Roles of lower-side leaf trichomes in diffusion resistance and gas-exchange characteristics across environmental gradients in Metrosideros polymorpha.

Leaf trichomes on the lower leaf surface are common in many plant species, especially those grown under dry and/or low-temperature conditions; however, their adaptive significance remains unclear. Lower-side leaf trichomes can directly decrease gas fluxes through increased gas-diffusion resistance but can indirectly increase gas fluxes through increased leaf temperature owing to increased heat-diffusion resistance. We examined whether the combined direct and indirect effects of trichome resistance increase photosynthetic rates and water-use efficiency (WUE) using Metrosideros polymorpha Gaud., which varies widely in the masses of lower-side non-glandular leaf trichomes across various environments on the Hawaiian Islands. We employed both field surveys, including ecophysiological measurements at five elevation sites, and simulation analyses to predict the gas-exchange rates of leaves with various trichome-layer thicknesses across a wide range of environmental conditions. Field surveys showed that the trichome-layer thickness was the largest at the coldest and driest site and the thinnest at the wettest site. Field surveys, experimental manipulations and simulation analyses demonstrated that leaf trichomes significantly increased leaf temperature owing to the increased heat resistance. Simulation analyses showed that the effect of leaf trichomes on heat resistance was much larger than that on gas-flux resistance. Leaf trichomes can increase daily photosynthesis only in cold dry areas by increasing the leaf temperature. However, the increased leaf temperature with leaf trichomes resulted in a consistent decrease in the daily WUE at all elevation sites. The magnitudes of trichome effects on gas-exchange rates were associated with the temperature difference across the elevational gradient, the strong light intensity in Hawaii, the leaf-size variation and the conservative stomatal behavior of M. polymorpha as well as the trichome-layer thickness. In summary, the lower-side leaf trichomes in M. polymorpha can be beneficial for carbon assimilation in low-temperature environments but not for water conservation in most environments in terms of diffusion resistance.

Demography and selection analysis of the incipient adaptive radiation of a Hawaiian woody species.

Ecological divergence in a species provides a valuable opportunity to study the early stages of speciation. We focused on Metrosideros polymorpha, a unique example of the incipient radiation of woody species, to examine how an ecological divergence continues in the face of gene flow. We analyzed the whole genomes of 70 plants collected throughout the island of Hawaii, which is the youngest island with the highest altitude in the archipelago and encompasses a wide range of environments. The continuous M. polymorpha forest stands on the island of Hawaii were differentiated into three genetic clusters, each of which grows in a distinctive environment and includes substantial genetic and phenotypic diversity. The three genetic clusters showed signatures of selection in genomic regions encompassing genes relevant to environmental adaptations, including genes associated with light utilization, oxidative stress, and leaf senescence, which are likely associated with the ecological differentiation of the species. Our demographic modeling suggested that the glaberrima cluster in wet environments maintained a relatively large population size and two clusters split: polymorpha in the subalpine zone and incana in dry and hot conditions. This ecological divergence possibly began before the species colonized the island of Hawaii. Interestingly, the three clusters recovered genetic connectivity coincidentally with a recent population bottleneck, in line with the weak reproductive isolation observed in the species. This study highlights that the degree of genetic differentiation between ecologically-diverged populations can vary depending on the strength of natural selection in the very early phases of speciation.

Leaf trichomes in Metrosideros polymorpha can contribute to avoiding extra water stress by impeding gall formation.

BACKGROUND AND AIMS: Plants inhabiting arid environments tend to have leaf trichomes, but their adaptive significance remains unclear. Leaf trichomes are known to play a role in plant defence against herbivores, including gall makers. Because gall formation can increase water loss partly through increased surface area, we tested the novel hypothesis that leaf trichomes could contribute to avoiding extra water stress by impeding gall formation, which would have adaptive advantages in arid environments. METHODS: We focused on Metrosideros polymorpha, an endemic tree species in the Hawaiian Islands, whose leaves often suffer from galls formed by specialist insects, Hawaiian psyllids (Pariaconus spp.). There is large variation in the amount of leaf trichomes (0-40 % of leaf mass) in M. polymorpha. Three gall types are found on the island of Hawaii: the largest is the 'cone' type, followed by 'flat' and 'pit' types. We conducted laboratory experiments to quantify the extent to which gall formation is associated with leaf water relations. We also conducted a field census of 1779 individuals from 48 populations across the entire range of habitats of M. polymorpha on the island of Hawaii to evaluate associations between gall formation (presence and abundance) and the amount of leaf trichomes. KEY RESULTS: Our laboratory experiment showed that leaf minimum conductance was significantly higher in leaves with a greater number of cone- or flat-type galls but not pit-type galls. Our field census suggested that the amount of trichomes was negatively associated with probabilities of the presence of cone- or flat-type galls but not pit-type galls, irrespective of environmental factors. CONCLUSION: Our results suggest that leaf trichomes in M. polymorpha can contribute to the avoidance of extra water stress through interactions with some gall-making species, and potentially increase the fitness of plants under arid conditions.