Biol. Rev. (2004), 79, pp. 121–186. f Cambridge Philosophical Society 121 DOI: 10.1017/S1464793103006237 Printed in the United Kingdom Male–female conflict and genitalia: failure to confirm predictions in insects and spiders William G. Eberhard Smithsonian Tropical Research Institute, and Escuela de Biologı´a, Universidad de Costa Rica Ciudad Universitaria, Costa Rica (E-mail: [email protected]) (Received 9 May 2002; revised 4 March 2003; accepted 7 March 2003) ABSTRACT Some recent models suggest a new role for evolutionary arms races between males and females in sexual selec- tion. Female resistance to males is proposed to be driven by the direct advantage to the female of avoiding male- imposed reductions in the number of offspring she can produce, rather than by the indirect advantage of selecting among possible sires for her offspring, as in some traditional models of sexual selection by female choice. This article uses the massive but hitherto under-utilized taxonomic literature on genitalic evolution to test, in a two- step process, whether such new models of arms races between males and females have been responsible for rapid divergent evolution of male genitalia. The test revolves around the prediction that ‘new arms races’ are less likely to occur in species in which females are largely or completely protected from unwanted sexual attentions from males (e.g. species which mate in leks or in male swarms, in which males attract females from a distance, or in which females initiate contact by attracting males from a distance). The multiple possible mechanical functions of male genitalia are summarized, and functions of male genitalic structures in 43 species in 21 families of Diptera are compiled. Functions associated with intromission and insemination (e.g. seizing and positioning the female appropriately, pushing past possible barriers within the female, orienting within the female to achieve sperm transfer), which are unlikely to be involved in new arms races when females are protected, are shown to be common (>50% of documented cases). This information is then used to generate the new arms race prediction: differences in genitalic form among congeneric species in which females are protected should be less common than differences among congeneric species in which females are vulnerable to harassment by males. This prediction was tested using a sample of 361 genera of insects and spiders. The prediction clearly failed, even when the data were adjusted to take into account several possible biases. Comparative analyses within particular taxonomic groups also failed to show the predicted trends, as did less extensive data on other non-genitalic male display traits. Arms races, as defined in some recent models, seem to have been less important in male–female coevolution of genitalic structures than has been suggested. By elimination, alternative interpretations, such as traditional female choice, which do not predict associations between female protection from harassment and rapid divergent evolution, are strengthened. Key words: genitalic evolution, sexual selection, cryptic female choice, male–female conflict. CONTENTS I. Introduction ................................................................................................................................................. 122 II. Methods ........................................................................................................................................................ 128 III. Results ........................................................................................................................................................... 143 (1) Functions of male genitalic structures in Diptera ............................................................................. 143 (2) Comparisons of groups with protected and unprotected females .................................................. 157 (a) Totals of genus-by-genus counts ................................................................................................... 157 (b) Analyses at higher taxonomic levels ............................................................................................. 161 IV. Discussion ..................................................................................................................................................... 162 (1) Genitalic functions in Diptera ............................................................................................................. 162 122 William G. Eberhard (2) Comparisons of groups with protected and unprotected females .................................................. 163 (a) Genus-by-genus comparisons ........................................................................................................ 163 (i) Totals ......................................................................................................................................... 163 (ii) Possible limitations of the analyses ......................................................................................... 163 (A) Data on genitalia ............................................................................................................... 163 (B) Data on mating behaviour ............................................................................................... 164 (C) The analyses ....................................................................................................................... 166 (D) Summary of limitations .................................................................................................... 166 (b) Large taxa with uniformly protected females ............................................................................. 166 (c) Other hypotheses and data ............................................................................................................ 167 (3) Non-genitalic traits ................................................................................................................................ 167 (4) Can one generalize from genitalia? .................................................................................................. 168 V. Conclusions .................................................................................................................................................. 169 VI. Acknowledgements ...................................................................................................................................... 169 VII. References .................................................................................................................................................... 169 I. INTRODUCTION activities such as feeding, sheltering, or resting. Costs could also be imposed on females after copulation ends, as a result Recent empirical and theoretical developments have of male effects on her reproductive physiology, such as suggested new interpretations of sexual selection. Some causing her to make disadvantageously large or premature evolutionary phenomena that were previously explained by investments in oviposition due to male induction of egg mate choice may be better explained by coevolution of males maturation or oviposition, or to lose the benefits (direct or and females resulting from conflicts of interest between the indirect) that she might obtain from other males due to sexes over control of copulation and fertilization (Parker, male-imposed suppression of her receptivity (Chen, 1984). 1979; Chapman et al., 1995, 2003; Rice, 1996; Alexander, Males and females are envisioned as being engaged in co- Marshall & Cooley, 1997; Holland & Rice, 1998, 1999; evolutionary arms races for control of the events that are Rice & Holland, 1999; Johnstone & Keller, 2000; Michiels, associated with copulation, insemination, and ultimately 1998; Gavrilets, Arnqvist & Friberg, 2001; Pitnick, Brown fertilization of the female’s eggs. Explicit models of this sort & Miller, 2001a; Pitnick, Reagan & Holland, 2001b; Stutt have been proposed for both classic, pre-copulatory female & Siva-Jothy, 2001; Moore et al., 2001). These recent dis- rejections (the ‘chase-away’ model of Holland & Rice, cussions emphasize one particular class of direct benefits 1998; Gavrilets et al., 2001), and female rejection during or that a female could derive from resisting male sexual following coupling (the male–female conflict model of behaviour: avoidance of male-inflicted reductions in her Alexander et al., 1997). These ideas will be referred to here ability to produce offspring. Evolutionary interactions as ‘new arms race’ models. As noted by Gavrilets et al. between males and females are thought to be driven by (2001) they contrast with ‘traditional’ ideas that emphasize selection on females to avoid these costs that are imposed other possible types of benefits that a female could derive by the male, resulting in subsequent male countermeasures. from rejecting some types of conspecific males (reviewed by For instance, in their ‘chase away’ model, Holland and Andersson, 1994). Setting aside the probably small subset Rice (1998) listed the possible costs of mating for females of species in which females gain direct benefits (Andersson, as mating ‘too often, [or at a] less-than-ideal time or place’. 1994), the distinction between the new arms race models Gavrilets et al. (2001) contrasted the proposed benefits to and the traditional female choice models involves selection females from rejecting males under their sexual conflict on the female that