexual segment of the kidney in females. Gabri (1983) examined captives of Bal- throughout the entire year. Although some unique similar- kan wall lizards, Podacris taurica (Lacertidae), ities appear during the optimization, no direct patterns or kept under temperatures mimicking natural directions are observed, and only the molecular based phy- logeny resolves the ancestral condition of the Squamata as the sexual segment of the kidney being observed in Additional Supporting Information may be found in the online the distal convoluted tubule, collecting duct, and ureter. J. version of this article. Morphol. 272:802–813, 2011. Ó 2011 Wiley-Liss, Inc. Contract grant sponsor: National Science Foundation; Contract grant number: DEB-0809831. KEY WORDS: reproduction; kidney; sexual segment; histology; gecko *Correspondence to: Justin L. Rheubert, Department of Biological Sciences, Southeastern Louisiana University, SLU 10736, Ham- mond, LA 70402. E-mail: [email protected] Received 27 October 2010; Revised 18 November 2010; INTRODUCTION Accepted 29 November 2010 The sexual segment of the kidney (SSK) was Published online 28 April 2011 in first described as a hypertrophied region of the Wiley Online Library (wileyonlinelibrary.com) kidney ducts by Gampert (1866) in the grass DOI: 10.1002/jmor.10949 Ó 2011 WILEY-LISS, INC. SEXUAL SEGMENT OF H. turcicus 803 conditions but a complete annual cycle was not To better understand the evolution of the SSK in a examined. Sever and Hopkins (2005) studied broad context, we then optimize SSK location on seasonal variation at the light- and electron- alternate squamate phylogenetic hypotheses. microscopy level of the SSK in the ground skink, Scincella lateralis (Scincidae). They reported data from wild-caught lizards collected throughout the MATERIALS AND METHODS entire year and found that, like most snakes Tissue Collection (Aldridge et al., in press), the SSK of S. lateralis is discernible from other nephridic tubules during Adult male H. turcicus were collected from southeast Louisi- the inactive season, which differs from that of ana from March 2007–March 2008 with the exception of Decem- ber, and a reproductively active female from April 2007 was other lizards (Sever et al., 2002). They also pro- examined. Geckos were euthanized within 48 h of capture using vided ultrastructural observations on correspond- a 0.2–0.5 ml intraperitoneal injection of sodium pentabarbitol ing areas of the female urinary ducts, and, like as approved by the Animal Care and Use Committee of South- C. lemniscatus, a hypertrophid region similar to eastern Louisiana University. Snout-vent lengths were meas- ured to the nearest 0.1 mm using calipers. The urogenital that of the male was found in females. systems were removed through gross dissection with the right Sever et al. (2002) proposed that the SSK is a side fixed in neutral buffered formalin for light microscopy and synapomorphy for squamates and possibly lepido- the left side fixed in Trump’s solution for electron microscopy. saurs (Sphenodon 1 Squamata), as a SSK may Carcasses of all specimens were deposited in the Southeastern also be present in tuataras, Sphenodon punctatus Louisiana University Vertebrate Museum. (Gabe and Saint Girons, 1964). However, a secre- tory region of the kidney is also developed in stickleback fish (Courrier, 1922) and in at least Light Microscopy three families of salamanders (Siegel et al., 2010). After fixation, tissues were rinsed with deionized water, dehy- However, sexual kidney structures in these other drated through a graded series of ethanol solutions (70%, 80%, vertebrate taxa do not appear to be homologous 95% 3 2, 100% 3 2), cleared in two changes of toluene, and with those found in the lepidosaurian reptiles placed in melted paraffin for 24 h under vacuum. Tissues were (Siegel and Aldridge, personal communication). then embedded in paraffin blocks and allowed to cure overnight. Paraffin sections were cut at 10 lm with a RMC rotary micro- The function of the SSK has yet to be fully eluci- tome (RMC Instruments, Tucson, AZ) and placed on albumi- dated, but the SSK has been hypothesized to acti- nized slides. Alternate slides were stained with hematoxylin vate and sustain sperm (Bishop, 1959; Cuellar, and eosin (general histological examination), bromphenol blue 1966), form copulatory plugs after insemination (protein concentrations), and periodic acid and Schiff reagent (PAS, neutral carbohydrates) counterstained with alcian blue (Devine, 1975), provide courtship pheromones 8GX at pH 2.5 (carboxylated glycosaminoglycans). Slides were (Volsøe, 1944), and/or provide other functions asso- viewed using a Leica DM2000 compound microscope and photo- ciated with seminal fluid (Prasad and Reddy, graphs were taken using a Leica DF420 digital camera (Leica 1972). Seasonal variation in the SSK has shown Microsystems, Wetzlar, Germany). Composite micrographs were strong correlation with spermatogenic activity, constructed using Adobe Photoshop 7.0 (Adobe Systems, San Jose, CA). mating, and increased androgen levels (Bishop, 1959; Pandha and Thapliyal, 1964; Misra et al., 1965; Prasad and Sanyal, 1969; Krohmer, 1986). Earlier research found that variation exists in Electron Microscopy the location of the SSK between different species Tissues for transmission electron microscopy were rinsed in of squamates. In most snakes, the SSK includes deionized water, postfixed in 2% osmium tetroxide, dehydrated portions of the distal convoluted tubule (Fox, through a graded series of ethanol solutions (0%, 85%, 95% 3 1977), and in the scolecophidia, the SSK is limited 2, 100% 3 2), cleared in propylene oxide, and embedded in ep- oxy resin (Embed 812, Electron Microscopy Sciences, Hatfield, to the collecting duct portions of the kidney (Fox, PA). Plastic sections were cut using a Reichert ultramicrotome 1965). However, recent studies have shown that (Reichert Microscope Services, Depew, NY) and DiATOME
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