Rapid Displacement of a Monoecious Plant Lineage Is Due to Pollen Swamping by a Dioecious Relative

Interspecific hybridization is recognized as a potentially destructive process that represents a major threat to biodiversity. The rate of population displacement by hybridization can be rapid, but underlying mechanisms are often obscure. One hypothesis is that a species may be driven to extinction by interspecific gene flow, or pollen swamping, when hybrids are inviable or sterile. Here, we document the rapid movement of two zones of contact between monoecious hexaploid and dioecious diploid populations of the wind-pollinated plant Mercurialis annua (Euphorbiaceae) in northeastern and northwestern Spain, where diploids have displaced hexaploids by about 80 and 200 km, respectively, over a period of four decades. By using experimental mating arrays, we show that hybridization is highly asymmetrical in favor of the diploids, mainly because they disperse substantially more pollen, as expected in a comparison between an obligate outcrosser and a facultative selfer. Self-fertilization, which is expected to reduce the proportion of sterile hybrids produced in mixed ploidy populations, allowed the hexaploids to avoid the effects of pollen swamping only slightly, and in a density-dependent manner. Our results thus provide a mechanistic explanation for the rapid movement of both contact zones of M. annua in Spain.