Rapid Divergent Evolution of Genitalia

The evolutionary forces responsible for the evolution of animal genitalia have a long history of controversy. Why the special interest in genitalia? In addition to the intrinsic interest of organs that are so intimately related to reproduction and fi tness, it is because of a classic property of genital evolution: the morphological forms of genitalia are often speciesspecifi c, and these forms are often more divergent among closely related species than other traits such as legs, antennae, eyes, etc. In addition, male genitalia often show exuberantly complex forms that seem inexplicable in terms of their sperm transfer function (fi gure 4.1). This trend toward greater diversity in genitalia than in other structures occurs in at least some subgroups of all major taxonomic taxa with internal fertilization (reviewed in Eberhard 1985). This widespread, relatively consistent usefulness of genital morphology in distinguishing species can be translated into a statement about evolutionary processes (unless the data are severely biased—see below): genitalia tend to show an evolutionary pattern of sustained, relatively rapid and divergent morphological change (Eberhard 1985). “Rapid” in this sense is in relative terms, with respect to changes in other traits. Genitalia are often much more elaborate than seems necessary for the simple function of gamete transfer to the female. What could be responsible for such an evolutionary pattern? The objective of this chapter is to review new data and ideas that have appeared since my 1985 book that can help answer this question. As a result of the sustained exploitation by taxonomists of genital morphology to discriminate closely related species, we surely know more about the evolution of species-level divergence in the morphology of genitalia than any other set of structures in the animal kingdom. For more than 100 years this huge mass of data on genitalia accumulated in nearly complete isolation from the study of sexual selection. The isolation was explicit in the original description of sexual selection by Darwin (1871), in which he specifi cally excluded genitalia from his discussion of sexual selection: “There are, however, other sexual differences quite unconnected with the primary reproductive organs, and it is with these that we are especially concerned” (p. 567). It ended abruptly, with Waage’s path breaking paper (1979) demonstrating that male genitalia are used in sperm competition in damselfl ies. During this long period of isolation the study of genitalia was the nearly exclusive province of taxonomists, and was largely descriptive. For their part, students of sexual selection did not even begin to recognize the possibility of post-copulatory competition among males until another crucial paper, that of Parker (1970) on