Genetic analysis of an ephemeral intraspecific hybrid zone in the hypervariable tree, Metrosideros polymorpha, on Hawai'i Island

Abstract

Intraspecific hybrid zones involving long-lived woody species are rare and can provide insights into the genetic basis of early-diverging traits in speciation. Within the landscape-dominant Hawaiian tree, Metrosideros polymorpha, are morphologically distinct successional varieties, incana and glaberrima, that dominate new and old lava flows, respectively, below 1200 me on volcanically active Hawai'i Island, with var. glaberrima also extending to higher elevations and bogs. Here, we use morphological measurements on 86 adult trees to document the presence of an incana-glaberrima hybrid zone on the 1855 Mauna Loa lava flow on east Hawai'i Island and parent-offspring analysis of 1311 greenhouse seedlings from 71 crosses involving 72 adults to estimate heritabilities and genetic correlations among vegetative traits. Both the variation in adult leaf pubescence at the site and the consistency between adult and offspring phenotypes suggest the presence of two hybrid classes, F1s and var. incana backcrosses, as would be expected on a relatively young lava flow. Nine nuclear microsatellite loci failed to distinguish parental and hybrid genotypes. All four leaf traits examined showed an additive genetic basis with moderate to strong heritabilities, and genetic correlations were stronger for the more range-restricted var. incana. The differences between varieties in trait values, heritabilities and genetic correlations, coupled with high genetic variation within but low genetic variation between varieties, are consistent with a multi-million-year history of alternating periods of disruptive selection in contrasting environments and admixture in ephemeral hybrid zones. Finally, the contrasting genetic architectures suggest different evolutionary trajectories of leaf traits in these forms.

Figure 1

(top) Map of East Hawai‘i Island showing the study site (oversized hatched circle) and (bottom) the locations of the 86 trees included in the analysis of morphology. Recent lava flows from Mauna Loa are indicated by shading, with the 1855 flow (study site) shown in black. The light gray background indicates lava flows >3000 years old. The map of the study trees is split in two halves, corresponding roughly with mile markers (MM) 11–11.5 and MM 11.5–12 on Saddle Road (dashed line); the tree circled with the dashed line is common to both halves. Adults were designated as var. incana (I), var. glaberrima (G) or an incana–glaberrima hybrid (H) based on leaf pubescence (see text). The underlined symbols indicate trees not included in the hand-crossing study (n=14).

Figure 2

Mean±1 s.e. PC1 and PC2 scores for (a) adults of var. glaberrima (G), var. incana (I) and their hybrids (H) at the study site, and (b) the same with hybrids divided into two classes (H1 and H2). Shared letters indicate no significant difference at α=0.05.

Figure 3

Mean values±1 s.e. of 6 leaf traits of 86 trees in an intraspecific M. polymorpha hybrid zone. Tree types are as in Figure 2. Shared letters indicate no significant difference at α=0.05.

Figure 4

Individual value plots of abaxial (bottom) leaf pubescence of parents and offspring (family-level means) from (a) 20 independent crosses involving pure-variety trees only (shared superscripts indicate no significant difference at α=0.05), and (b) the same from 42 not fully independent crosses involving pure-variety and H1 trees only (for graph only). Tree types are as in Figure 2. Solid bars indicate medians.

Figure 5

Scatter plots of mid-parent (x axis) and mid-offspring (y axis) values for (a) leaf length, (b) leaf width, (c) leaf shape (leaf length/leaf width) and (d) petiole length from 33 independent crosses involving 66 randomly paired adults of all phenotypes at the study site. Weighted linear regressions: leaf length: F_{1, 31}=18.85, P<0.001, R²=35.81; leaf width: F_{1, 31}=5.68, P=0.023, R²=12.76; leaf shape: F_{1, 31}=21.17, P<0.001, R²=38.66; petiole length: F_{1, 31}=17.60, P<0.001, R²=34.15.

Figure 6

Scatter plots of mid-parent (x axis) and mid-offspring (y axis) values for (a) leaf length, (b) leaf width, (c) leaf shape (leaf length/leaf width) and (d) petiole length from 15 independent crosses involving 30 randomly paired adults of var. glaberrima at the study site. Linear regressions: leaf length: F_{1, 13}=5.49, P=0.036, R²=24.26; leaf width: F_{1, 13}=3.27, P=0.094, R²=13.93; leaf shape: F_{1, 13}=18.4, P=0.001, R²=54.47; petiole length: F_{1, 13}=5.16, P=0.041, R²=22.91.