Coevolution of Male and Female Genital Morphology in Waterfowl

Patricia L.R Brennan,Michael D Sorenson,Kevin G Mccracken,Robert E Wilson,Tim R Birkhead,Richard O Prum,Tom Pizzari

doi:10.1371/journal.pone.0000418

Abstract

Most birds have simple genitalia; males lack external genitalia and females have simple vaginas. However, male waterfowl have a phallus whose length (1.5–>40 cm) and morphological elaborations vary among species and are positively correlated with the frequency of forced extra-pair copulations among waterfowl species. Here we report morphological complexity in female genital morphology in waterfowl and describe variation vaginal morphology that is unprecedented in birds. This variation comprises two anatomical novelties: (i) dead end sacs, and (ii) clockwise coils. These vaginal structures appear to function to exclude the intromission of the counter-clockwise spiralling male phallus without female cooperation. A phylogenetically controlled comparative analysis of 16 waterfowl species shows that the degree of vaginal elaboration is positively correlated with phallus length, demonstrating that female morphological complexity has co-evolved with male phallus length. Intersexual selection is most likely responsible for the observed coevolution, although identifying the specific mechanism is difficult. Our results suggest that females have evolved a cryptic anatomical mechanism of choice in response to forced extra-pair copulations.

Highlights

Complex genitalia can result from different evolutionary mechanisms [reviewed in 1,2], in recent years sexual selection is increasingly regarded as the primary force behind the evolution of genital diversity [1,2,3,4]
Elaborate vaginal morphology appears to have coevolved with male phallus length, which in turn covaries with levels of forced extra-pair copulation [16]
Phallus length is positively correlated with both vagina length and the number of vaginal elaborations

Summary

Introduction

Complex genitalia can result from different evolutionary mechanisms [reviewed in 1,2], in recent years sexual selection is increasingly regarded as the primary force behind the evolution of genital diversity [1,2,3,4]. If males have genital traits that allow them to manipulate females and bias paternity, coevolved modifications in female genital anatomy would allow females to regain some control over copulation and/or fertilization success [12]. These female morphological adaptations would select for additional adaptations in the male anatomy, resulting in coevolution of male and female structures [6,13]. The avian phallus may allow males to achieve intromission without female cooperation [14,18], and to deposit semen closer to the site of sperm storage and/or fertilization to increase their likelihood of fertilization [14], thereby providing males with a copulatory advantage over females

Methods

Results

Conclusion