Incipient ecological speciation between successional varieties of a dominant tree involves intrinsic postzygotic isolating barriers

Abstract

Whereas disruptive selection imposed by heterogeneous environments can lead to the evolution of extrinsic isolating barriers between diverging populations, the evolution of intrinsic postzygotic barriers through divergent selection is less certain. Long‐lived species such as trees may be especially slow to evolve intrinsic isolating barriers. We examined postpollination reproductive isolating barriers below the species boundary, in an ephemeral hybrid zone between two successional varieties of the landscape‐dominant Hawaiian tree, Metrosideros polymorpha, on volcanically active Hawai'i Island. These archipelago‐wide sympatric varieties show the weakest neutral genetic divergence of any taxon pair on Hawai'i Island but significant morphological and ecological differentiation consistent with adaptation to new and old lava flows. Cross‐fertility between varieties was high and included heterosis of F1 hybrids at the seed germination stage, consistent with a substantial genetic load apparent within varieties through low self‐fertility and a lack of self‐pollen discrimination. However, a partial, but significant, barrier was observed in the form of reduced female and male fertility of hybrids, especially backcross hybrids, consistent with the accumulation of genetic incompatibilities between varieties. These results suggest that partial intrinsic postzygotic barriers can arise through disruptive selection acting on large, hybridizing populations of a long‐lived species.

The role of hybridization during ecological divergence of southwestern white pine (Pinus strobiformis) and limber pine (P. flexilis)

“…Our results are in accordance with studies in other coniferous species demonstrating that speciation is likely initiated through ecological barriers, and several generations of hybridization might occur before the evolution of intrinsic barriers to gene flow (Hamilton et al 2013; Zhou et al 2014; Stacy et al 2017). Integrating the existing genomic dataset with ongoing planting experiments involving climate treatments and measurements of fitness related traits should also help resolve the joint influence of extrinsic and intrinsic isolating mechanisms.…”

“…This is consistent with known patterns of forced crosses for these and other white pine species (Critchfield 1986). The limited evidence of intrinsic incompatibilities noted in our study could be generalized across conifers with similar divergence history, owing to their life history strategies such as long generation time and high dispersal capacity, which will restrict the evolution of post- and pre-zygotic isolating mechanism (Stacy et al 2017). Absence of negative β outliers and of recent hybrids indicates widespread recombination within the hybrid zone and an intermediate stage of divergence between our focal species (Nosil et al 2009).…”

Phylogeography of the highly dispersible landscape‐dominant woody species complex,Metrosideros, in Hawaii

“…These varieties differ further in leaf size and shape, leaf nitrogen content, water retention, cuticle thickness, plant shape and seed germination responses to light and heat (Dawson & Stemmermann, 1990;Drake, 1993;Kitayama et al, 1997;Stacy et al, 2016;Stemmermann, 1983;Vitousek, Turner, & Kitayama, 1995). Differential adaptation on Hawaii Island coincides with partial reproductive isolation between these varieties via genetic incompatibilities that compromise hybrid fertility, especially of backcrosses, in the ephemeral hybrid zones that form on intermediate-aged lava flows (Stacy et al, 2017). Niche divergence between M. polymorpha var.…”

Peer Review #1 of "Tall Pinus luzmariae trees with genes from P. herrerae (v0.2)"

“…Interspecific hybridization is very common in natural stands of the genus Pinus (Critchfield, 1967;Quijada et al, 1997;Conkle & Critchfield, 1988;López Upton et al, 2001;Delgado et al, 2007;Ávila-Flores et al, 2016;Stacy et al, 2017;Vasilyeva & Goroshkevich, 2018;Mo et al, 2019), because of very weak reproductive barriers between pine species (Little & Righter, 1965;Garrett, 1979;Dungey, 2001); this could be generalized across conifers with similar divergence history (Menon et al, 2018). Interspecific F 1 hybrids in this genus are highly viable and fertile (Critchfield 1975), which complicates taxonomic classification (Martínez, 1948;Lanner, 1974).…”