Maternal risk-management elucidates the evolution of reproductive adaptations in sharks by means of natural selection

Abstract

Maternal investment theory is the study of how breeding females allocate resources between offspring size and brood size to achieve reproductive success. In classical trade-off models, r/K-selection and bet-hedging selection, the primary predictors of maternal investments in offspring are population density and resource stability. In crowded, stable environments, K-selected females invest in large offspring at an equivalent cost in brood size. In uncrowded, unstable environments, r-selected females invest in large broods at an equivalent cost in offspring size. In unpredictable resource environments, bet-hedging females invest moderately in brood size and offspring size. The maternal risk-management model represents a profound departure from classical trade-off models. Maternal investments in offspring size, brood size, and brood number are shaped independently by autonomous risk factors: the duration of gaps in resources during seasonal cycles, rates of predation, and unpredictable catastrophic events. To date, no single model has risen to a position of preeminence. Here in sharks, we show that maternal investments within and across species do not agree with the predictions of trade-off models and instead agree with the predictions of the maternal risk-management model. Within and across shark species, offspring size and brood size were independent maternal investment strategies. The risk of starvation favored investments in larger offspring. The risk of predation favored investments in larger broods. If empirical studies continue to confirm its predictions, maternal-risk management may yet emerge as a unifying model of diverse reproductive adaptations by means of natural selection.