Morphogenesis and Patterning of the Phallus and Cloaca in the American Alligator, <b><i>Alligator mississippiensis</i></b>

Abstract

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.

Evolution of External Genitalia: Insights from Reptilian Development

“…Similarly, among waterfowl, the phallus varies extensively in length, coiling pattern, and degree of ornamentation [Coker et al, 2002;Brennan et al, 2007]. Like turtles, crocodilians have notable variation in the morphology of the glans [Ziegler and Olbort, 2007;Gredler et al, 2014b]. For many squamate species, each hemipenis assumes a common general plan as a distally bilobed organ with rounded tips, although cylindrical, bulbous, and clavate morphologies have been described [Dowling and Savage, 1960].…”

“…Most of the work regarding hormonal regulation of turtle development has examined development of the gonads, but androgen likely has a role in development of the phenotypically male phallus, as androgen exposure in turtles causes accelerated growth and hypertrophy of the phallus [Wibbels and Crews, 1992;Crews et al, 1995;Crespo et al, 2013]. The role of estrogen in regu- [Larkins and Cohn , 2014], Alligator mississippiensis [Gredler et al, 2014b], Gallus gallus [Herrera et al, 2013], Anolis carolinensis [Gredler et al, 2014a], Python regius [Leal and Cohn, 2014], and Mus musculus [Perriton et al, 2002] lating development of the phallus is not clear, although estrogen is required for development of the ovary, and estrogen production may be upregulated in response to female-producing temperatures [Wibbels et al, 1991;Bergeron et al, 1999]. Examination of the phallus in androgen-or estrogen-treated turtles will be important to determine the role of hormones in turtle external genital development.…”

Resurrecting embryos of the tuatara, Sphenodon punctatus , to resolve vertebrate phallus evolution

“…Lett. 11: 20150694 that expand towards the midline, where they merge to form the genital tubercle, the precursor to the phallus [12,14,15,19]. The squamate hemiphallus also forms from paired swellings, but rather than merging at the midline, they remain separate to form two discrete phalluses [9,16,17].…”

Aphallia (Penile agenesis): A preliminary report of three cases

“…Either the absence of the genital tubercle or failure of genital tubercle to fully develop is responsible for this anomaly. Genitourinary anomalies such as renal agenesis or cystic kidney, horseshoe kidney, vesicoureteral reflux (VUR), prostate agenesis are found in about fifty-four percent of cases of aphallia [2][3][4]. Additionally, aphallia has also been reported with other abnormalities such as skeletal and neural disorders, annular pancreas, clubfoot and heart problems [2][3][4].…”

“…Genitourinary anomalies such as renal agenesis or cystic kidney, horseshoe kidney, vesicoureteral reflux (VUR), prostate agenesis are found in about fifty-four percent of cases of aphallia [2][3][4]. Additionally, aphallia has also been reported with other abnormalities such as skeletal and neural disorders, annular pancreas, clubfoot and heart problems [2][3][4]. Imminger was the first to report a case of aphallia in 1853 [5], and till date, less than 100 cases have been reported in literature.…”