An alternative to classic sexual selection hypotheses for sex differentiated pre-mating behavior is that time available for mating—as individuals experience it—along with fitness differences among alternative potential mates, induces choosy versus indiscriminate mating behavior. This alternative hypothesis says that selection has acted so that all individuals flexibly express fitness-enhancing choosy, indiscriminate, and competitive mating behavior, induced by time-varying life histories, environmental and social cues. Key predictions of DYNAMATE, the formal model of adaptively flexible sex role behavior of individuals of both sexes within dynamically changing populations, include: (1) All individuals regardless of sex assess likely fitness outcomes from mating with alternative potential mates before expressing choosy or indiscriminate behavior. (2) Males and females express adaptively flexible, choosy and indiscriminate behavior so that individuals may change their behavior—from moment to moment—to fit dynamically changing circumstances. (3) Indiscriminate behavior of males and (4) choosy behavior of females would often be maladaptive even in species with greater female than male parental investment, when females have longer latencies to receptivity to re-mating than males, and when the relative reproductive rate of males is greater than in females. (5) Whether or not females show choosy behavior will not affect whether or not males exhibit choosy or indiscriminate behavior, and vice versa. (6) When other model parameters are equal, the proportion of individuals of a given sex expressing choosy or indiscriminate mating behavior is a function of the distribution of fitness ratios (a distribution of all fitness differences that would be conferred on an individual by mating with any two sequentially or simultaneously encountered alternative potential mates). (7) Whether same-sex individuals behaviorally compete is a function of the fitness that would be conferred if the strategist won access to a potential mate, but not a function of relative reproductive rate or its proxy, the operational sex ratio. We call for re-evaluation of sex differences in choosy, indiscriminate, and competitive behavior under strong experimental controls that level the ecological playing fields of males and females, i.e., under experimental conditions informing the mechanisms of phenotypic expression. We end with comments on the classic question of questions: why are the sexes as they are?