Development of a phallus occurs in almost all amniotes; however, considerable variation in phallus morphology among different amniote lineages has contributed to the debate about their structural homology. Mammals are the only amniotes that form a closed urethral tube within the penis. In contrast, the phallus of reptiles and birds has an open urethral groove, or sulcus spermaticus, that facilitates directional flow of sperm along the penis. One condition of structural homology is that the organs should share a common developmental origin; de novo development from different embryonic progenitors would indicate that the structure re-evolved in a new position. Although a common developmental origin does not itself demonstrate homology, different origins could indicate a lack of homology. To further understand how development of external genitalia evolved in amniotes, we examined this in the turtle Trachemys scripta. We found that phallus development in the turtle closely resembles that of mice at the tissue, cellular, and molecular levels, consistent with the hypothesis that their phalluses are homologous structures. We find that acquisition of specialized characters, such as a closed urethral tube, involved lineage-specific specialization of the common plan for amniote phallus development.

1.
Baskin L, Erol A, Jegatheesan P, Li Y, Liu W, Cunha G: Urethral seam formation and hypospadias. Cell Tissue Res 305:379-387 (2001).
2.
Brennan PL, Birkhead TR, Zyskowski K, van der Waag J, Prum RO: Independent evolutionary reductions of the phallus in basal birds. J Avian Biol 39:487-492 (2008).
3.
Briskie JV, Montgomerie R: Sexual selection and the intromittent organ of birds. J Avian Biol 28:73-86 (1997).
4.
Carmichael SL, Ma C, Choudhry S, Lammer EJ, Witte JS, Shaw GM: Hypospadias and genes related to genital tubercle and early urethral development. J Urol 190:1884-1892 (2013).
5.
Chen T, Li Q, Xu J, Ding K, Wang Y, et al: Mutation screening of BMP4, BMP7, HOXA4 and HOXB6 genes in Chinese patients with hypospadias. Eur J Hum Genet 15:23-28 (2007).
6.
Cobb J, Duboule D: Comparative analysis of genes downstream of the Hoxd cluster in developing digits and external genitalia. Development 132:3055-3067 (2005).
7.
Greenbaum E: A standardized series of embryonic stages for the emydid turtle Trachemys scripta. Can J Zool 80:1350-1370 (2002).
8.
Haraguchi R, Mo R, Hui C, Motoyama J, Makino S, et al: Unique functions of sonic hedgehog signaling during external genitalia development. Development 128:4241-4250 (2001).
9.
Herrera AM, Shuster SG, Perriton CL, Cohn MJ: Developmental basis of phallus reduction during bird evolution. Curr Biol 23:1065-1074 (2013).
10.
Hosken DJ, Stockley P: Sexual selection and genital evolution. Trends Ecol Evol 19:87-93 (2004).
11.
Hynes PJ, Fraher JP: The development of the male genitourinary system. I. The origin of the urorectal septum and the formation of the perineum. Br J Plast Surg 57:27-36 (2004).
12.
Kalfa N, Philibert P, Sultan C: Is hypospadias a genetic, endocrine or environmental disease, or still an unexplained malformation? Int J Androl 32:187-197 (2009).
13.
Kardong K: Vertebrates: Comparative Anatomy, Function, and Evolution, ed 3 (McGraw-Hill, Boston 2002).
14.
Kelly DA: The functional morphology of penile erection: tissue designs for increasing and maintaining stiffness. Integr Comp Biol 42:216-221 (2002).
15.
Kelly DA: Turtle and mammal penis designs are anatomically convergent. Proc Biol Sci 271: S293-S295 (2004).
16.
King A: Form and Function in Birds, vol 2 (Academic Press, New York 1981).
17.
Laufer E: BMP expression in duck interdigital webbing: a reanalysis. Science 278:305-305 (1997).
18.
Lin C, Yin Y, Veith GM, Fisher AV, Long F, Ma L: Temporal and spatial dissection of Shh signaling in genital tubercle development. Development 136:3959-3967 (2009).
19.
Lombardi J: Comparative Vertebrate Reproduction (Kluwer Academic Publishers, Boston 1998).
20.
Morgan EA: Loss of Bmp7 and Fgf8 signaling in Hoxa13-mutant mice causes hypospadia. Development 130:3095-3109 (2003).
21.
Mortlock DP, Innis JW: Mutation of HOXA13 in hand-foot-genital syndrome. Nat Genet 15:179-180 (1997).
22.
Moustakas JE: Development of the carapacial ridge: implications for the evolution of genetic networks in turtle shell development. Evol Dev 10:29-36 (2008).
23.
Nieto MA, Patel K, Wilkinson DG: In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219-235 (1996).
24.
Nievelstein RA, van der Werff JF, Verbeek FJ, Valk J, Vermeij-Keers C: Normal and abnormal embryonic development of the anorectum in human embryos. Teratology 57:70-78 (1998).
25.
Paulozzi LJ, Erickson JD, Jackson RJ: Hypospadias trends in two US surveillance systems. Pediatrics 100:831-834 (1997).
26.
Perriton CL, Powles N, Chiang C, Maconochie MK, Cohn MJ: Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26-46 (2002).
27.
Petiot A, Perriton CL, Dickson C, Cohn MJ: Development of the mammalian urethra is controlled by Fgfr2-IIIb. Development 132:2441-2450 (2005).
28.
Qi BQ, Beasley SW, Williams AK, Frizelle F: Apoptosis during regression of the tailgut and septation of the cloaca. J Pediatr Surg 35:1556-1561 (2000a).
29.
Qi BQ, Williams A, Beasley S, Frizelle F: Clarification of the process of separation of the cloaca into rectum and urogenital sinus in the rat embryo. J Pediatr Surg 35:1810-1816 (2000b).
30.
Raynaud A, Pieau C: Embryonic development of the genital system, in Gans C, Billett F: (eds): Biology of the Reptilia, vol 15, pp 149-300 (John Wiley and Sons, New York 1985).
31.
Romer A, Parsons T: The Vertebrate Body, ed 6 (Saunders, Philadelphia 1986).
32.
Sasaki C, Yamaguchi K, Akita K: Spatiotemporal distribution of apoptosis during normal cloacal development in mice. Anat Rec A Discov Mol Cell Evol Biol 279:761-767 (2004).
33.
Satoh Y, Haraguchi R, Wright TJ, Mansour SL, Partanen J, et al: Regulation of external genitalia development by concerted actions of Fgf ligands and Fgf receptors. Anat Embryol 208:479-486 (2004).
34.
Seifert AW, Harfe BD, Cohn MJ: Cell lineage analysis demonstrates an endodermal origin of the distal urethra and perineum. Dev Biol 318:143-152 (2008).
35.
Seifert AW, Bouldin CM, Choi KS, Harfe BD, Cohn MJ: Multiphasic and tissue-specific roles of sonic hedgehog in cloacal septation and external genitalia development. Development 136:3949-3957 (2009a).
36.
Seifert AW, Yamaguchi T, Cohn MJ: Functional and phylogenetic analysis shows that Fgf8 is a marker of genital induction in mammals but is not required for external genital development. Development 136:2643-2651 (2009b).
37.
Seifert AW, Zheng Z, Ormerod BK, Cohn MJ: Sonic hedgehog controls growth of external genitalia by regulating cell cycle kinetics. Nat Commun 1:23 (2010).
38.
Suzuki K, Ogino Y, Murakami R, Satoh Y, Bachiller D, Yamada G: Embryonic development of mouse external genitalia: insights into a unique mode of organogenesis. Evol Dev 4:133-141 (2002).
39.
Suzuki K, Bachiller D, Chen YP, Kamikawa M, Ogi H, et al: Regulation of outgrowth and apoptosis for the terminal appendage: external genitalia development by concerted actions of Bmp signaling [corrected]. Development 130:6209-6220 (2003).
40.
Tuzel E, Samli H, Kuru I, Turkmen S, Demir Y, et al: Association of hypospadias with hypoplastic synpolydactyly and role of HOXD13 gene mutations. Urology 70:161-164 (2007).
41.
Wake MH: Hyman's Comparative Vertebrate Anatomy, ed 3 (The University of Chicago Press, Chicago 1979).
42.
Wang MH, Baskin LS: Endocrine disruptors, genital development, and hypospadias. J Androl 29:499-505 (2008).
43.
Wu X, Ferrara C, Shapiro E, Grishina I: Bmp7 expression and null phenotype in the urogenital system suggest a role in re-organization of the urethral epithelium. Gene Expr Patterns 9:224-230 (2009).
44.
Yntema C: A series of stages in the embryonic development of Chelydra serpentina. J Morphol 125:219-251 (1968).
45.
Yucel S, Dravis C, Garcia N, Henkemeyer M, Baker LA: Hypospadias and anorectal malformations mediated by eph/ephrin signaling. J Pediatr Urol 3:354-363 (2007).
46.
Zucker RM, Hunter ES, 3rd, Rogers JM: Confocal laser scanning microscopy of morphology and apoptosis in organogenesis-stage mouse embryos. Methods Mol Biol 135:191-202 (2000).
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.