Natural selection should favor litter sizes that optimize trade-offs between brood-size and offspring viability. Across the primate order, modal litter size is one, suggesting a deep history of selection favoring minimal litters. Humans, however---despite having the longest juvenile period and slowest life-history of all primates---still produce twin-births at appreciable rates, even though such births are costly. This presents an evolutionary puzzle. Why is twinning still expressed in humans despite its cost? More puzzling still, is the discordance between the principal explanations for human twinning and extant empirical data. Such explanations propose that twinning is regulated by phenotypic plasticity in polyovulation, permitting production of larger sib-sets if-and-when resources are abundant. However, comparative data suggest that twinning rates are actually highest in poorer countries and lowest in developed economies. We propose that a historical dynamic of gene-culture coevolution might explain this geographic patterning. Our explanation distinguishes geminophilous and geminophobic cultural contexts, as those celebrating twins (e.g., through material support) and those hostile to twins (e.g., through sanction of twin-infanticide). Geminophilous institutions, in particular, may buffer the fitness cost associated with twinning, potentially reducing selection pressures against polyovulation. We conclude by synthesizing a mathematical and empirical research program that might test our ideas.