The amount of trichomes on the leaves of Metrosideros polymorpha varies enormously, ranging from 0 to ca 150 g/m2 across environmental gradients on the island of Hawaii. Pubescent individuals are abundant in dry areas or on young lava flows, whereas glabrous individuals are abundant in wet areas or on developed soils. To understand the adaptive advantages of pubescent individuals in arid environments, we addressed the following questions: (1) whether leaf trichomes increase the boundary layer resistance to gas diffusion, which in turn reduces the transpiration rate and increases water‐use efficiency (WUE); and (2) whether pubescent individuals have other associated leaf and shoot traits that have adaptive significance in arid environments. We made detailed ecophysiological measurements on M. polymorpha in three populations in habitats that varied in aridity. We found a large allocation of leaf mass to trichomes, up to 33 percent at the arid site, but our analyses showed that trichomes had small effects (1–9%) on gas exchange and negligible effects on WUE, suggesting the trichomes may have roles beyond increasing WUE. However, pubescent individuals did have higher Rubisco amount and a lower leaf‐to‐ sapwood area ratio, which are considered adaptive in arid environments. These results suggest that pubescent individuals of M. polymorpha are indeed adapted to arid environments with changes in a suite of traits. The adaptive significance of the enormous variation in amounts of trichomes remains unclear and may be related to functions other than increasing boundary layer resistance.

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.

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.

Dense leaf trichomes can directly decrease gas fluxes through increased gas diffusion resistance and indirectly increase gas fluxes through increased leaf temperature due to increased heat diffusion resistance, which may contribute to adaptation to dry and/or low‐temperature conditions. However, it remains unclear whether the leaf‐trichome resistance increases or decreases the gas‐exchange rates through combined direct and indirect effects. We focused on Metrosideros polymorpha, a dominant tree species inhabiting a large range of environmental gradients in the Hawaiian Islands, whose leaves have an enormous variation in trichome thickness on the lower surface. In five elevational sites, we measured leaf morphological and physiological traits including trichome thickness, gas‐exchange characteristics, and leaf temperature. The trichome thickness was largest in the coldest and driest site and thinnest at the wettest site. Leaf temperature was significantly increased with trichome thickness. With biophysical and physiological models, we show that leaf trichomes can increase the daily photosynthesis through increasing leaf temperature only in the cold alpine area. The daily water‐use efficiency can be lower with increasing leaf trichomes at any elevational sites. Therefore, in terms of diffusion resistance, the leaf trichomes of M. polymorpha can contribute to the adaptation to low‐temperature environments but not to dry environments.

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