Does retained-seed priming drive the evolution of serotiny in drylands? An assessment using the cactus Mammillaria hernandezii

Abstract

Premise of the study: Serotinous plants retain their seeds for a long time. In deserts, retained seeds undergo hydration-dehydration cycles and thus may become primed. Priming enhances germination and seedling vigor. We test the hypothesis that serotiny evolves because it provides a site protected from predators in which seeds can become primed. Rainfall-cued dispersal of primed seeds may enhance this effect. Methods: We tested this hypothesis with Mammillaria hernandezii through protein-content analyses; field and laboratory germination experiments with primed, unprimed, and retained seeds; and fitness estimations from demographic models. Key results: Hydration-dehydration cycles induced priming, enhancing germination. Artificial priming and retention in the parent plant for 1 yr induced similar changes in seed protein patterns, suggesting that priming occurs naturally while seeds are retained. Under field conditions, germination of seeds retained for 1 yr more than doubled that of seeds of the same cohort that were not primed or that remained buried for 1 yr. The first seeds to germinate died rapidly. Serotinous plants whose seeds underwent priming had higher fitness than those whose seeds were in the soil seed bank or that did not experience priming. Conclusions: Priming in soil seed banks may be costly because of high predation, so seed protection during priming is sufficient to promote the evolution of serotiny. Bet hedging contributes to this process. Rapid germination of primed seeds that respond to brief rainfall events is disadvantageous because such rainfall is insufficient for seedling survival. Serotinous species counteract this cost by cueing dispersal with heavy precipitation.