Development of the cloaca, hemipenes, and hemiclitores in the green anole, anolis carolinensis

Sexual Development

Volumn 9, Issue 1, 2015, Pages 21-33

  Gredler, Marissa L ^a   Sanger, Thomas J ^a,b   Cohn, Martin J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Anolis; Cloaca; Development; External genitalia; Genital tubercle; Hemipenes; Reptiles; Squamates

Indexed keywords

AMNIOTA; ANOLIS; ANOLIS CAROLINENSIS; AVES; MAMMALIA; REPTILIA; SERPENTES; SQUAMATA; TESTUDINES;

ANIMAL; CLITORIS; CLOACA; EMBRYOLOGY; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENITAL SYSTEM; LIZARD; MALE; ORGANOGENESIS; PENIS; SEX DIFFERENTIATION;

ANIMALS; BIOLOGICAL EVOLUTION; CLITORIS; CLOACA; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA; LIZARDS; MALE; ORGANOGENESIS; PENIS; SEX DIFFERENTIATION;

EID: 84923382320     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000363757     Document Type: Article

References (69)

1. Ammini AC, Sabherwal U, Mukhopadhyay C, Vijayaraghavan M, Pandey J: Morphogenesis of the human external male genitalia. Pedriatr Surg Int 12: 401-406 (1997).
2. Andrew DJ, Ewald AJ: Morphogenesis of epithelial tubes: insights into tube formation, elongation, and elaboration. Dev Biol 341: 34-55 (2010).
3. Arnold EN: The hemipenis of lacertid lizards (Reptilia: Lacertidae): structure, variation and systematic implications. J Nat Hist 20: 1221-1257 (1986a).
4. Arnold EN: Why copulatory organs provide so many useful taxonomic characters: the origin and maintenance of hemipenial differences in lacertid lizards (Reptilia: Lacertidae). Biol J Linn Soc Lond 29: 263-281 (1986b).
5. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, Tabin CJ: Genetic analysis of the roles of BMP2, 4 and 7 in limb patterning and skeletogenesis. PLoS Genet 2:e216 (2005).
6. Beck LA, Wade J: Steroid receptor expression in the developing copulatory system of the green anole lizard (Anolis carolinensis) . Gen Comp Endocrinol 157: 70-74 (2008).
7. Bellinger MF: Embryology of the male external genitalia. Urol Clin North Am 8: 375-382 (1981).
8. Berg T, Rountree CB, Lee L, Estrada J, Sala FG, et al: Fibroblast growth factor 10 is critical for liver growth during embryogenesis and controls hepatoblast survival via -catenin activation. Hepatology 46: 1187-1197 (2007).
9. Beuchat CA: Phylogenetic distribution of the urinary bladder in lizards. Copeia 1986: 512-517 (1986).
10. Bitgood MJ, McMahon AP: Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 172: 126-138 (1995).
11. Bohme W, Ziegler T: A review of iguanian and anguimorph lizard genitalia (Squamata: Chamaeleonidae; Varanoidea, Shinisauridae, Xenosauridae, Anguidae) and their phylogenetic significance: comparisons with molecular data sets. J Zool Syst Evol Res 47: 189-202 (2009).
12. Brandley MC, Huelsenbeck JP, Wiens JJ: Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and longterm persistence of intermediate body forms. Evolution 62: 2042-2064 (2008).
13. Cohen RE, Roach J, Wade J: The distribution of estrogen receptor mRNA in male and female green anole lizards. Brain Res 1430: 43-51 (2012).
14. Cohn MJ: Development of the external genitalia: conserved and divergent mechanisms of appendage patterning. Dev Dyn 240: 1108-1115 (2011).
15. Conner J, Crews D: Sperm transfer and storage in the lizard, Anolis carolinensis . J Morphol 348: 331-348 (1980).
16. Crews D: Studies in squamate sexuality. Bioscience 30: 835-838 (1980).
17. Das M, Purkayastha J: Insight into hemipenial morphology of five species of Hemidactylus Oken, 1817 (Reptilia: Gekkonidae) of Guwahati, Assam, India. Hamadryad 36: 32-37 (2012).
18. De Moerlooze L, Spencer-Dene B, Revest JM, Hajihosseini M, Rosewell I, Dickson C: An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127: 483-492 (2000).
19. Dowling H, Savage J: A guide to the snake hemipenis: a survey of the basic structure and systematic characteristics. Zoologica 45: 17-25 (1960).
20. Fraser BA, Sato AG: Morphological sex differentiation in the human embryo: a light and scanning electron microscopic study. J Anat 165: 61-74 (1989).
21. Gadow H: Remarks on the cloaca and on the copulatory organs of the Amniota. Philos T Roy Soc B 178: 5-37 (1887).
22. Glenister TW: The origin and fate of the urethral plate in man. J Anat 88: 413-425 (1954).
23. Haraguchi R, Mo R, Hui CC, Motoyama J, Makino S, et al: Unique functions of Sonic hedgehog signaling during external genitalia development. Development 128: 4241-4250 (2001).
24. Herrera AM, Shuster SG, Perriton CL, Cohn MJ: Developmental basis of phallus reduction during bird evolution. Curr Biol 23: 1065-1074 (2013).
25. Holmes MM, Wade J: Sexual differentiation of the copulatory neuromuscular system in green anoles (Anolis carolinensis) : normal ontogeny and manipulation of steroid hormones. J Comp Neurol 489: 480-490 (2005).
26. Jadin RC, Parkhill RV: Hemipenis descriptions of Mastigodryas (Serpentes: Colubrinae) from northern Middle America, with comments on the use of hemipenial data in phylogenetics. Herpetol Notes 4: 207-210 (2011).
27. Kelly DA: The functional morphology of penile erection: tissue designs for increasing and maintaining stiffness. Integr Comp Biol 42: 216-221 (2002).
28. Keogh JS: Evolutionary implications of hemipenial morphology in the terrestrial Australian elapid snakes. Zool J Linn Soc 125: 239-278 (1999).
29. King AS: Phallus, in King AS, McLelland J (eds): Form and Function in Birds, pp 107-147 (Academic Press, London 1979a).
30. King AS: Cloaca, in King AS, McLelland J (eds): Form and Function in Birds, pp 63-105 (Academic Press, London 1979b).
31. Klaver CJ, Bohme W: Phylogeny and classification of the Chamaelonidae (Sauria) with special reference to hemipenis morphology. Bonn Zool Monogr 22: 1-64 (1986).
32. Kohler J, Hahn M, Kohler G: Divergent evolution of hemipenial morphology in two cryptic species of mainland anoles related to Anolis polylepis . Salamandra 48: 1-11 (2012).
33. Kusumi K, Kulathinal RJ, Abzhanov A, Boissinot S, Crawford NG, et al: Developing a community-based genetic nomenclature for anole lizards. BMC Genomics 12: 554 (2011).
34. 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).
35. Lovern MB, Wade J: Yolk testosterone varies with sex in eggs of the lizard, Anolis carolinensis . J Exp Zool A Comp Exp Biol 295: 206-210 (2003).
36. Lovern MB, Holmes MM, Fuller CO, Wade J: Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles (Anolis carolinensis) . Horm Behav 45: 295-305 (2004).
37. Miyagawa S, Moon A, Haraguchi R, Inoue C, Harada M, et al: Dosage-dependent hedgehog signals integrated with Wnt/-catenin signaling regulate external genitalia formation as an appendicular program. Development 136: 3969-3978 (2009).
38. Mouden EE, Bons J, Pieau C, Renous S, Znari M, Boumezzough A: Table de de veloppement embryonnaire d'un le zard agamide , Agama impalearis Boettger, 1874. Annales des Sciences Naturelles 21: 93-115 (2000).
39. 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).
40. Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, et al: FGF10 acts as a major ligand for Fgf receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277: 643-649 (2000).
41. 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).
42. Petiot A, Perriton CL, Dickson C, Cohn MJ: Development of the mammalian urethra is controlled by Fgfr2-IIIb. Development 132: 2441-2450 (2005).
43. Pispa J, Thesleff I: Mechanisms of ectodermal organogenesis. Dev Biol 262: 195-205 (2003).
44. 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 & Sons, New York 1985).
45. Revest JM, Spencer-Dene B, Kerr K, De Moerlooze L, Rosewell I, Dickson C: Fibroblast growth factor receptor 2-IIIb acts upstream of Shh and Fgf4 and is required for limb bud maintenance but not for the induction of Fgf8 , Fgf10 , Msx1 , or Bmp4 . Dev Biol 231: 47-62 (2001).
46. Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C: Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121: 3163-3174 (1995).
47. Roelink H: Tripartite signaling of pattern: interactions between Hedgehogs, BMPs and Wnts in the control of vertebrate development. Curr Opin Neurobiol 6: 33-40 (1996).
48. Roscito JG, Rodrigues MT: Embryonic development of the fossorial gymnophthalmid lizards Nothobachia ablephara and Calyptommatus sinebrachiatus . Zoology (Jena) 115: 302-318 (2012).
49. Rosenberg HI, Bauer AM, Russell AP: External morphology of the developing hemipenes of the dwarf chameleon, Bradypodion pumilum (Reptilia: Chamaeleonidae). Can J Zool 67: 884-890 (1989).
50. Rosenberg HI, Cavey MJ, Gans C: Morphology of the hemipenes of some Amphisbaenia (Reptilia: Squamata). Can J Zool 69: 359-368 (1991).
51. Ruiz CC, Wade J: Sexual dimorphisms in a copulatory neuromuscular system in the green anole lizard. J Comp Neurol 443: 289-297 (2002).
52. Sala FG, Curtis JL, Veltmaat JM, Del Moral PM, Le LT, et al: Fibroblast growth factor 10 is required for survival and proliferation but not differentiation of intestinal epithelial progenitor cells during murine colon development. Dev Biol 299: 373-385 (2006).
53. Sanger TJ, Losos JB, Gibson-Brown JJ: A developmental staging series for the lizard genus Anolis : a new system for the integration of evolution, development, and ecology. J Morphol 269: 129-137 (2008a).
54. Sanger TJ, Hime PM, Johnson MA, Diani J: Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herpetol Rev 39: 58-63 (2008b).
55. Sanger TJ, Sherratt E, McGlothlin JW, Brodie III ED, Losos JB, Abzhanov A: Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67: 2180-2193 (2013).
56. Sanger TJ, Seav SM, Tokita M, Langerhans RB, Ross LM, et al: The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards. Proc R Soc B 281: 20140329 (2014).
57. Sasaki Y, Iwai N, Tsuda T, Kimura O: Sonic hedgehog and bone morphogenetic protein 4 expressions in the hindgut region of murine embryo with anorectal malformations. J Pediatr Surg 39: 170-173 (2004).
58. 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).
59. 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 (2009).
60. 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).
61. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, et al: Fgf10 is essential for limb and lung formation. Nat Genet 21: 138-141 (1999).
62. Sukegawa A, Narita T, Kameda T, Saitoh K, Nohno T, et al: The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development 127: 1971-1980 (2000).
63. 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).
64. Tokarz RR, Slowinski JB: Alternation of hemipenis use as a behavioral means of increasing sperm transfer in the lizard Anolis sagrei . Anim Behav 40: 374-379 (1990).
65. Wade J: Sculpting reproductive circuits: relationships among hormones, morphology and behavior in anole lizards. Gen Comp Endocrinol 176: 456-460 (2012).
66. Weaver M, Dunn NR, Hogan BL: Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127: 2695 (2000).
67. Winkler SM, Wade J: Aromatase activity and regulation of sexual behaviors in the green anole lizard. Physiol Behav 64: 723-731 (1998).
68. Wu P, Hou L, Plikus M, Hughes M, Scehnet J, et al: Evo-Devo of amniote integuments and appendages. Int J Dev Biol 48: 249-70 (2004).
69. Xu X, Weinstein M, Li C, Naski M, Cohen RI, et al: Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125: 753-765 (1998).