Male–female conflict and genitalia: failure to confirm predictions in insects and spiders

Abstract

Some recent models suggest a new role for evolutionary arms races between males and females in sexual selection. Female resistance to males is proposed to be driven by the direct advantage to the female of avoiding maleimposed 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 twostep 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.

Evolution of genitalia: theories, evidence, and new directions

“…Female countermeasures could be in her sense organs and nervous system, and thus invisible externally. If such a coevolutionary struggle between males and females did not ''spill over'' into struggles involving physical coercion, it would not be visible in studies of external morphology such as those reviewed in this paper (Eberhard 2004a).…”

“…Almost any part of the male can be modified in this way, from the sucker-like ''bursa'' of male nematodes to the cephalothorax, the chelicerae and anterior legs of spiders, the antennae and telson in crustaceans, and the head, mandibles, antennae, pronotum, cerci, and wings of insects. As pointed out by Robson and Richards (1936), the mechanical function of many (though not all) of these structures is to grasp the female during copulation, the same function that is performed by a large fraction of the male genital structures that are species-specific in form (summaries in Eberhard 1985Eberhard , 2004aScudder 1971). The line between ''true'' genital claspers and non-genital claspers is, in the end, arbitrary (Chapman 1969;Darwin 1871;Eberhard 1985; see also Ghiselin 2009;Leonard and Cordoba-Aguilar 2009).…”

“…The two groups they discussed fit their prediction: male genitalia are often speciesspecific in grasshoppers, but are simple and not divergent in species of Gryllus (Alexander et al 1997). Subsequently this sample was greatly enlarged by using publications on behavioral ecology and taxonomy to discriminate between SAC and CFC (Eberhard 2004a). Discrimination is possible, because CFC predicts that no trend should occur: female use of male genitalia to bias paternity could occur equally well in species with protected or unprotected females (unless unprotected females are more likely to be monandrous due to male manipulations, in which case the prediction is the opposite-there should be greater genital divergence in non-coercive mating systems).…”

Postcopulatory sexual selection: Darwin's omission and its consequences

“…An extensive review of groups of insects and spiders in which SAC should be more or less common nevertheless showed no trend toward lack of rapid divergent genital evolution (to have less distinctive male genitalia) in groups in which male-female conflict over copulation is less likely (42). Several reanalyses of these data, in attempts to mitigate possible biases in the literature, failed to reveal any trend in the predicted direction; in fact, the only significant difference found in the reanalyses was in the opposite direction from that predicted by SAC.…”

Sexual selection and genital evolution

“…Given the widespread occurrence of both these conditions, sexual conflict is rife and can favour traits that increase the fitness of one sex even when it is costly to the other. Hence, elaborate genitals might be the result of an evolutionary arms race between males and females in the struggle for control over reproduction [33], although recent evidence suggests widespread genital divergence is not the result of conflict over mating per se [31]. Sensory exploitation [68], also implicated in genital evolution, could represent the initial evolutionary step in any of the above mechanisms.…”