Drastic shift in flowering phenology of F₁ hybrids causing rapid reproductive isolation in Imperata cylindrica in Japan

Hybridization is a major source of phenotypic variation and a driving force for evolution. Although novel hybrid traits can often disrupt adaptive relationships between the parental phenotypes and their environments, how new hybrid traits disrupt local adaptation remains unclear. Here, we report how a new phenotype of hybrids between two Imperata cylindrica ecotypes contributes to rapid reproductive isolation from their parents and affects hybrid fitness. We analysed 350 accessions of I. cylindrica collected from the 1980s to the 2010s throughout Japan to explore the genetic population structure of the hybrids. We surveyed the flowering periods, seed set, and germination of two ecotypes and their hybrids in both natural habitats and common gardens. Genetic analyses of population structure revealed that the hybrid populations consisted of only F₁ individuals, without advanced generation hybrids. The flowering phenology of the F₁ plants was delayed until autumn, 5–6 months later than the parental ecotypes. The drastic shift in flowering phenology prevents F₁s from backcrossing. In addition, it changes their seed dispersal time to winter. Germination is inhibited by low temperatures, and the seeds likely decay before the next spring, resulting in the absence of an F₂ generation. We identified the environmental mismatch of the F₁ population as a specific mechanism for the maintenance of an only F₁ population. Synthesis. We have demonstrated that this flowering phenology mismatch promotes reproductive isolation between the parents and F₁s and affects various temporal components of the hybrids, resulting in a unique hybrid population consisting only of F₁s. This system sheds light on the importance of hybrid traits in driving rapid reproductive isolation.