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Penile Anatomy and Hypotheses of Erectile Function in the American Alligator (Alligator mississippiensis): Muscular Eversion and Elastic Retraction
The Anatomical Record
Abstract
The intromittent organs of most amniotes contain variable-volume hydrostatic skeletons that are stored in a flexible state and inflate with fluid before or during copulation. However, the penis in male crocodilians is notable because its shaft does not seem to change either its shape or bending stiffness as blood enters its vascular spaces before copulation. Here I report that crocodilians may have evolved a mechanism for penile shaft erection that does not require inflation and detumescence. Dissections of the cloaca in sexually mature male American alligators (Alligator mississippiensis) show that the cross section of the proximal shaft of the alligator penis contains dense collagenous tissues that do not significantly change shape when fluid is added to the central vascular space. The large amount of collagen in the wall and central space of the alligator penis stiffen the structure so it can be simply everted for copulation and rapidly retracted at its completion. Because no muscles insert directly onto the penis, eversion and retraction must be produced indirectly. My results suggest that the contraction of paired levator cloacae muscles around the anterior end of the cloaca rotates the penis out of the cloacal opening and strains the ligamentum rami that connect the base of the penis to the ischia. When the cloacal muscles relax, the elastic recoil of the ligamentum rami can return the penis to its original position inside the cloaca. Anat Rec, 296:488-494, 2013. © 2013 Wiley Periodicals, Inc.
... Before intromission, coordinated cloacal muscle contractions protrude the phallus from intracloacal storage to an external copulatory position. Suspensory connective tissue attached to the phallic shaft acts as a pivot point rotatating the emerging shaft and glans cranially (Kelly, 2013). The rigid corpus fibrosum of the phallus shaft facilitates intromission that, in turn, places the distal male glans in contact with female reproductive tract openings in the walls of the uroprotodeal fold . ...
... The simplest cause may be inflammation following trauma to the highly vascularized glans tissues that prevents retraction of the phallus into the vent (Lankester and Hernandez-Divers, 2005). The phallic eversion mechanism in crocodilians is complex, and other kinds of damage can also prevent retraction (Kelly, 2013). Because the crocodilian phallus is everted by cloacal muscle contraction, tonic contraction of these muscles could force the phallus out of the vent (Kelly, 2013). ...
... The phallic eversion mechanism in crocodilians is complex, and other kinds of damage can also prevent retraction (Kelly, 2013). Because the crocodilian phallus is everted by cloacal muscle contraction, tonic contraction of these muscles could force the phallus out of the vent (Kelly, 2013). Lankester and Hernandez-Divers (2005) posit that paraphimosis could be caused by "neurologic deficits involving the retractor phallus muscles" but did not know that unlike other amniotes, crocodilians lack a retractor muscle on their phallus (Kelly, 2013). ...
Phallic malformations directly impact crocodilian copulatory function and thus could impact reproductive success in individual animals. This case series characterizes malformations observed and the implied reproductive consequences. We assessed a range of phallic malformations observed in saltwater crocodile (Crocodylus porosus), Nile crocodile (Crocodylus niloticus), broad-snouted caiman (Caiman latirostris), and Cuban crocodile (Crocodylus rhombifer) during veterinary examinations or postmortem studies and characterized observation into the following categories: amputation, phallic glans malformations, sulcus spermaticus obstruction, and prolapse. Through detailed descriptions of these anomalies, we discuss potential reproductive health impact based on current knowledge across crocodilian species. When considering captive management of breeding stock, it is vital to examine individual efficacy at achieving proper intromission and insemination. Therefore, full reproductive examination in males should be part of routine examination to best manage individuals with such anomalies.
... Phallus anatomy has been characterized in detail for the saltwater crocodile (Crocodylus porosus) (Johnston et al., 2014), Nile crocodile (Crocodylus niloticus) (Moore, Francis, et al., 2020), American alligator (Alligator mississippiensis) (Kelly, 2013;Moore, Spears, Mascari, & Kelly, 2016) and false gharial (Tomistoma schlegelii) (Moore, Fitri, & Augustine, 2020), spanning species from all three families of modern Crocodylia (Oaks, 2011;Pan et al., 2020). In all of these taxa, the phallus can be divided into three regions: a pair of proximal crura, a cylindrical shaft, and the distal glans. ...
... Semen is transferred through a medial groove, the sulcus spermaticus, located on the ventral surface of the everted phallus (Johnston et al., 2014;Moore & Kelly, 2015;Ziegler & Olbort, 2007). The shaft is anchored to a thick tendon originating on the ischium that acts as a fixed point around which the male phallus rotates when it is everted for copulation via cloacal muscle contraction (Kelly, 2013). Both the sulcus spermaticus and the distal end of the phallus contain spongiform erectile tissue that inflates with blood to close the sulcal groove (Moore & Kelly, 2015) and produce species-specific glans morphology (Moore et al., 2016;Moore et al. 2020,b;Moore et al., 2021). ...
... Both the sulcus spermaticus and the distal end of the phallus contain spongiform erectile tissue that inflates with blood to close the sulcal groove (Moore & Kelly, 2015) and produce species-specific glans morphology (Moore et al., 2016;Moore et al. 2020,b;Moore et al., 2021). The shaft contains a core of dense, collagenous tissue that does not change shape during vascular inflation (Kelly, 2013;Moore et al., 2021); this tissue maintains a high resistance to bending that is likely to facilitate intromission through the female vent (Kelly, 2016). ...
The broad snouted caiman is a crocodylian native to South America that is subject to extensive conservation management in both wild and farming environments. Although reproductive behaviors like egg laying and clutch care have been examined in this species, little else is known about their copulatory system. We examined the anatomy of male and female cloacal and genital tissues ex vivo to build hypotheses of their interactions during copulation and the effects of that interaction on insemination. Male phallic glans tissues were artificially inflated to expand into their copulatory state, allowing the examination and quantification of structural changes at the gross and tissue levels. Digital reconstruction of MRI stacks yielded three‐dimensional tissue compartment specific glans models of the inflated state. Silicone molds of female cloacae and oviducts in conjunction with dissection and diceCT analysis allowed us to assess internal geometry and infer how male and female features interact in copulo. We observed glans expansion within the female proctodeum would result in a copulatory lock limiting deeper intromission or retraction. Intromission and subsequent creation of the copulatory lock produces extensive clitoral compression, providing a possible mechanism for female assessment of male copulatory performance. Further, glans expansion forms a distal lumen that positions the glans tip in or near the vaginal openings. A coiled, muscular vagina provides a possible mechanism for postcopulatory sexual selection by excluding semen. Together, the complex male–female interaction supports evidence for cryptic selection by female choice, which can act as a driver of genital coevolution.
... Crocodylians are an excellent system for analyzing the copulatory interactions of genital tissues. First, while the amniote phallus is responsible for both intromission and insemination [9], crocodylians split those functions between distinct tissues with different mechanical behaviors [10,11], permitting targeted analysis of intromissive and inseminatory tissue behavior during copulation. The inflated crocodylian glans also has species-specific morphology-both gross anatomical reports of several juvenile [11,12] and adult [13] crocodylian species and more detailed studies of adult male saltwater crocodile (Crocodylus porosus [14]), Nile crocodile (Crocodylus niloticus [15,16]), and false/Sunda gharial (Tomistoma schlegelii [17]) indicate a substantial, but thus far uncatalogued diversity of glans shapes within the clade. ...
... Anatomically, a crocodylian phallus can be divided into three sections arranged proximal to distal: the crura, the shaft, and the glans. Previous research has described the anatomy of the stiff intromissive tissues in the crura and shaft [10,17], and the inflatable tissues of the semen-conducting open groove on the ventral phallus, termed the sulcus spermaticus [14,18] and two sections of the glans: the more proximal ridge (alternatively termed the cuff) and the distal tip extending along the ventral aspect of the glans [19]. The glans tip is the termination site of the sulcus spermaticus [14,18], and during copulation the glans features have the closest, most intimate mechanical interactions with the female urodeum-the middle cloacal chamber that contains the opening to the vaginal passages and oviducts [13,20,21]. ...
... It is possible that glans inflation occurs only after the male has successfully inserted his phallus into the female cloaca. This copulatory pattern is probable because the shaft of the phallus does not rely on inflation to become stiff [10] and could be beneficial in achieving intromission if the glans is to be inflated to a sizable circumference/volume ( Figures 4H, 5, and 6A). This procedure would be similar to copulation in some testudines, where the stiffened phallus is everted directly from its stored position in the male cloaca into the female cloaca, and the glans region is only fully inflated after insertion [38,39]. ...
The phallic glans of the American alligator (Alligator mississippiensis) is the distal termination of the semen-conducting sulcus spermaticus and during copulation has the closest, most intimate mechanical interactions with the female urodeum, the middle cloacal chamber that contains the opening to the vaginal passages and oviducts. However, the details of this interface leading to insemination and gamete uptake are unclear. Here we: 1) Histologically characterize the underlying tissue types and morphologically quantify the shape changes associated with glans inflation into the copulatory conformation, 2) Digitally reconstruct from MRI the 3D shape of functional tissue compartments, and 3) diceCT image the copulatory fit between male phallus and female cloaca. We discuss these results in relation to tissue type material properties, the transfer on intromittent forces, establishing potential copulatory lock, inflated glans volume scaling with body mass/length, the mechanics of semen targeting and insemination, and potential female cryptic choice impacting multiple clutch paternity. In part, this study further clarifies the phallic morphological variation observed among crocodylians and begins to investigate the role(s) these divergent male forms play during copulation interacting with female cloacal forms to increase reproductive success.
... Amniote phalluses can exist as paired, single, or rudimentary appendages, and contain a spermatic canal located either within the phallus as a closed urethral tube or along its ventral side as an open phallic sulcus (also known as the sulcus spermaticus or urethral groove ;Günther 1867;Gadow 1887;Cope 1896;Liebe 1914;Reese 1915Reese , 1924Dowling and Savage 1960;Zug 1966;King 1979b;Ferguson 1985;Raynaud and Pieau 1985;Banks 1986;Williams-Ashman 1990;Ziegler and Olbort 2007;Böhme and Ziegler 2009;Kardong 2009). Mechanical properties of amniote penile tissues vary; dynamic tissues change shape, size, or stiffness in response to hydrostatic pressure or muscular action, whereas static tissues provide structural support via rigid calcified or collagenous elements (Banks 1986;Kelly 1999Kelly , 2000Kelly , 2002Kelly , 2004Kelly , 2007Brennan et al. 2010;Kelly 2013). ...
... All amniote phalluses are built from connective tissue, smooth muscle, and endothelium; however, variation in the type and organization of these tissues underlies the morphological diversity in reptilian and mammalian intromittent organs. Component tissues in amniote phalluses facilitate two processes: the acquisition and/or maintenance of structural rigidity (Banks 1986;Kelly 2000Kelly , 2002Kelly , 2004Kelly , 2007Kelly , 2013Porto et al. 2013) and the tubular function of the phallic sulcus (Zug 1966;Kelly 1999;Rao and Vijayaragavan 2000;Brennan et al. 2010;Capel et al. 2011). ...
... In contrast to the morphological plasticity of other reptilian penises, crocodilian and turtle phalluses undergo comparatively subtle changes upon erection (Reese 1915(Reese , 1924Zug 1966;Cabrera et al. 2007;Ziegler and Olbort 2007;Kelly 2013). Fibrous bodies composed of rigid, dense connective tissue constitute the penile shaft in crocodilians and turtles; intromission competency is achieved by eversion or rotation of the phallus out of the cloaca driven by muscular action and is accompanied by secondary inflation of erectile tissues in the distal glans and adjacent to the phallic sulcus (Reese 1915(Reese , 1924Zug 1966;Sadleir 1973;Powell 1999;Cabrera et al. 2007;Ziegler and Olbort 2007;Kelly 2013). ...
An intromittent phallus is used for sperm transfer in most amniote taxa; however, there is extensive variation in external genital morphology within and among the major amniote clades. Amniote phalluses vary in number (paired, single, or rudimentary), spermatic canal morphology (closed tube or open sulcus), and mode of transition between resting and tumescent states (inflation, rotation, eversion, or muscle relaxation). In a phylogenetic context, these varying adult anatomies preclude a clear interpretation for the evolutionary history of amniote external genitalia; as such, multiple hypotheses have been presented for the origin(s) of the amniote phallus. In combination with historic embryological studies, recent comparative developmental analyses have uncovered evidence that, despite extensive morphological variation in adult anatomy, embryonic patterning of the external genitalia is similar among amniotes and begins with emergence of paired swellings adjacent to the cloaca. External genital development in mammals, squamates (lizards, snakes, and amphisbaenians), Rhyncocephalians (tuataras), turtles, crocodilians (alligators, crocodiles, and gharials), and birds proceeds by iterative sequences of budding and fusion events, initiated by emergence of paired swellings adjacent to the embryonic cloaca. Conservation of the embryonic origins, morphogenetic processes, and molecular genetic mechanisms involved in external genital development across Amniota supports derivation from the common ancestor of amniotes, and suggests that lineage-specific divergence of later patterning events underlies the variation observed in extant adult amniote phallus morphology.
... But comparative studies show that intromittent organ morphology also diverges among the taxa within a lineage. For example, while recent developmental studies suggest that the amniote phallus evolved only once (Gredler et al. 2014;Tschopp et al. 2014;Infante et al. 2015;Sanger et al 2015), its anatomical organization and erectile mechanics have diversified across amniotes, producing from the same ancestral developmental plan an inflatable penis that stiffens before copulation in mammals (Kelly 1999), a stiff densely-collagenous phallus that is muscularly everted for copulation in crocodilians (Kelly 2013), paired hemipenes that are everted and inflated inside the female in squamates (King 1981;Friesen et al. 2013), a phallus that pairs a band of stiff material with a large mass of inflatable tissue in turtles (Zug 1966;King 1981), and a flexible penis that explosively inflates into the female in waterfowl (Brennan et al. 2010). Subtler differences in the external shape, surface features, or internal elements of intromittent organs can evolve rapidly among closely related populations (Soto et al. 2013;Simmons and Firman 2013;Heinen-Kay et al. 2013) or species (Klaczko et al. 2015), a phenomenon which is now thought to be the result of postcopulatory sexual selection (Eberhard 1985;Arnqvist 1998;Hosken and Stockley 2004;Rowe and Arnquist 2011;Simmons 2014). ...
... The mechanisms they drive can be quite simple: in turtles and most mammals, for example, the flaccid penis is held inside the 706 D. A. Kelly male's body by a pair of contracted retractor muscles; penile protrusion requires only their relaxation after which the weight of the penis slides it outside the body (Zug 1966;Sjostrand and Klinge 1995). In taxa as disparate as poeciliid fish (Rosen and Gordon 1953;Meisner 2005), insects (Fairbarn et al. 2003;Jaloszynski et al. 2014), crocodilians (Kelly 2013), and isopods (Wilson 1991), muscle contractions rotate the intromittent organ around a fulcrum into the correct position for copulation. Other taxa rely on muscularly-driven linkage systems, as in the monogean Amphibdelloides maccallumi, whose penis is stored in a tube surrounded by a circular muscle; contractions of that muscle evert the penis ''in a manner reminiscent of an engineer's cable-operated mechanical device'' (Kearn and Whittington 2015), or in harvestmen species where contractions of genital muscles change the pressure inside a hemolymph-filled reservoir which in turn changes shape to evert the penis (Shultz and Pinto-da-Rocha 2007;Burns and Shultz 2015). ...
... Copulatory organs in the teleost fish that derived their intromittent organs from pelvic fins (e.g., Phallostethidae) or anal fins (e.g., Brosmophycinae, Poeciliidae, Anablepidae) contain bone (Rosen and Gordon 1953;Meisner 2005); elasmobranch claspers, which are derived from pelvic fins, are supported by cartilage (Klimley 2013) that is heavily calcified, at least in adult basking, blue, and white sharks (Pratt 1996). Crocodilian phalluses are solid columns built of an integrated network of stiff collagen fibers (Kelly 2013). The portions of arthropod intromittent organs that push open female genital openings contain sclerotized cuticle (Fairbarn et al. 2003;Ewers-Saucedo et al 2015;Burns and Shultz 2015), as does the penis of some monogean parasites (Kearn and Whittington 2015). ...
Intromittent organs—structures that place gametes into a mate for internal fertilization—evolved many times within the animal
kingdom, and are remarkable for their extravagant morphological diversity. Some taxa build intromittent organs from tissues
with reproductive system antecedents, but others copulate with modified fins, tentacles, or legs: anatomically, these structures
can include combinations of stiff tissues, extensible tissues, and muscle. Their mechanical behavior during copulation is
also diverse: males in some taxa reorient or protrude genital tissues, others inflate them and change their shape, while still
other taxa combine these strategies. For these animals, the ability to ready an intromittent organ for copulation and physically
interact with a mate’s genital tissues is critical to reproductive success, and may be tied to aspects of postcopulatory selection
such as sperm competition and sexual conflict. But we know little about their mechanical behavior during copulation. This
review surveys mechanical strategies that animals may use for intromittent organ function during intromission and copulation,
and discusses how they may perform when their tissues experience stresses in tension, compression, bending, torsion, or shear.
... During amniote copulation, the male intromittent organ acquires and maintains rigidity in order to direct sperm into the female reproductive tract [Gadow, 1887;King, 1979;Powell, 2000;Kelly, 2002]. Erection and eversion by hydrostatic pressure and muscle contraction function to achieve turgor and to create a functional channel for sperm transfer [Hart and Melese-D'Hospital, 1983;Schmidt and Schmidt, 1993;Andersson and Wagner, 1995;Kelly, 2002Kelly, , 2004Kelly, , 2013Hsu et al., 2005;Cabrera et al., 2007]. Hydrostatic pressure is produced by blood vasculature in penises of crocodilians, turtles and mammals [Zug, 1966;King, 1979;Kelly, 2004;Moore et al., 2012], by lymphatic vessels in bird penises, when present [King, 1979], and by both blood and lymph in squamates [Dowling and Savage, 1960]. ...
... Internally, crocodilian, turtle, and mammalian penises have large fibroelastic, vascular, and lacunar tissues that support vascular erection [Zug, 1966;King, 1979;Kelly, 2004]. Two regions of erectile tissue are present; the corpus spongiosum is flexible, fibrous tissue that surrounds the penile sulcus in non-mammalian amniotes and the penile urethra in mammals, and the corpora cavernosa are large, paired regions of highly vascularized tissue that expand upon increased blood flow [Reese, 1915;Zug, 1966;King, 1979;Powell, 2000;Kelly, 2004Kelly, , 2013Cabrera et al., 2007]. The base of the alligator penis is formed from paired penile bodies called crura [Gadow, 1887;Reese, 1924;Kelly, 2013]. ...
... Two regions of erectile tissue are present; the corpus spongiosum is flexible, fibrous tissue that surrounds the penile sulcus in non-mammalian amniotes and the penile urethra in mammals, and the corpora cavernosa are large, paired regions of highly vascularized tissue that expand upon increased blood flow [Reese, 1915;Zug, 1966;King, 1979;Powell, 2000;Kelly, 2004Kelly, , 2013Cabrera et al., 2007]. The base of the alligator penis is formed from paired penile bodies called crura [Gadow, 1887;Reese, 1924;Kelly, 2013]. Proximally, each crus is connected to the pelvic girdle and adjacent cloacal muscles; distally, the crura fuse to form the shaft of the corpus cavernosum [Powell, 2000;Kelly, 2013]. ...
In most animals, reproduction by internal fertilization is facilitated by an intromittent organ, such as the penis in amniote vertebrates. Recent progress has begun to uncover the mechanisms of mammalian external genital development; however, comparatively little is known about the development of the reptilian penis and clitoris. Here, we describe the development of the phallus and cloaca in the American alligator, Alligator mississippiensis. The embryonic precursor of the penis and clitoris is the genital tubercle, which forms by the budding of genital mesenchyme beneath the ventral body wall ectoderm, adjacent to the cloacal membrane. The cloacal lips develop from another pair of outgrowths, the lateral swellings. Early development of the alligator phallus, cloaca, and urogenital ducts generally resembles that of other reptiles, suggesting that differences in adult reptilian phallus and cloacal anatomy arise at later stages. The phallic sulcus is derived from the cloacal endoderm, indicating that the crocodilian sulcus is functionally and developmentally homologous to the mammalian urethra. Initial external genital outgrowth and patterning occur prior to temperature-dependent sex determination. Our analysis of alligator phallus and cloaca development suggests that modifications of an ancestral program of urogenital development could have generated the morphological diversity found in the external genitalia of modern amniotes. © 2014 S. Karger AG, Basel.
... In male differentiation, the embryonic genital tubercle elongates into a proximal dense fibrous corpus fibrosum and elaborates into a distal inflatable glans of corpus spongiosum terminating in the sperm-carrying sulcus spermaticus. These structures facilitate female cloacal intromission and insemination upon phallic eversion and copulation (Kelly, 2013). Although the generalized male phallic form and copulatory function is conserved across taxa, the distal glans shape is clade specific, with Alligatoridae presenting a more rounded glans and filiform glans tip (Moore, Fitri, et al., 2020;Moore, Francis, et al., 2020;Moore et al., 2016) and Crocodylidae presenting a notched glans with a blunt deflected glans tip (Fitri et al., 2018;Johnston et al., 2014;Moore, Groenewald, et al., 2020). ...
... Crocodilian copulation often takes place in water with males approaching females laterally from the rear and assuming a superior position. Prior to intromission, the male phallus is protruded from intracloacal storage to its external copulatory position by coordinated cloacal muscle contractions that rotate the shaft and glans cranially via a suspensory connective tissue pivot point (Kelly, 2013). With applied muscular force, intromission is facilitated by the rigid corpus fibrosus element of the phallus shaft that, in turn, places the distal male glans in the proctodeum abutting the female reproductive tract openings in the distal ventral folds of the urodeum, the second internal chamber of the cloaca. ...
... Unlike the homologous mammalian or turtle penises (Kelly 2004;Brennan 2016), the phallus does not inflate to erection for copulation. Instead, indirect cloacal muscle activity rotates the rigid phallus out of the cloaca into a position that allows intromission (Kelly 2013). However, its glans does inflate during copulation, with a mechanism thought to be blood vascular (King 1979). ...
... We find that the American alligator phallus has a glans containing both: (1) a network of vascular tissues that can be traced to paired supracrural plexuses at the base of the phallus; and (2) an array of collagen and elastin fibers characteristic of tissues that allow expansion in conjunction with an internal increase in fluid volume (Kelly 1999a;Shadwick 1999). These features suggest that unlike the densely collagenous and permanently rigid central shaft of the alligator phallus (Kelly 2013), alligator glans tissues inflate to a characteristic and repeatable shape via an influx of blood. ...
The distal part of the crocodilian phallus consists of a bulbous glans containing well-developed vascular tissues that can
inflate before or during sexual activity, enlarging and elaborating the glans into a complex, though still functionally undefined,
copulatory structure. An enlarged glans putatively interacts with the female cloaca and may change the shape of her reproductive
tract to facilitate insemination and increase the probability of fertilization. Here, we investigated the cellular-level properties
of the glans and other inflatable phallic tissues associated with the sperm-conducting sulcus spermaticus in the American
alligator (Alligator mississippiensis). Using histochemical staining, we visualized and defined collagen and elastin fiber densities and orientations in these
tissues. Extracellular matrix architectures provided insights about phallic glans material properties and how they may affect
tissue strength and flexibility during inflation and in response to copulatory forces. We also investigated the potential
sources of fluids that induce inflation in alligator phalli. Combining serial sectioning and three-dimensional reconstruction,
we identified a pair of supracrucal plexus vascular bodies at the proximal end of the alligator phallus that extend distally
adjacent to ventro-medial sulcus tissues. Together, our gross and histological examination of the American alligator phallic
glans suggests that its tissues are arranged in a manner that would allow vascular inflation to expand the glans to a specific
and repeatable shape, and potentially release secretory products into the female reproductive tract. Both elements could play
roles in postcopulatory sexual selection, by mechanically and/or chemically affecting female reproductive physiology.
... In many taxa, the phallus contains distinct tissues for each function ( King, 1981;Kelly, 1997; Miller and Dinkelacker, been hypothesized to play a role in moving semen down the sulcus ( Caberea and Garcia, 2004;Moore et al., 2012). It should be noted that the tissues associated with the sulcus make up only a small portion of the phallus in adult male crocodilians: in most of the shaft the organ's internal volume is comprised of tissues containing densely packed collagen fibers ( Caberea and Garcia, 2004;Lankester and Hernandez-Divers, 2005;Kelly, 2013). These collagenous tissues seem to increase the resistance of the phallus to bending and probably improve intromission by preventing the phallus from bending away from the female vent during copulation; they may also provide structural support for the sulcus and its associated tissues. ...
... If true, it is possible that the flow characteristics they describe were produced solely by coordinated ciliary beating within the sulcus ( Fulford and Blake, 1986;Sleigh et al., 1988). While the crocodilian phallic shaft is densely collagenous and rigid ( Cabrera and Garcia, 2004;Kelly, 2013) with only a small ridge of erectile tissue along the sulcus, the glans region is highly vascular, spongiform ( Moore et al., 2012;Johnston et al., 2014), and has been observed to inflate and change shape with phallic eversion and semen release ( Johnston et al., 2014). Sulcus morphology also changes as it enters the glans and tip regions. ...
Male intromittent organs serve two primary reproductive functions: the physical entry into the female body during copulation and the effective delivery of gametes resulting in internal fertilization. Here we present a histological examination of the adult male American alligator phallus semen delivery apparatus, the sulcus spermaticus. While the highly collagenous basal crurae and more distal shaft of the alligator penis contain the rigid structures that facilitate cloacal intromission, the sulcus is more functionally intricate. Here we show the sulcus spermaticus (an open groove that runs along the ventral aspect of the phallic shaft) to be a spatially heterogeneous reproductive structure containing a complex architecture of multiple tissue types. Sulcus morphology markedly changes from its proximal origin between the crurae to its distal exit from the phallus tip. At the proximal origin of the sulcus, the ductus deferens vent semen into an expanded lumen lined by a convoluted secretory epithelium. Along the length of the phallic shaft, an arrangement of longitudinally and radially oriented smooth muscle bundles may act via rhythmic contractions to produce peristaltic sperm conveyance through the sulcus. An extensive vascular network of blood and lymph vessels putatively engorges the sulcus tissues during reproductive activity, increasing tension on an internal network of connective tissues and leading to localized inflation and increased tissue rigidity. We hypothesize that this engorgement works to seal the sulcus groove and allow the structure to convey semen through a functionally closed tube. Further, numerous epithelial secretory cells contribute seminal fluids to the ejaculate and may aid in as yet uncharacterized aspects of sulcus functioning. Together, these observations establish that the sulcus spermaticus is far more than a simple furrow in the phallus shaft for sperm conduction: it contains elements that form a complex functional gamete delivery system.
... Crocodilians, like chelonians, have a single penis (or phallus) rather than hemipeni (Jacobson, 2007). Similar to what has been noted in other crocodilians (Kelly, 2013;Moore et al., 2012), the saltwater crocodile penis arises from the ventral wall of the proctodeum. However, to our knowledge, there has been no illustrative evidence of the opening point of the ductus deferens, although this information is important for the purposes of semen collection. ...
... Presumably, when blood is supplied to this vascular space during erection, the cuff of the glans penis inflates (see Fig. 3C). Kelly (2013) proposed that erection of the alligator penis does not change its shape or bending stiffness as blood enters the vascular spaces of the penis. While such a phenomenon needs to be examined in the shaft of the penis of the crocodile, our initial observations revealed significant changes in the size and shape of the morphology of the glans penis during erection. ...
... The ductus deferens is covered by a pseudostratified epithelium and opens via a papilla at the proximal end into a single medial groove along the shaft and glans penis, which is known as the sulcus spermaticus [33]. As previously reported by other authors [28,34,35], crocodiles (as chelonians) possess a single penis; it arises from the wall of the proctodeum and is contained in this structure when not erect. The glans penis possesses a hollow cavity that opens towards the tip of the penis, which is not directly connected to the medial groove. ...
Reptile biodiversity is rapidly declining, with over 11,733 recognized species across 1226 genera being documented, many of which are endangered. Captive breeding programs play a crucial role in conservation; however, effective management requires accurate sex determination, especially due to the fact that many reptile species exhibit minimal or no sexual dimorphism. When present, sexual dimorphism manifests as differences such as size, coloration, and morphological features influenced by evolutionary pressures and hormones. Various sex determination techniques are employed due to the lack of external sexual characteristics in many species. These methods include probing, hydrostatic eversion, popping, ultrasound, CT, radiography, contrast radiography, endoscopy, and genotypic sex determination. Accurate sex determination is crucial for the success of captive breeding programs and the conservation of reptile species. Advanced imaging and molecular methods offer promising non-invasive alternatives but may not be universally accessible or effective. An understanding of the unique reproductive anatomy and the use of appropriate sexing techniques are fundamental to establishing breeding groups, preventing aggressive behaviours among groups, and ensuring the long-term survival of endangered reptile populations.
... We lastly discussed another possibility that the imprint was originated from a crocodilians' penis. Kelly (2013) ...
A rare ichnological example of a crocodilian footprint on an Eocene crocodilian coprolite has been discovered. The enigmatic specimen, measuring 4 cm in length, was found among 100 coprolites at the Na Duong coal mine in Lang Son province, northern Vietnam. Almost all the discovered coprolites were ascribed to a potential crocodilian producer, suggesting the existence of an ancient lacustrine environment. Furthermore, neoichnological analyses of extant crocodilian footprints also corroborate the inference of a crocodilian as the producer of the footprint. We concluded that the 4-cm-long Na Duong fingerprints most likely belonged to a 2-mlong crocodilian whose IV or V finger of the right manus might have made the fingerprints. Since no other records of foot traces or trackways were identified during the fieldwork in the fall of 2018, the Na Duong fossil site should be investigated for further ichnofossil analysis.
... Similar to descriptions of other crocodilians (Kelly 2013;Moore et al. 2020), the saltwater crocodile has a single phallus, which arises from the ventral wall of the proctodeum (Johnston et al. 2014a(Johnston et al. , 2014b. The exit position of the ostia of the ductus deferens has a distinctive papilla opening at the base of a single medial groove, known as the sulcus spermaticus ( Fig. 2; see also Johnston et al. 2014b). ...
Information on the morphology and histology of the male reproductive system of the Crocodylia species is necessary to determine the role of these tissues in the production of functional spermatozoa. Accordingly, in this study we examined the gross morphology and microanatomy of the testis and the male excurrent duct system through which spermatozoa pass before ejaculation. The data demonstrate that the reproductive system in male saltwater crocodiles comprises paired testes, which convey spermatozoa distally via the rete testis into an excurrent duct system comprising ductuli efferentes, ductuli epididymides, ductus epididymidis and ductus deferens. The epithelium delineating the male tract was dominated by non-ciliated and ciliated cells structured into a simple columnar lining of the ductuli efferentes and ductuli epididymides, through to the high pseudostratified columnar epithelium of the ductus epididymidis and ductus deferens. The morphology and histochemical staining of these ducts suggest their involvement in seminal fluid production and/or its modification, which likely contributes to the nourishment, protection and/or storage of crocodile spermatozoa. As a reflection of their common Archosaurs ancestry, the overall structural characteristics we describe for the crocodile male excurrent duct system share closer similarities to those of the Aves than other clades within the Reptilia class or Mammalia.
... Male crocodylians use an intromittent organ during reproduction to transfer sperm to the female cloaca and ultimately the reproductive tract (Ziegler and Olbort, 2007;Grigg and Kirshner, 2015). At copulation, phalli of crocodylians, homologous to all vertebrate penises (Gredler, 2016), are mechanically everted from within the male cloaca (Kelly, 2013), and the exposed portion is comprised of a stiff proximal shaft and an inflatable distal glans (Moore et al., 2012). Upon intromission, the phallus moves through the female vent and enters the first chamber of the cloaca, the proctodeum. ...
The male crocodylian phallus, an intromittent organ, transfers sperm to the female cloaca during reproduction. During copulation, the distal phallic glans inflates via blood-filled spongiform tissues; it enlarges into an elaborate shape that directly interacts with the female urodeumthe cloacal chamber that contains the female reproductive tract openings. Alas, the specific mechanics of crocodylian insemination and gamete transfer remain unclear. To that end, we investigated the gross and cellular morphology of the Nile crocodile (Crocodylus niloticus) glans characterizing tissues types and structural morphologies to better predict how these male tissues may interact with those of the female. We tracked blood flow from the descending aorta to the phallic glans by way of sulcus spermaticus-adjacent blood vessels. Utilizing an artificial inflation technique, we documented how the glans tissue shape changes with increased hydrostatic pressure in spongiform tissues including increases in height and width and the enlargement of a cup-like distal lumen. Sectioning the glans, we traced the decrease in dense collective tissues and the proliferation of inflatable tissues moving from proximal to distal. Concomitant with the development of the inflatable glans, we identified elastin-rich tissues around the inflatable glans regions and the deep sulcus spermaticus semen conduit. Together, these observations demonstrated the dynamic nature of the tissues, where collagen fibers supply mechanical strength and elastin fibers provide resilience and recoil. We hypothesize how these glans characteristics may interact with female tissues during copulation to increase the chance of successful gamete transfer.
... Arrowheads mark a slender dense connective tissue process located dorsal to the sulcus spermaticus and intromission (Garrick & Lang, 1977). While a male crocodylian's stiff, noninflatable phallic shaft facilitates initial intromission into the female vent (Kelly, 2013), subsequent movements of the pair such as rolls during copulation risk dislodging the male before insemination is completed. Upon inflation, the lateral glans expansion may help prevent the phallus from dislodging by interacting with female cloaca tissues to produce a "genital copulatory lock." ...
The crocodylian phallic glans is the distal inflatable structure that makes the most direct contact with the female cloacal and associated reproductive tract openings during copulation. Therefore, its form and function directly impact female tissue sensory interactions and insemination mechanics. Compared to mammals, less is known about glans functional anatomy among other amniotes, including crocodylians. Therefore, we paired an ex vivo inflation technique with magnetic resonance imaging 3D‐reconstructions and corresponding histological analyses to better characterize the morphological glans restructuring occurring in the Nile crocodile (Crocodylus niloticus) at copulation. The expansion of contiguous inflatable spongiform glans tissues is variably constrained by adjacent regions of dense irregular collagen‐rich tissues. Therefore, expansion shows regional differences with greater lateral inflation than dorsal and ventral. Furthermore, this enlargement elaborates the cup‐like glans lumen, dorsally reorients the glans ridge, stiffens the blunt and bifid glans tip, and putatively works to seal the ventral sulcus spermaticus semen conduit groove. We suggest how these dynamic male structures may interact with structures of the female cloacal urodeum and how these morphological changes, in concert with the varying material properties of the structural tissue compartments visualized in this study, aid copulatory gamete transfer and resulting fecundity.
Research Highlights
• Nile crocodile glans inflation produces a reproductively relevant copulatory structure directing insemination and female tissue interactions.
• Pairing magnetic resonance imaging 3D reconstruction with corresponding histology effectively studies functional anatomy.
... Such stimulation may serve as a form of copulatory courtship. Recent research on crocodiles and alligators has focused on understanding the complexity of their genital morphology (Kelly, 2013;Moore, Spears, Mascari, & Kelly, 2016). ...
In internal fertilizers, copulatory behavior and genital morphology are intricately connected because there are many functional and morphological challenges that genitalia must overcome for successful transfer of male gametes into the female reproductive tract. In addition, selective forces can act either on copulatory behavior and genitalia independently or concurrently. However, collecting data on copulatory behavior can be challenging, and there are relatively few studies of genital morphology in Amniotes, which include reptiles, birds, and mammals. As a result, we know little about the relationship between copulation and genitalia in this group. Here we examine copulatory behavior in Amniotes using particularly well-known examples, and add information about the morphology and function of their genitalia to lay a framework for further research on the integration of these traits.
... After dissection, the ventral tendon and the two ligamentum rami (not shown) which respectively project from the crura to dorsal midline of the caudal ischia were removed before histological processing. The location and mechanical function of ventral penile tendon and ligamentum rami are suspending the phallus in the cloaca, regulating rotation with eversion and placing the ligamentum rami under tension when the phallus is out of the cloaca agrees with American alligator (Alligator mississippiensis) functional penile anatomy (Kelly, 2013). ...
As wild population threats for the endangered false gharial (Tomistoma schlegelii) persist, conservation breeding programs, including developing semen collection techniques for subsequent artificial insemination, are becoming important species conservation measures. Developing reproductive biology understanding of a species is important to developing best practices and hopefully maximizing reproductive successes. However, information on crocodylians functional copulatory anatomy in general is lacking. To that end, zoological facilities and conservation centres have the exceptional opportunity to contribute new understandings that may not otherwise be attainable regarding crocodylian reproductive anatomy, particularly during routine physical examinations or post-mortem necropsies. Therefore, to better understand T. schlegelii reproductive biology, to contribute knowledge in support of zoo breeding conservation efforts and to contribute to what is known overall about crocodylian reproduction, we investigated phallic anatomy of adult male Tomistoma from two zoological populations, the St. Louis Zoo, USA and Sungai Dusun Wildlife Reserve, Peninsular Malaysia. Here, we present the gross anatomical features and histological analysis of underlying tissue-level details in pursuit of a better understanding of copulatory function and associated gamete transfer mechanisms. While much of the overall Tomistoma phallic morphology and inferred function corresponds to that of other crocodylian species and speaks to conserved aspects of functional anatomy across taxa, species-specific aspects of glans and glans tip morphology are also identified. These novelties are discussed in a general function and overall broader evolutionary contexts.
... Male crocodylians use a phallus (penis) as an intromittent organ to place sperm in proximity of the female reproductive tract . During copulation, the phallus everts from the male cloaca (Kelly, 2013) and enters the female cloaca (Kuchel & Franklin, 2000). The distal phallus has an inflatable, elaborated, and cup-like glans that is the terminus of the gamete-conducting sulcus spermaticus (Johnston et al., 2014;Moore, Spears, Mascari, & Kelly, 2016). ...
While puberty is an animal commonality, little is known of its timing or process in crocodylians. Males copulate with an intromittent phallus that has a distinct glans morphology which directly interacts with the female cloaca, putatively effecting effective semen transfer and ultimately increased fecundity. Here we present, during the Morelet's crocodile lifecycle, a well-defined body length (65 cm snout-vent length) inflection point that marks a subsequent increase of phallic glans growth rates. Putatively, this postpubescent growth produces a copulatory-effective phallus. While not as robust of a trend as snout-vent length, this growth inflection concomitantly begins with a body condition index (CI = BM/SVL3 ) between 2.0 and 2.5 and is most distinct above a CI of 2.5. Also, in males, this 65 cm size threshold also aligns with the initiation of more robust growth in caniniform alveoli associated with prominent maxillary and mandibular teeth. This inflection was not observed in females, thus marking a sexual dimorphism that begins to present with the onset of puberty. This bodily manifestation of puberty other than those changes observed in the reproductive tracts is a novel observation for crocodylians and lays a foundation for further study among species of how changing endocrine signaling within sexually maturing males may also influence a broader range of secondary sex characteristics.
... Our observation of lymphocyte aggregates in the phallus agrees with the latter, since the C. latirostris individuals studied here were healthy and raised in sanitary controlled conditions. In turtles and mammals, the stiffness of the phallus is achieved through peri-vascular muscle relaxation and engorgement of the corpus cavernosum vascular spaces, whereas, in crocodilians, the corpus cavernosum is comprised of collagen fibers arranged in orthogonal geometries that result in an erect structure that is resistant to bending during copulation (Kelly, 2013;Gredler et al., 2014;Gredler, 2016). In agreement, highly birefringent and densely packed collagen fibers were observed in the phallus of C. latirostris males. ...
The broad-snouted caiman (Caiman latirostris) is a crocodilian species that inhabits South American wetlands. As in all other crocodilians, the egg incubation temperature during a critical thermo-sensitive window (TSW) determines the sex of the hatchlings, a phenomenon known as temperature-dependent sex determination (TSD). In C. latirostris, we have shown that administration of 17-β-estradiol (E2) during the TSW overrides the effect of the male-producing temperature, producing phenotypic females (E2SD-females). Moreover, the administration of E2 during TSW has been proposed as an alternative way to improve the recovery of endangered reptile species, by skewing the population sex ratio to one that favors females. However, the ovaries of E2SD-female caimans differ from those of TSD-females. In crocodilians, the external genitalia (i.e. clitero-penis structure or phallus) are sexually dimorphic and hormone-sensitive. Despite some morphological descriptions aimed to facilitate sexing, we found no available data on the C. latirostris phallus histoarchitecture or hormone dependence. Thus, the aims of this study were: (1) to establish the temporal growth pattern of the phallus in male and female caimans; (2) to evaluate histo-morphological features and the expression of estrogen receptor alpha (ERα) and androgen receptor (AR) in the phallus of male and female pre-pubertal juvenile caimans; and (3) to determine whether the phallus of TSD-females differs from the phallus of E2SD-females. Our results demonstrated sexually dimorphic differences in the size and growth dynamics of the caiman external genitalia, similarities in the shape and spatial distribution of general histo-morphological compartments, and sexually dimorphic differences in innervation, smooth muscle fiber distribution, collagen organization, and ERα and AR expressions. The external genitalia of E2SD-females differed from that of TSD-females in many histological features and in the expression of ERα and AR, resembling patterns described in males. Our results alert on the effects of estrogen agonist exposure during TSW and suggest that caution must be taken regarding the use of E2SD as a procedure for wildlife population management.
... Our technique of inflating post-mortem penises and inserting them into vaginas revealed that marine mammal genitalia vary in their shape correspondence and in the possible mechanical interactions that may occur during non-simulated copulation. Other techniques to artificially inflate flaccid postmortem intromittent organs have been developed for insects [44,45], snakes [12], alligators [46], armadillos [47], bats [48] and rats [12]. However, as the cetacean penis is fibroelastic rather than vascular, a novel inflation approach was necessary to overcome the resistance of dense collagenous and fibrous tissue. ...
Genitalia are morphologically variable across many taxa and in physical contact during intromission, but little is known about how variation in form correlates with function during copulation. Marine mammals offer important insights into the evolutionary forces that act on genital morphology because they have diverse genitalia and are adapted to aquatic living and mating. Cetaceans have a fibroelastic penis and muscular vaginal folds, while pinni-peds have a baculum and lack vaginal folds. We examined copulatory fit in naturally deceased marine mammals to identify anatomical landmarks in contact during copulation and the potential depth of penile penetration into the vagina. Excised penises were artificially inflated to erection with pressurized saline and compared with silicone vaginal endocasts and within excised vaginas in simulated copulation using high-resolution, diffusible iodine-based, contrast-enhanced computed tomography. We found evidence suggestive of both congruent and antagonistic genital coevolution, depending on the species. We suggest that sexual selection influences morphological shape. This study improves our understanding of how mechanical interactions during copulation influence the shape of genitalia and affect fertility, and has broad applications to other taxa and species conservation.
... Even in birds, in which the phallus does not have a blind tubular cavity, the phallus is asymmetric (Montgomerie & Briskie, 2007). In Testudines and Crocodylia, the phallus is intromittent, symmetric and has sigmoidal curvature (Kelly, 2013). Only in groups of birds, in which the phallus has reduced and become non-intromittent, the phallus is symmetric without curvature (Brennan et al., 2008;King, 1981). ...
We studied the morphology of the copulatory organ of Ortalis canicollis and its evolution in birds. The phallus of O. canicollis is intromittent, with a blind tubular cavity and two distinct regions when erect: the base of the phallus, which shows the mucosa smooth and lined by a pseudostratified columnar epithelium, and the tubular portion, which shows the mucosa lined by a keratinized stratified squamous epithelium with little knobs. The phallus includes two vascular bodies at the cranial portion in the urodeum. A fibrocartilaginous body anchors the tubular portion therefrom up to the eversible portion. A branched elastic ligament inserts on different regions of the
tubular portion. The phallus is plesiomorphic in birds and it has disappeared in Megapodius, Leipoa and Neoaves. The asymmetric phallus evolved early and it was retained in the basal branches of birds. The intromittent phallus is plesiomorphic in birds (found in Archosauria’s ancestor), but Crypturellus, Numididae, Odontophoridae and Phasianidae have developed a non- intromittent phallus a posteriori. The blind tubular cavity and the fibrocartilaginous body evolved as an adaptive convergence many times in birds. Therefore, this study shed some light on morphological aspects of the phallus and contributed to understand its evolution in birds.
... The ichthyosaur hind fin possibly had a function related to reproduction or locomotion. Male turtles and crocodilians possess a penis [92], but most fully terrestrial reptiles do not, and it is unknown in ichthyosaurs. Assuming their involvement in reproductive purposes, the hind fins could have played a role in coupling, or the pelvic girdle may have anchored the penis muscles, as in cetaceans [16]. ...
In spite of a fossil record spanning over 150 million years, pelvic girdle evolution in Ichthyopterygia is poorly known. Here, we examine pelvic girdle size relationships using quantitative methods and new ophthalmosaurid material from the Slottsmøya Member Lagerstätte of Svalbard, Norway. One of these new specimens, which preserves the most complete ichthyosaur pelvic girdle from the Cretaceous, is described herein as a new taxon, Keilhauia nui gen. et sp. nov. It represents the most complete Berriasian ichthyosaur known and the youngest yet described from the Slottsmøya Member. It is diagnosed on the basis of two autapomorphies from the pelvic girdle, including an ilium that is anteroposteriorly expanded at its dorsal end and an ischiopubis that is shorter or subequal in length to the femur, as well as a unique character combination. The Slottsmøya Member Lagerstätte ichthyosaurs are significant in that they represent a diverse assemblage of ophthalmosaurids that existed immediately preceding and across the Jurassic–Cretaceous boundary. They also exhibit considerable variation in pelvic girdle morphology, and expand the known range in size variation of pelvic girdle elements in the clade.
... Developmental patterns affect how tissues are arranged in the mature intromittent organ, and the material properties and arrangement of these tissues can influence how the organ achieves and maintains a specific shape (Kelly 1999(Kelly , 2013. Copulation also subjects both intromittent organs and the female genital tract to forces that can stress tissues in tension, compression, bending, torsion, or shear (Wainwright et al. 1976). ...
Intromittent organs are structures that enter the female genital tract and deposit sperm; these organs are found in many animal taxa that use internal fertilization. Despite their shared function, they are fantastically diverse morphologically. Many of their species-specific shape differences are likely the result of sexual selection and coevolution between male and female reproductive tracts, but a growing number of studies have identified other factors that can also affect their functional anatomy. In this symposium, we united scientists who combine morphological methods with contemporary molecular, phylogenetic, and imaging techniques to study the reproductive performance of intromittent organs in invertebrate and vertebrate model systems. The result was a collection of studies discussing competing selective pressures that act on these structures, including the effects of life history, genes and development, sexual conflict, ecological interactions, the biomechanics of copulation, and phenotypic plasticity. There was also an overwhelming consensus that a full understanding of intromittent organ evolution will not be possible without complimentary studies of morphology and function in female reproductive tracts.
... For example, lizards and snakes (squamates) have two penises instead of one, known as hemipenes, erected by either just blood [2], or a combination of blood and lymph [7]. Crocodiles have a stiff dense collagenous organ with minimal blood erectile potential that is inserted into the female cloaca by well-developed muscles [8]. Ducks have a penis that everts explosively inside the female and is inflated by lymphatic fluid [2,9]. ...
Amniote penises come in many shapes but are missing from the basal tuatara. This has been taken as evidence for multiple evolutionary origins of the penis. Now, genital swellings have been found in tuatara embryos, arguing for a single origin.
... There is a glans (glans penis) of cavernous tissue at the extremity of the phallus. When engorged with blood, the corpora cavernosa enlarge and shape the sulcus spermaticus into a duct through which sperm flows and protrude the glans from the cloacal vent enabling its insertion into the cloaca of the female (Kelly, 2013). ...
Objectives: Mugger crocodiles breed twice in a year under captivity resulting in over population; requiring birth control measures. As the testis and vas deferens are intra-abdominal, the efficacy of surgical ablation of sulcus spermaticus that transport the sperm during copulation, on the dorsal surface of the phallus was assessed. Methods: Twelve male crocodiles weighing between 140 to 230 kg were immobilized and anaesthetized with a combination of xylazine-ketamine at the dose rate of 1.5 and 20 mg/kg body weight respectively. Under aseptic precautions the phallus was retracted through cloacal slit as the animal was positioned on dorsal recumbency. The mucous membrane guarding the groove and floor were resected to ablate the sulcus spermaticus and the mucous membrane on either side was sutured. After 6 to 8 months randomly 6 crocodiles were immobilized and the phallus was examined, which revealed no signs of regeneration of the groove. Conclusion: The study revealed that ablation of sulcus spermaticus could be followed as a birth control surgery in male mugger crocodiles without affecting the welfare and breeding behavior.
... In many amniotes, erection of the phallus is achieved by muscle contraction in addition to hydrostatic pressure. Anatomical studies have proposed a different mechanism for crocodilia, in which the penis is protruded from the vent by adjacent cloacal musculature; both the sphincter cloacae and levator cloacae muscles have been implicated in this process [Powell, 1999;Kelly, 2013]. In squamates, the transversus penis muscle acts to evert the hemipenes, whereas the retractor penis magnus functions in retraction [Ruiz and Wade, 2002]. ...
External genitalia are found in each of the major clades of amniotes. The phallus is an intromittent organ that functions to deliver sperm into the female reproductive tract for internal fertilization. The cellular and molecular genetic mechanisms of external genital development have begun to be elucidated from studies of the mouse genital tubercle, an embryonic appendage adjacent to the cloaca that is the precursor of the penis and clitoris. Progress in this area has improved our understanding of genitourinary malformations, which are among the most common birth defects in humans, and created new opportunities for comparative studies of other taxa. External genitalia evolve rapidly, which has led to a striking diversity of anatomical forms. Within the past year, studies of external genital development in non-mammalian amniotes, including birds, lizards, snakes, alligators, and turtles, have begun to shed light on the molecular and morphogenetic mechanisms underlying the diversification of phallus morphology. Here, we review recent progress in the comparative developmental biology of external genitalia and discuss the implications of this work for understanding external genital evolution. We address the question of the deep homology (shared common ancestry) of genital structures and of developmental mechanisms, and identify new areas of investigation that can be pursued by taking a comparative approach to studying development of the external genitalia. We propose an evolutionary interpretation of hypospadias, a congenital malformation of the urethra, and discuss how investigations of non-mammalian species can provide novel perspectives on human pathologies. © 2014 S. Karger AG, Basel.
Sexual identification of crocodilians is important in population studies and provides useful information for conservation and management plans and monitoring populations over time. It is possible to distinguish between male and female Caiman latirostris by cloacal palpation or eversion of the penis in individuals larger than 75 cm total length, but smaller animals possess a barely differentiable cliteropenis. In hatchlings, sex determination methods involve surgical examination, necropsy, or analysis of cranial dimorphism, which cannot be applied in the field. We classified hatchlings of C. latirostris by observing the color and shape of their genitals. The penis is a milky white organ with a rounded shape at the tip and a purple hue at the end, whereas the clitoris is shorter, whitish, and has a pointed end. The procedure was tested on hatchlings from three nests at the Proyecto Yacar study area (Santa Fe province); half of the eggs of each nest were incubated at a constant temperature of 31C (producing females) and the other half at 33C (producing males). To observe the sexual organs by cloacal inspection, we used a modified instrument whose function during palpation is like that of a finger applied in large animals to evert the penis or clitoris. In the first days after hatching we correctly scored the sex of 80% of the individuals. The number of correct identifications was slightly lower for males than for females. This technique might be a useful tool for field studies, as it allows the sex of small caimans to be estimated in situ.
We compare and contrast the signalling systems and social behaviors of Alligator mississippiensis, Crocodylus aculus, and Crocodylus mloticus. Our qualitative analysis focuses primarily on the behaviors of adults during three phases of reproduction: I. Defense of Territory and Courtship, II. Nesting and Incubation, and III. Hatching and Post Hatching. Signals and signal elements are very similar among the three species. For example, all have vocal, non-vocal acoustic, and visual signals, some transmitted through air or water and others through both media. In addition, each species' repertoire is composed of discrete, graded and complex signals. A few signals are unique to each species. However, their signalling systems differ in the temporal organization of the behaviors, and in the relative frequency in which certain functional groups of signals occuror in which signals occur in a particular sensory mode. Apparently, the signalling systems of C. acutus and C. niloticus are more similar to each other than either is to the signalling system of A. mississippiensis. The signalling systems of the crocodile species appear to be adapted to open water habitats in which visual signals are advantageous and to high density breeding groups and post-copulatory intersexual contact. In contrast, the Alligatorsignalling system appears adapted to a marsh habitat in which vocal signals are likely favored and to low density breeding groups.
An histological description of the male genital apparatus of 9 mature wild spectacled caimans (Caiman crocodilus crocodi- lus) from Apure Plains, Venezuela, was carried out; the sam- ples obtained by necropsy were fixed in formalin to 10% buff- ered to pH 7.0 processed by means of the paraffin inclusion technique and stained with the routine Haematoxylin-Eosin and Mallory's Tricromic stains. The most important discoveries were: great spermatogenic activity, evidence of granules of se- cretion whit acid-stain affinity in some cases, and without stain affinity in others, in different segments of the epididymis, pres- ence of glands of mucous secretion in the ejaculatory groove, and great quantity of erectile tissue at level of this groove and along the penis.
The erection mechanism of the penis in most vertebrates is blood vascular. A major evolutionary transition occurred in birds, where the erection mechanism changed from blood vascular to lymphatic. Within birds, however, the erection mechanism of the ratite penis has remained unknown. Early work suggested that the erection mechanism in ostrich Struthio camelus was blood vascular while no description existed for the emu Dromaius novaehollandiae or the rhea Rhea ameri-cana. Because the penis in all other described birds has a lymphatic erection mechanism, clarifying that the erection mechanism of ratites is of great importance to understanding one of the major evolutionary transitions of penis morphology within amniotes. Here, we show that the erection mechanism of ratites is lymphatic, confirming that the evolutionary transition to lymphatic erection occurred in the last common ancestor of Aves.
We present the first genomic-scale analysis addressing the phylogenetic position of turtles, using over 1000 loci from representatives of all major reptile lineages including tuatara. Previously, studies of morphological traits positioned turtles either at the base of the reptile tree or with lizards, snakes and tuatara (lepidosaurs), whereas molecular analyses typically allied turtles with crocodiles and birds (archosaurs). A recent analysis of shared microRNA families found that turtles are more closely related to lepidosaurs. To test this hypothesis with data from many single-copy nuclear loci dispersed throughout the genome, we used sequence capture, high-throughput sequencing and published genomes to obtain sequences from 1145 ultraconserved elements (UCEs) and their variable flanking DNA. The resulting phylogeny provides overwhelming support for the hypothesis that turtles evolved from a common ancestor of birds and crocodilians, rejecting the hypothesized relationship between turtles and lepidosaurs.
Phalli of male crocodilians transfer sperm to female cloaca during sexual intercourse, resulting in internal fertilization. For over a century there have been scientific descriptions of crocodilian phallus morphologies; however, little work has presented detailed cellular-level analyses of these structures. Here we present a histological investigation of the complex functional anatomy of the juvenile male American alligator phallus, including fibrous and vascular erectile structures, a variety of secretory epithelium morphologies, and observed immune cells. Using 3D reconstruction software, we show the shape and location of vascular erectile tissues within the phallus. Histochemical staining detected mucin-rich secretory cells in glandular epithelial cells of the phallic shaft and also of the semen-conducting ventral sulcus. Lymphoid aggregates, lymphocytes, and epithelial mucin coats suggest an active immune system in the phallus defending from both the external and intracloacal environments. These results better characterize the complexity of the alligator phallus and predict later reproductive functions during adulthood.
Despite much interest in amniote systematics, the origin of turtles remains elusive. Traditional morphological phylogenetic analyses place turtles outside Diapsida-amniotes whose ancestor had two fenestrae in the temporal region of the skull (among the living forms the tuatara, lizards, birds and crocodilians)-and allied with some unfenestrate-skulled (anapsid) taxa. Nonetheless, some morphological analyses place turtles within Diapsida, allied with Lepidosauria (tuatara and lizards). Most molecular studies agree that turtles are diapsids, but rather than allying them with lepidosaurs, instead place turtles near or within Archosauria (crocodilians and birds). Thus, three basic phylogenetic positions for turtles with respect to extant Diapsida are currently debated: (i) sister to Diapsida, (ii) sister to Lepidosauria, or (iii) sister to, or within, Archosauria. Interestingly, although these three alternatives are consistent with a single unrooted four-taxon tree for extant reptiles, they differ with respect to the position of the root. Here, we apply a novel molecular dataset, the presence versus absence of specific microRNAs, to the problem of the phylogenetic position of turtles and the root of the reptilian tree, and find that this dataset unambiguously supports a turtle + lepidosaur group. We find that turtles and lizards share four unique miRNA gene families that are not found in any other organisms' genome or small RNA library, and no miRNAs are found in all diapsids but not turtles, or in turtles and archosaurs but not in lizards. The concordance between our result and some morphological analyses suggests that there have been numerous morphological convergences and reversals in reptile phylogeny, including the loss of temporal fenestrae.
Coevolution of male and female genitalia in waterfowl has been hypothesized to occur through sexual conflict. This hypothesis raises questions about the functional morphology of the waterfowl penis and the mechanics of copulation in waterfowl, which are poorly understood. We used high-speed video of phallus eversion and histology to describe for the first time the functional morphology of the avian penis. Eversion of the 20 cm muscovy duck penis is explosive, taking an average of 0.36 s, and achieving a maximum velocity of 1.6 m s(-1). The collagen matrix of the penis is very thin and not arranged in an axial-orthogonal array, resulting in a penis that is flexible when erect. To test the hypothesis that female genital novelties make intromission difficult during forced copulations, we investigated penile eversion into glass tubes that presented different mechanical challenges to eversion. Eversion occurred successfully in a straight tube and a counterclockwise spiral tube that matched the chirality of the waterfowl penis, but eversion was significantly less successful into glass tubes with a clockwise spiral or a 135 degrees bend, which mimicked female vaginal geometry. Our results support the hypothesis that duck vaginal complexity functions to exclude the penis during forced copulations, and coevolved with the waterfowl penis via antagonistic sexual conflict.
http://deepblue.lib.umich.edu/bitstream/2027.42/57083/1/OP647.pdf
In mammalian embryos, male and female external genitalia develop from the genital tubercle. Outgrowth of the genital tubercle is maintained by the urethral epithelium, and it has been reported that Fgf8 mediates this activity. To test directly whether Fgf8 is required for external genital development, we conditionally removed Fgf8 from the cloacal/urethral epithelium. Surprisingly, Fgf8 is not necessary for initiation, outgrowth or normal patterning of the external genitalia. In early genital tubercles, we found no redundant Fgf expression in the urethral epithelium, which contrasts with the situation in the apical ectodermal ridge (AER) of the limb. Analysis of Fgf8 pathway activity showed that four putative targets are either absent from early genital tubercles or are not regulated by Fgf8. We therefore examined the distribution of Fgf8 protein and report that, although it is present in the AER, Fgf8 is undetectable in the genital tubercle. Thus, Fgf8 is transcribed, but the signaling pathway is not activated during normal genital development. A phylogenetic survey of amniotes revealed Fgf8 expression in genital tubercles of eutherian and metatherian mammals, but not turtles or alligators, indicating that Fgf8 expression is neither a required nor a conserved feature of amniote external genital development. The results indicate that Fgf8 expression is an early readout of the genital initiation signal rather than the signal itself. We propose that induction of external genitalia involves an epithelial-epithelial interaction at the cloacal membrane, and suggest that the cloacal ectoderm may be the source of the genital initiation signal.
The ecology and reproductive biology of chelonians have received a great deal of attention. Many publications focus on the ecology or reproductive biology of a single species (e.g., Macrochelys temminckii: Pritchard, 2006; Chelydra serpentina: White & Murphy, 1973; Geochelone radiata: Auffenberg, 1978; Trachemys scripta: Moll & Legler, 1971; Gibbons, 1990; Gopherus polyphemus: Iverson, 1980; Chrysemys picta: Zweifel, 1989; Iverson & Smith, 1993; Apalone ferox: Iverson & Moler, 1997; Webb, 1956; Chelodina novaeguineae: Kennett et al., 1992). Some studies provide comparative information on reproductive behaviors and biology of two or more species (e.g., Chelydra serpentina, Apalone, Macrochelys, Trachemys), and some contain drawings or pictures of pre-copulatory and mating behavior of different species (e.g., Legler, 1955; Webb, 1961, 1962; Auffenberg, 1978; Bellairs, 1970; Bustard, 1972; LeBuff, 1990; Obst, 1986; Oliver, 1955; Dodd, 2001; Ewert, 1976; Harrel et al., 1996). Some provide comparative information on the biology and ecology of multiple species grouped by general habitat; for example, river turtles (Moll & Moll, 2004) and sea turtles (Lutz & Musick, 1997; Lutz et al., 2002). Still others summarize the information concerning multiple species over large geographic areas (Australia: Legler, 1985; Cann, 1998; Venezuela: Pritchard & Trebbau, 1984). Some species and groups have received more attention than others as a result of their accessibility (e.g., Pseudemys concinna: Seidel & Dreslik, 1996; Trachemys scripta: Seidel & Ernst, 2006; Terrapene carolina: Ernst & McBreen, 1991), distribution (e.g., Chelydra serpentina: Ernst et al., 1988; Gibbons et al., 1988; Lovich, 1993; Apalone: Webb, 1990), or conservation status (Swingland & Klemens, 1989; Van Abbema, 1997; Klemens, 2000).
Wild caught, captive alligators (Alligator mississippiensis) over a seven-year period exhibited a successful nesting rate of 48 percent in six pens maintained on Rockefeller Refuge. Hatching success in pens (56 percent) closely correlated the 58 percent determined for wild alli-gators inhabiting natural marsh. Pen construction methods, stocking rates, and maintenance techniques were implemented to simulate natural marsh conditions, thereby en-couraging breeding and contributing to the well being of the alligators. Diseases posed no problem during this investigation although fighting did cause some concern during the early stages of the study. Courtship activities, nest construction techniques and maternal duties following egg laying were highly variable among the various alligators under study. Also, courtship behavior was highly ritualized. Behavior of pen reared alligators as compared to wild captured adult alligators were compared. Stocking rates were found to differ greatly. Pen reared adult animals could be maintained in much closer confine-ment and under less stress when compared to wild captured adults. INTRODUCTION Alligators have been kept in captivity throughout Louisiana for many years. However, only on rare occasions do they reproduce under captive conditions. As alligators are easily maintained in captivity and fairly disease free, in the past they were sold by the thousands in Louisiana as pets. Also, alligator hunters would capture young alligators at a nest site and return home to confine them to some type of make shift pen under the pretense of starting an "alligator farm".
Solid Biomechanicsis the first book to comprehensively review the mechanical design of organisms. With a physical approach and a minimum of mathematics, the textbook introduces readers to the world of structural mechanics and sheds light on the dazzling array of mechanical adaptations that link creatures as dissimilar as bacteria, plants, and animals. Exploring a wide range of subjects in depth, from spider silks and shark skin to climbing plants and human food processing, this immensely accessible text demonstrates that the bodies of animals and plants are masterpieces of engineering, enabling them to survive in a hostile world. The textbook describes how organisms construct materials from limited components, arrange materials into efficient structures that withstand different types of stresses, and interact mechanically with their environment. Looking at practical and historical aspects of the subject, the book delves into how the mechanics of organisms might be applied to other engineering scenarios and considers the ways structural biomechanics could and should develop in the future if more is to be learned about the form and function of organisms.Solid Biomechanicswill be useful to all those interested in how organisms work, from biologists and engineers to physicists and students of biomechanics, bionics, and materials science. The first comprehensive review of the structural mechanics of organisms Introduces the subject using a physical approach involving minimal mathematics Three complementary sections: materials, structures, and mechanical interactions of organisms Links the dazzling array of mechanical adaptations seen in widely differing organisms Practical and historical approach shows how mechanical adaptations have been discovered and how readers can perform their own investigations.
Modern cetaceans possess a suite of morphological adaptations that permit their existence in the marine environment (e.g., Howell, 1930; Slijper, 1936, 1979). Their streamlined body shape, hypertrophied axial musculoskeletal system, thick blubber layer, and de novo dorsal fin and flukes are morphological features that reduce the energetic costs of both swimming (e.g., Fish and Hui, 1991; Williams et al., 1992; Fish, 1993a,b; Pabst, 1996) and whole body thermoregulation (e.g., Worthy and Edwards, 1990; Koopman et al., 1996).
The erection mechanism of the penis in most vertebrates is blood vascular. A major evolutionary transition occurred in birds, where the erection mechanism changed from blood vascular to lymphatic. Within birds, however, the erection mechanism of the ratite penis has remained unknown. Early work suggested that the erection mechanism in ostrich Struthio camelus was blood vascular while no description existed for the emu Dromaius novaehollandiae or the rhea Rhea americana. Because the penis in all other described birds has a lymphatic erection mechanism, clarifying that the erection mechanism of ratites is of great importance to understanding one of the major evolutionary transitions of penis morphology within amniotes. Here, we show that the erection mechanism of ratites is lymphatic, confirming that the evolutionary transition to lymphatic erection occurred in the last common ancestor of Aves.
It is becoming increasingly clear that cells behave differently in two-dimensional (2D) culture than in three-dimensional
(3D) tissues, and that 3D culture models and new tools for probing them are needed for advancing our knowledge of mechanobiology.
Cells physically interact with their surrounding extracellular matrix; they are able to sense the local stiffness, tension,
and deformation within the matrix and, in turn, are able to remodel the matrix and generate forces with long-range effects.
In tissues with sufficiently high cell density, the cells interact and generate coordinated forces which can be regulated
by controlling the macroscopic mechanical boundary conditions. Understanding this dynamic reciprocity between the cells, matrix,
and external environment is critical for determining how the cells sense, transduce, and respond to their mechanical surroundings.
However, even in simplified models of 3D tissues, quantification of local (non-linear viscoelastic) mechanical properties
is problematic, and the transfer of strain and stress to the cells is complicated by non-affine, non-uniform deformation of
the cell/matrix composite. This review focuses on methods for characterizing and modulating the mechanical environment of
cells cultured within reconstituted collagen gels, the most extensively utilized in vitro models of native 3D tissue.
The reproductive cycle of the American alligator, Alligator mississippiensis, was studied using blood and tissue samples from wild alligators, and blood samples drawn from a captive breeding stock at the Rockefeller Wildlife Refuge in Louisiana. Generally the cycle commences in March as air and water temperatures increase. By early April the seminiferous tubules are full of actively dividing spermatocytes and maturing spermatids. Testis mass is greatest at this time and plasma testosterone is at a peak (>50 ng/ml), but mature spermatozoa do not appear until late April and mid May when mating takes place. Plasma testosterone levels decline rapidly in June after spermiation, and are low to nondetectable in July and August when the testes are fully regressed. A second small peak in testosterone occurs in September without any obvious changes in testicular histology. In the female a similar temperature dependent initiation of the ovarian cycle occurs in late March. Plasma estradiol levels reach a peak (>600 pg/ml) in mid April, and ovarian follicles increase from 5 mm to 45 mm in diameter at ovulation in May. Plasma testosterone is also high in preovulatory females (ca. 1.5 ng/ml). Plasma progesterone shows a periovulatory surge to levels as high as 16 ng/ml, but declines rapidly during the 3½ wk between ovulation and oviposition. During egg incubation (66 days) when the female remains close to the nest, ovarian steroids remain undetectable.
Arich material of Crocodiles and Alligators has enabled me to clear up several points in the structure of their sexual apparatus, which have hitherto escaped notice, probably owing to the scarcity of suitable specimens. This latter difficulty has been removed in my case by the liberality of the University of Cambridge and of the Royal Society, which has enabled me, in conjunction with Dr. Gaskell, to construct a special house to keep alive, and in a healthy condition, a considerable number of Reptiles of all orders.
For the purpose of defending itself against predators, the balloonfish (Diodon holocanthus) can triple its body volume by pumping water into its stomach. Diodon holocanthus exhibits striking structural and functional specializations for inflation. The stomach of the balloonfish is highly extensible and has lost its digestive function, it is repeatedly folded upon itself and is lined with transitional epithelium. The peritoneal cavity of the balloonfish is also large and extensible. During inflation, the stomach expands into an existing peritoneal space surrounding the axial musculature and presses the folded peritoneum out into potential peritoneal spaces ventral to the head and surrounding the dorsal fin, anal fin, and caudal peduncle; only the dorsal and lateral surfaces of the head are unaffected. Balloonfish skin is also specialized for inflation. Because the collagen fibers in the dermis of unstretched skin are wavy, little force is required to extend the skin up to 40% of its rest length. At high strains, the collagen fibers are stressed directly and the skin suddenly becomes stiff. Stiff skin surrounding a ball of incompressible water provides a rigid framework for the support of the erectile spines, and the balloonfish becomes a formidable, spiny sphere. However, not all of the structural and functional features that contribute to the ability of balloonfish to inflate are evolutionary adaptations specifically for inflation. Absence of pleural ribs, absence of a pelvis, and the orthogonal arrangement of dermal collagen sheets in the skin were all present in the ancestor of pufferfishes, and thus, must be considered exaptations. Sagittal plane flexibility of the vertebral column may be an epiphenomenon of the lengthening of the body cavity for more spherical inflation. Together these structural and functional features—whether adaptations, exaptations, or epiphenomena—combine to produce a highly effective mechanical defense. © 1994 Wiley-Liss, Inc.
The grooved throat wall of fin whales, Balaenoptera physalus, extends tremendously during feeding causing the whale to expand its profile from a cigar shape to the shape of an elongated, bloated tadpole. Ventral groove blubber associated with the engulfing feeding mechanism can be extended reversibly to as much as 4 times its resting length in the circumferential direction, and to 1.5 times its resting length along the long axis of the body. The muscle in the throat wall can be reversibly extended up to 3 times its resting length. Both these tissues have large amounts of the protein elastin in their microstructures that may function in retracting the expanded buccal cavity. Calculations of forces contributing to the expansion of the buccal cavity show that the engulfing process in feeding can be powered solely by the speed of swimming.
1. Lake Rudolf, nothern Kenya, has one of the largest undisturbed populations of the Nile Crocodile. In 1965 the Kenya Game Department initiated the Lake Rudolf Crocodile Research Project. Central Island, where the crocodiles live under undisturbed conditions, was chosen for studying breeding behaviour and ecology of the reptile. Eight months were spent on the island.
2. On the island most of the crocodile population was confined to a crater lake, Lake C, which supported up to 500 animate at the height of the 1965-66 breeding season.
3. The 1200 m shoreline of Lake C was shared out between about a dozen large males each guarding his territory by patrolling up and down the shore. The territorial shore lengths ranged from 60 to 230 m. The territories extended about 50 m into the water.
4. The crocodiles were first seen courting on 10.10.65 in Lake C. The territorial males exhibited a “courtship splash display”. Copulation ranged from 30 to 100 seconds; eleven copulations averaged 58 seconds.
5. The factors important in site selection for nesting are shade, suitable soil, proximity to water and the degree of slope of the shore. Because the shores of a second crater lake, Lake A, satisfied these conditions they had the largest number of nests. The fully exposed sites on Lake C, and the Lake Rudolf shores, had very few nests.
6. The females dig the nests with their forelimbs, using them in turn. The hind limbs and the belly are used to push away the soil collecting at the mouth of the burrow. The female guards the nest constantly throughout the incubation period of three months against monitor luzards. Laying began in the third week of November, 1965 reaching its peak during the second week of December. The crocodile egg is oblong, measuring 55.5 to 89.0 mm in length and 43.0 to 54.0 mm in width. Mean weights of the eggs from 15 clutches ranged from 83.7 to 126.6 g. Clutch sizes on Central Island varied from 14 to 46 eggs, giving a mean of 33 eggs per clutch.
When the young are about to hatch, the mother releases them by digging up the nest. The young when they hatch are about 31.0 cm long and weigh about 76.8 g. They are guarded by the mother for at least six weeks. Infant mortality is probably very considerable.
The relationship of the hemipenis to the cloaca in copula and sperm storage and transport in the female oviduct were studied in Anolis carolinensis using light and scanning electron microscopy. During copulation, the hemipenis does not penetrate beyond the cloaca, but the two apical openings of the bifurcate sulcus spermaticus appose the openings of the oviducts from the cloaca. Sperm enter the sperm storage tubules between 2 and 6 hr after insemination and small amounts of sperm reach the infundibulum 6 to 24 hr following mating. Sperm storage tubules are embedded in the wall of the utero-vaginal transition, and are formed by the folding and fusion of the oviducal epithelium. The importance of the hemipenile-cloacal relationship and the role of sperm storage in the life history of A. carolinensis are discussed.
Artificial inflation of corpora cavernosa from the nine-banded armadillo (Dasypus novemcinctus) showed that the expansion of the tunica albuginea during erection increases both components of flexural stiffness: the second moment of area and Young's modulus of elasticity. Folded tissue and crimped collagen fibers in the tunica albuginea permit its expansion during erection. As the tunica albuginea's radii increase in size, its second moment of area also increases. The crimped collagen fibers permit the flaccid tunica albuginea to expand to strains of 25 % longitudinally and 15 % circumferentially, after which tissue stiffness increases by 3-4 orders of magnitude. Radial expansion of the corpus cavernosum is limited by collagenous trabeculae. The trabeculae maintain the non-circular cross section of the corpus cavernosum during erection. Restricting expansion appears to protect the corpus spongiosum and urethra from occlusion, but has the side effect of reducing the potential flexural stiffness of the corpus cavernosum by reducing the second moment of area of the tunica albuginea.
The cloacal complex of Crocodylus porosus is composed of three chambers (proctodaeum, urodaeum, and coprodaeum) separated by tight, muscular sphincters. The proctodaeum is proximal to the cloacal vent and houses the genitalia. The urodaeum is the largest chamber, is capable of storing large quantities of urine, and is lined with an epithelium with the capacity for transepithelial water and ion exchange. The coprodaeum, the most orad cloacal chamber, is a small, only marginally expandable chamber that has an epithelium composed almost entirely of mucus-secreting cells. The coprodaeum and lower intestine are reported to be the site(s) for urine modification in birds and bladderless lizards. A radiographic trace of urine storage in C. porosus kept for 2 months under hyperosmotic conditions showed no signs of retrograde movement of urine into the coprodaeum or rectum. Instead, urine was stored in the urodaeum of C. porosus. Examination of the mucosal surface of the urodaeum by SEM showed a plastic response to environmental salinity, with a possible increase in surface area in animals kept in hyperosmotic water compared with animals from fresh water. We propose the urodaeum as the primary site for postrenal modification of urine in C. porosus.
Sexual dimorphisms in neuromuscular systems have been investigated in several vertebrate groups, but data on reptiles are limited. The present studies were designed to establish the copulatory neuromuscular system of the green anole lizard (Anolis carolinensis) as an appropriate model. Like mammals, male reptiles have copulatory organs. However, each individual has two "hemipenes" that are controlled by bilateral sets of muscles. First, the anatomy of the hemipenes and associated muscles was described in males and the same anatomical region examined in females. Second, spinal motoneurons innervating one of these muscles, the transversus penis (TPN), were localized by using the retrograde tracer biocytin. They were detected in the last trunk and first sacral segments (T17-S1). Third, motoneuron number and soma size were assessed in Nissl-stained sections of spinal cord segments T17-S1 of breeding males and females. Male-biased sexual dimorphisms were detected in both measures, but the motoneurons innervating a tail muscle, the caudifemoralis (CF), are also located in the same region of cord. Therefore, in the last study, the CF was injected with biocytin in both sexes to eliminate its motoneurons from the analysis and gain a more accurate representation of the TPN motoneuron pool. An equivalent number of CF motoneurons were labeled in both sexes, and the results from the previous study were replicated. Thus, similar to other vertebrate models, parallels between morphology and function exist in the green anole copulatory system. Future investigations will broaden the comparative perspective on mechanisms regulating sexual dimorphisms relating to reproductive behaviors in vertebrates.
Males in many modern amniote taxa have a hydraulic penis that inflates for copulation. Hydraulic skeletons are typically reinforced with inextensible fibres; the specific arrangement of the fibres within the skeleton determines whether it is flexible or resists bending. I show that the hydraulic skeleton in the turtle penis is reinforced by an axial orthogonal array of collagen fibres. This microanatomy is evolutionarily convergent with that of mammalian penises, and implies that there is a limited number of mechanical designs for an inflatable structure with high bending stiffness.
A captive Nile crocodile (Crocodylus niloticus) developed recurrent episodes of paraphimosis over a 2-yr period, which eventually led to hemorrhage and obvious inflammation. Two months postsurgery, the crocodile remained clinically normal.
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Breeding biology of the spectacled caiman, Caiman crocodilus crocodilus, in the Venezuelan llanos
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