Evolution of External Genitalia: Insights from Reptilian Development

Abstract

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.

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

“…To better understand the positional relationship of the genital swellings to the cloaca and hindlimb, we prepared a second reconstruction that focused on the cloacal region ( figure 1d ). In this model, one genital swelling is visible immediately lateral to the cloacal urodeum, at the same position where one finds the right genital swelling in other amniotes [10,19]. A second swelling is observed anterior to the cloaca, in the position appropriate for the anterior cloacal swelling of squamates (figure 1e; electronic supplementary material, S2.5, [9,16,17]).…”

Morfologia de órgãos genitais femininos de quelônio semi-aquático Mesoclemmys vanderhaegei

“…A cloaca de M. vanderhaegei apresenta os compartimentos coprodeum, urodeum e proctodeum, sendo esse arranjo um consenso na literatura em répteis (Sánchez-Martínez et al 2007, Rosa et al 2011, Gredler et al 2014) e aves (King 1993b). Apesar de estudos anteriores definirem a cloaca como um compartimento comum aos sistemas digestório e urogenital (Machado Júnior et al 2006, Pinheiro et al 2010, pouca atenção foi dada ao urodeum, em cujo assoalho repousa o clitóris, não mencionado em K. scorpioides (Machado Júnior et al 2006) e tampouco em P. expansa, P. unifilis, Chelus fimbriatus e Phrynops geoffroanus (Rosa et al 2011).…”

Shared Enhancer Activity in the Limbs and Phallus and Functional Divergence of a Limb-Genital cis-Regulatory Element in Snakes

“…Furthermore, we find that of the mouse limb-GT enhancers with orthologs in Anolis , a relatively small proportion exhibit conserved enhancer activity in the hemiphallus as compared to the limbs of Anolis embryos (16.8% in the hemiphallus vs. 40.2% in the forelimb and 46.7% in the hindlimb; Figure 4). The modest number of limb-GT enhancers with conserved genital activity might reflect the striking anatomical differences between the genitalia of these species (Gredler et al, 2014). In most amniotes, including mammals, the external genitalia form as paired swellings, which then merge to form a single phallus.…”

“…The phallus is a feature present in many amniotes and likely evolved in a common ancestor more than 310 million years ago (Gredler et al, 2014; Hedges et al, 2004). Although the phallus differs from limbs in both form and function, the development of the phallus and limbs share certain features.…”