The importance of postzygotic barriers at the early stages of speciation in trees

Abstract Recent reviews of isolating barriers in plants conclude that prezygotic barriers play an outsized role in plant speciation; yet these conclusions derive overwhelmingly from studies of sympatric, perennial herbs in temperate zones, and at later stages of speciation. Trees possess several traits that are expected to influence barrier evolution, including prolonged generation times and reproduction, predominant outcrossing, and long-distance gene flow. We examined early-evolving post-pollination barriers between ecologically diverged, vegetatively distinct varieties of the tree species, Metrosideros polymorpha , that have a common floral morphology and highly overlapping flowering times. We performed controlled crosses between each of Hawaii Island’s four varieties and maternal trees of the high-elevation variety and examined pollen-tube growth, fruit set, seed germination, and seedling phenotype. We then monitored survivorship, maturation rate, and fertility of F 1 hybrids over ≥8 years alongside parental controls and a fourth F 1 genotype derived from companion studies. The four F 1 crosses showed four contrasting patterns and strengths of predominantly postzygotic isolation, including high F 1 mortality that manifested over several years. Results from this and other tree studies suggest that ecological speciation in trees follows the classical speciation model of early postzygotic barrier formation followed by reinforcement, whenever stable environments promote recurring hybridization.