The breeding system of an animal population is thought to depend on the ability of one sex (usually the male) to acquire mates, either directly through association with females or indirectly through defense of the resources desired by females. The sex that contributes most to infant care (usually the female) is constrained by parental involvement and thereby limits reproduction of the opposite sex. Accordingly, males, but not females, enhance their reproductive success by acquiring additional mates. This classical view has emphasized the role of male–male competition in sexual selection, at the expense of fully exploring the potential for female choice. A more recent shift in focus has revealed substantial variation in female reproductive success and increasingly accentuates the importance of female intrasexual competition and male mate choice. A comparative review of primate reproduction, therefore, challenges expectations of male control and female compliance, and calls for a comprehensive treatment of costs and benefits that extends beyond conventional mention of heavy female investment versus male negligence or absenteeism. For individuals that manipulate their social environment or reproductive output, consideration of more subtle, even cryptic, aspects of female behavior and physiology (e.g., social strategizing, sexual solicitation or rejection, sexual advertisement or concealed ovulation, multiple mating, and reproductive failure) raises the question of whether females can be effectively ‘monopolized.’ Widespread patterns that counter Bateman's paradigm call for a reexamination of the predictions generated by dichotomizing gametes into ‘expensive eggs’ and ‘cheap sperm,’ and encourage continued mechanistic research focused on conception quality rather than quantity.