Incipient radiation within the dominant Hawaiian tree Metrosideros polymorpha

Abstract

Although trees comprise a primary component of terrestrial species richness, the drivers and temporal scale of divergence in trees remain poorly understood. We examined the landscape-dominant tree, Metrosideros polymorpha, for variation at nine microsatellite loci across 23 populations on young Hawai'i Island, sampling each of the island's five varieties throughout its full geographic range. For four varieties, principal coordinate analysis revealed strong clustering of populations by variety across the 10 430 km(2) island, indicating partitioning of the species into multiple evolutionarily significant units. The single island-endemic form, riparian var. newellii, showed especially strong differentiation from other varieties despite occurring in sympatry with other varieties and likely evolved from a bog form on the oldest volcano, Kohala, within the past 500 000 years. Along with comparable riparian forms on other Pacific Islands, var. newellii appears to represent parallel incipient ecological speciation within Metrosideros. Greater genetic distance among the more common varieties on the oldest volcano and an inverse relationship between allelic diversity and substrate age appear consistent with colonization of Hawai'i Island by older, partially diverged varieties followed by increased hybridization among varieties on younger volcanoes. This study demonstrates that broad population-level sampling is required to uncover patterns of diversification within a ubiquitous and long-lived tree species. Hawaiian Metrosideros appears to be a case of incipient radiation in trees and thus should be useful for studies of divergence and the evolution of reproductive isolating barriers at the early stages of speciation.

Figure 1

Locations of 23 populations of M. polymorpha sampled from four volcanoes: Kohala, Mauna Kea, Mauna Loa and Kilauea on Hawai'i Island. Dotted lines depict the approximate boundaries between surface flows from adjacent volcanoes. No sampling was done from Hualalai.

Figure 2

Relationship between geographic distance and pairwise F_ST for 23 populations of M. polymorpha on Hawai'i Island. F_ST values for same variety population pairs (closed circles) are typically lower than those for different variety population pairs (open circles) regardless of the geographic distance between populations. Exceptions include unusually high F_ST values¹ among the three small populations of the riparian endemic var. newellii likely due to genetic drift, and a high F_ST value² between var. glaberrima-Alakahi in Kohala and the var. macrophylla (glaberrima, see text)-Halepua'a on the southwest side of the island.

Figure 3

Principal coordinate analysis of pairwise F_ST values of 23 populations of five varieties of M. polymorpha on Hawai'i Island, using PAST software. Variety codes: G=var. glaberrima, I=var. incana, M=var. macrophylla, N=var. newellii, P=var. polymorpha. All populations, except those of M, cluster by variety. With one exception (M), the dashed curve separates pubescent populations from glabrous populations.

Figure 4

Splitstree network of 23 populations of five varieties of M. polymorpha from across Hawai'i Island. The positions of populations from the four supported varieties are indicated by curved lines and labels. The four populations from Kohala are underlined.

Figure 5

Relationship between log substrate age and population-level allelic richness for the three varieties that occur across a broad range of substrate ages: var. incana (squares and dashed line), var. glaberrima (including var. macrophylla; circles and solid line) and var. polymorpha (diamonds and dotted line). ANCOVA: variety: F=13.82, df=2, P=0.001; log minimum substrate age (covariate): F=10.02, df=1, P=0.007; R²=61.5%.