The Functional Morphology of Penile Erection: Tissue Designs for Increasing and Maintaining Stiffness

Abstract

Inflatable penises have evolved independently at least four times in amniotes, specifically in mammals, turtles, squamates, and the archosaurs. Males in these lineages therefore share the functional problem of building a penis out of soft and flexible tissues that can increase its flexural stiffness and resist bending during copulation. Research on penile erectile tissues in mammals and turtles shows that these two taxa have convergently evolved an axial orthogonal array of collagen fibers to reinforce the penis during erection and copulation; in both lineages, the collagen fibers in the array are crimped and folded in the flaccid penis. Collagen fiber straightening during erection increases the stiffness of the tissue and allows changes in penile radius that increase its second moment of area: both of these changes increase the flexural stiffness of the penis as a whole. And once erect, axial orthogonal arrays have the highest flexural stiffness of any fiber arrangement. The high degree of anatomical convergence (to the level of microanatomical features) within mammals and turtles suggests that the stiffness requirements for copulation produce an extremely restrictive selective regime in organisms that evolve inflatable penises.

The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour

“…The phylogenetic distribution of intromittent organs in the amniotes would strongly indicate that a penis-like structure is a synapomorphy for amniotes with independent losses in both the Sphenodontidae and Neognathae, although it is alternatively possible that intromittent organs were a convergent trait (cladogram inspired by Kelly 2002Kelly , 2004. This study would strongly indicate that a phallus is ancestral to the Archosauria to be lost in the Neognathae.…”

“…Both types of phallus employ a blood vascular mode of erection, are composed of two joined fibrous bodies and use a seminal groove to transport semen (King 1981a). The chelonian phallus furthermore demonstrates a remarkable convergence with the true penis of mammals in that both are reinforced by an axial orthogonal array of collagen fibres, a layout believed to maximally increase the flexural stiffness of the intromittent organ while resisting bending forces during coitus (Kelly 2002(Kelly , 2004). …”

The diversity of hydrostatic skeletons

“…The primary erectile tissue of the penis is the corpus cavernosum, which is wrapped with a tough layer, the tunica albuginea, containing robust collagen fibers that do not follow helical paths around the penis, but instead are aligned both parallel and perpendicular to the longitudinal axis, i.e. fiber angles of 0 and 90deg (Kelly, 1997;Kelly, 2002;Kelly, 2007). In the flaccid state, the tunica albuginea is highly folded.…”

Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia

“…The erect penises of mammals and turtles are stiff hydrostats supported by axial-orthogonal layers of inextensible collagen fibres (Kelly 2002(Kelly , 2004Babinski et al 2005). Unlike mammals and turtles, the waterfowl penis is flexible when erect, suggesting that the collagen fibres are not arranged in axial-orthogonal arrays.…”