Developmental and Evolutionary Origins of the Amniote Phallus

Abstract

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.

Female Genital Variation Far Exceeds That of Male Genitalia: A Review of Comparative Anatomy of Clitoris and the Female Lower Reproductive Tract in Theria

“…It is present in both sexes, the penis in males and the clitoris in females. Comparative anatomy, physiology, and function of the male phallus are well-studied (e.g., Dixson and Anderson 2001 ; Dixson 2012 ; Gredler et al 2014 ; Gredler 2016 ; Schutz et al 2016 ), whereas similarly detailed descriptions of the clitoris are scarce, in particular when seeking broad comparative accounts. Multiple reasons explain this situation.…”

Histological Investigation of the Nile Crocodile (Crocodylus niloticus) Phallic Glans

“…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.…”

Morphological changes associated with Nile crocodile (Crocodylus niloticus) phallic glans inflation

“…Although amniote phalli share homologous embryonic origins, morphogenetic processes, and molecular genetic mechanisms associated with early development (Brennan, 2016a; Gredler, 2016), their adult morphologies across major amniote lineages are quite diverse (Eberhard, 2010). Three lineages, turtles (Kelly, 2004; McDowell, 1983; Zug, 1966), crocodylians (Johnston et al, 2014; Moore, Spears, Mascari, & Kelly, 2016; Otaño, Imhof, Bolcatto, & Larriera, 2010; Tavalieri et al, 2019; Ziegler & Olbort, 2007), and mammals (Akbari, Babaei, & Goodarzi, 2018; Baskin et al, 2018; Comelis, Bueno, Góes, Taboga, & Morielle‐Versute, 2018; Cunha et al, 2014; Phillips, Wright, Gradie, Johnston, & Pask, 2015), have conspicuous glans structures on the distal phallus.…”