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

Abstract

Coevolution of male and female genitalia in waterfowl has been hypothesized to occur through sexual conflict. This hypothesis raises questions about the functional morphology of the waterfowl penis and the mechanics of copulation in waterfowl, which are poorly understood. We used high-speed video of phallus eversion and histology to describe for the first time the functional morphology of the avian penis. Eversion of the 20 cm muscovy duck penis is explosive, taking an average of 0.36 s, and achieving a maximum velocity of 1.6 m s(-1). The collagen matrix of the penis is very thin and not arranged in an axial-orthogonal array, resulting in a penis that is flexible when erect. To test the hypothesis that female genital novelties make intromission difficult during forced copulations, we investigated penile eversion into glass tubes that presented different mechanical challenges to eversion. Eversion occurred successfully in a straight tube and a counterclockwise spiral tube that matched the chirality of the waterfowl penis, but eversion was significantly less successful into glass tubes with a clockwise spiral or a 135 degrees bend, which mimicked female vaginal geometry. Our results support the hypothesis that duck vaginal complexity functions to exclude the penis during forced copulations, and coevolved with the waterfowl penis via antagonistic sexual conflict.

Figure 1.

Duck genitalia and mechanical barriers. (a) Male and female genitalia in a Pekin duck (Anas sp.). The male phallus (right) spirals in a counterclockwise direction and the female oviduct (left) spirals in a clockwise direction. The female vagina has blind pouches (b.p.) proximal to the cloacal entrance, followed by a series of spirals (sp.). s.s., sulcus spermaticus; a. ph., tip of the penis; cl, cloaca. Scale bar, 2 cm. (b) Diameter glass tubes (10 mm) of different shapes used to test male penis eversion; from left to right, straight, anticlockwise (male-like), clockwise and 135° bend (female-like).

Figure 2.

The explosive eversion of the muscovy duck penis in air. (a) Tracings of the penis at the start of the eversion (prior to the eversion of the basal portion of the penis), midway through the eversion (prior to the eversion of the apical portion of the penis) and at the end of the eversion just before ejaculation. Tracings are from high-speed video. Arrows indicate direction of movement. Scale bar, 5 cm. (b) Average speed of the penis during the basal and apical stages (eversions through the straight tube). Error bars = 95% CI.

Figure 3.

Histological sections of the mallard penis. (a) Cross section of the base of a mallard penis. l.c.ph, lymphatic cavity of the phallus; s.s., sulcus spermaticus; gl.p.ph, glandular part of the phallus; lig.el, elastic ligament. Scale bar, 1 mm. (b) Close view of the wall of the penis at the base (20×). i, inner layer of collagen; o, outer layer of collagen; k, keratinized epithilium. (c) Longitudinal section of the outer layer (o) of the penis at the base (20×) showing collagen fibres not arranged in any particular pattern. Scale bar, (b,c) 100 µm.