Drivers of incipient sympatric speciation in a long-lived tree in a riparian zone

This work examines the roles of divergent selection and adaptation to an extreme environment in initiating sympatric speciation between two varieties of the endemic Hawaiian tree Metrosideros polymorpha. In the extremely remote Hawaiian Islands where speciation plays a central role in generating biodiversity, M. polymorpha presents an extraordinary opportunity to investigate how new tree species arise. I focus on a poorly understood riparian ecotype, variety newellii, whose few known populations are found along windward Hamakua Coast rivers on Hawaii Island, sympatric with the closely related wet-forest variety glaberrima. Facing the harsh environmental extremes of its riparian habitats, var. newellii has taken on morphological traits typical of plants in riparian habitats and shows striking neutral genetic differentiation from var. glaberrima despite their sympatry. This work compared the growth and survivorship of seedlings of M. polymorpha vars. newellii and glaberrima grown both in their respective habitats and under experimental environmental conditions to uncover functional differences between varieties which explain their contrasting distributions in nature, while leaf anatomies and morphologies revealed the architectures underlying some of those differences. Light and strong water current were identified as key abiotic pressures leading to differential survivorship between these varieties, with newellii seedling survivorship declining significantly in low light but showing remarkable resistance to the mechanical stress of water currents, retaining significantly more leaves and branches than glaberrima, and surviving significantly better immediately after exposure and for the five weeks following. Field leaf venation, as well as heritable stenophylly and reduced specific leaf area seen in newellii were consistent with the stresses found in its riparian environments. These results suggest that strong abiotic selection at the seedling stage has promoted adaptive genetic divergence between these two varieties, with immigrant inviability and reduced immigrant growth in both habitats inhibiting gene flow and leading to a high level of isolation in var. newellii and neutral genetic divergence between these sympatric varieties. Interestingly, the most genetically isolated population of newellii was also the most ecologically diverged at the seedling stage from glaberrima. These findings support my prediction that strong selection in a marginal habitat is responsible for the emergence of the island-endemic riparian var. newellii on young Hawai'i Island, and indicate that strong selection can drive striking population divergence between trees in sympatry within ∼500,000 years.