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 21. 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 1358 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.

PHYSIOLOGY AND ENDOCRINOLOGY SYMPOSIUM: Role of the oviduct in maintaining sustained fertility in hens1

“…In describing the duck vagina, Brennan et al (2007) observed a spiral-shaped tube that was further characterized by blind pouches stemming from its distal half. When considering the waterfowl penis is corkscrewed with an opposite orientation to the spirals in the vagina (Brennan et al, 2010), the authors concluded that the anatomical incongruity between the phallus and vagina would be used by the female to impede the penetration of the penis during attempts at forced copulation.…”

The limits of sexual conflict in the narrow sense: new insights from waterfowl biology

“…In waterfowl species that have evolved more elaborate phalluses, females have coevolved complex oviducts-i.e. blind pouches, and counter-sense spirals-that appear to function to selectively exclude the phallus [27]. Coevolutionary elaboration is positively associated with rate of forced extra-pair copulations (FEPCs) [26].…”

“…Coevolutionary elaboration is positively associated with rate of forced extra-pair copulations (FEPCs) [26]. Because female genital adaptations in waterfowl do not decrease the direct costs of male sexual coercion but appear to function solely in manipulating fertilization success ( [27], and discussion in §4), these structures could not have evolved by a narrow sense sexual conflict mechanism that excludes indirect effects. In addition, in waterfowl, females choose a mate and form a pair bond over a period of weeks prior to the breeding season when sexual coercion is non-existent [28].…”

Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia

“…Male genital morphology has been shown to be associated with sexual conflict during copulation in many taxa [14][15][16][17][18]. In North American natricine snakes, taxa with bilobed hemipenes have longer copulation durations than those with cylindrical hemipenes [34].…”

“…When males transfer other substances during copulation, for example a copulatory plug, conflict is likely to be more intense if these secretions negatively affect female fitness but positively affect male fitness [5,12,13]. Male genital morphology has been shown to be associated with sexual conflict during copulation in many taxa [14][15][16][17][18][19][20].…”