Pollen competition in hybridizing Cakile species: How does a latecomer win the race?

Abstract

Premise: Hybridization between cross-compatible species depends on the extent of competition between alternative mates. Even if stigmatic compatibility allows for hybridization, hybridization requires the heterospecific pollen to be competitive. Here, we determined whether conspecific pollen has an advantage in the race to fertilize ovules and the potential handicap to be overcome by heterospecific pollen in invasive Cakile species.

Methods: We used fluorescence microscopy to measure pollen tube growth after conspecific and heterospecific hand-pollination treatments. We then determined siring success in the progeny relative to the timing of heterospecific pollen arrival on the stigma using CAPS markers.

Results: In the absence of pollen competition, pollination time and pollen recipient species had a significant effect on the ratio of pollen tube growth. In long-styled C. maritima (outcrosser), pollen tubes grew similarly in both directions. In short-styled C. edentula (selfer), conspecific and heterospecific pollen tubes grew differently. Cakile edentula pollen produced more pollen tubes, revealing the potential for a mating asymmetry whereby C. edentula pollen had an advantage relative to C. maritima. In the presence of pollen competition, siring success was equivalent when pollen deposition was synchronous. However, a moderate 1-h advantage in the timing of conspecific pollination resulted in almost complete assortative mating, while an equivalent delay in conspecific pollination resulted in substantial hybrid formation.

Conclusions: Hybridization can aid the establishment of invasive species through the transfer of adaptive alleles from cross-compatible species, but also lead to extinction through demographic or genetic swamping. Time of pollen arrival on the stigma substantially affected hybridization rate, pointing to the importance of pollination timing in driving introgression and genetic swamping.

Keywords: Brassicaceae; Cakile edentula; Cakile maritima; hybridization; invasion; pollination timing; post-pollination; reproductive barrier; species-specific markers.