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M. p. var. glaberrima near HAVO

Metrosideros polymorpha var. glaberrima near Hawaii’s Volcanoes National Park, Hawai’i Island.

Research in my lab centers on how tree species form and how they respond to environmental change.  We examine how differential adaptation of woody species across heterogeneous environments leads to phenotypic divergence and the accumulation of reproductive isolating barriers (i.e., speciation).  We also study short-term responses of trees to environmental change involving largely developmental and physiological plasticity, as these shed light on a population’s capacity to tolerate novel conditions.  This multi-disciplinary program involves studies in the field, greenhouse, environmental chamber, and microscopy and molecular labs as well as a broad range of modern analytical approaches.  Our work is increasingly focused on the integration of genomic analyses with the growing data set on phenotypes, ecology, and reproductive isolating barriers in our primary study system, Hawaiian Metrosideros.

Hawaiian Metrosideros (Myrtaceae) is a hyper-variable woody species complex that dominates the islands’ native forests, occurs in massive, continuous populations that span a broad range of climates, and appears to capture multiple stages of speciation.  The group comprises numerous mostly conspecific, vegetatively distinct forms that are non-randomly distributed across Hawaii’s famously heterogeneous landscape.  Metrosideros possesses several characteristics that make it unusually amenable to experimental studies: a) adult trees are short in many areas where conditions are limiting, allowing access to the canopy for hand-pollinations; b) in a greenhouse, individuals of most taxa can begin annual flowering at 3-6 years of age; c) air-layering of branches permits the collection of large numbers of independent flowering “trees” in a greenhouse for controlled crossing studies; and d) seeds can be dried for long-term storage, allowing the staggering of experiments with seeds and seedlings.  Baseline studies in my lab have identified >20 predominantly single-island-endemic taxa of Metrosideros across the island chain, demonstrated heritability of taxon-diagnostic phenotypes, and provisionally named six new taxa (in collaboration with Neil Snow at Pittsburgh State University).

Half-open inflorescence of M. polymorpha.

Development of Hawaiian Metrosideros as a model for resilience and speciation in trees has led to the generation of: four high-quality chromosome-level reference genomes (from Nanopore and PacBio sequencing; in collaboration with Michael Purugganan at New York University and Jae Young Choi at the University of Kansas); Illumina resequencing data for 131 adults from 11 taxa; DNA samples from > 1,400 adults from across the Hawaiian Islands and greater Pacific; current greenhouse and common-garden populations of nine taxa, select F1 and backcross hybrids; and stored seeds of ‘pure-taxon,’ F1, F2, and backcross genotypes from > 2,300 controlled, greenhouse-based crosses within and among 10 taxa.

Divergence and Speciation in Trees – There are an estimated 100,000 species of trees, yet we know little about how new tree species arise.  Speciation in trees is an especially intriguing problem because their long life spans, often large, continuous populations, and propensity for outcrossing and long-distance gene flow should counteract divergent selection and the evolution of reproductive isolating barriers.  Moreover, the long life spans, delayed maturity, and large body size of trees preclude traditional experimental approaches for most species.

Our population genetic/genomic studies of Hawaiian Metrosideros have: a) revealed significant clustering of individuals by taxon on Hawaii Island and Oahu, a significant pattern of isolation by distance across the island chain, and peak morphotype richness and number of genetic clusters on islands of intermediate age; b) suggested that persistent, sharp ecotones may be required for speciation in trees; c) suggested that M. polymorpha var. glaberrima is a “flexible stem” that has given rise to island-endemic forms, and that riparian M. polymorpha var. newellii arose from M. polymorpha var. glaberrima through sympatric speciation with primary gene flow; d) revealed moderate heritabilities and contrasting genetic architectures of leaf traits in the successional varieties consistent with the purported role of M. polymorpha var. glaberrima as a “flexible stem;” and e) suggested that diversification in Metrosideros has involved the sorting of ancient variants through recurring selection.

Our ongoing studies of reproductive isolating barriers are revealing a range of partial barriers between co-occurring taxa on Hawaii Island and Oahu, including reduced or delayed pollen tube growth, reduced F1 seedling survivorship and/or fertility, and reduced backcross vigor and fertility.  Some cases of reduced hybrid fitness appear to be due to incompatibilities at disease-resistance (R) genes (evidenced through apparent hybrid necrosis), and chloroplast-nuclear incompatibility (evidenced through low survivorship of F1s and variegation and chlorosis in F2s and backcrosses).  Finally, these studies suggest that speciation may come at the cost of increased inbreeding depression within recently isolated taxa.

Variegated LxT F2s and LT-T backcrosses.

Variegated F2 and backcross seedlings from crosses between M. tremuloides, M. polymorpha race L, and their F1 hybrids.

Tree Resilience in the Face of Climate Change – We are currently leading a study of The Genetic Basis of Local Adaptation Across an Island Adaptive Radiation (NSF IOS 2204729) (2022-2026) with co-PIs: Jae Young Choi at the University of Kansas and Susan Cordell at the USDA-Forest Service, Hilo, Hawaii.  This project takes an evolutionary systems biology approach to Hawaiian Metrosideros to characterize the genetic basis of adaptation to drought and water-logging, two conditions that are expected to increase in frequency and intensity with climate change.  The three aims of the project are to: 1) contrast seedling physiology and patterns of gene expression between replicate dry- and wet-adapted taxa in response to drought and water-logging; 2) identify phenotypic traits and quantitative trait loci (QTL) for resistance to drought or water-logging and identify QTL that colocalize with differentially expressed genes (DEGs); and 3) examine the evolution of the colocalized DEG-QTL regions across the adaptive radiation to test the prediction that recurring adaptation to parallel environments involves recurring selection on shared genomic regions of predominantly ancestral origin.

Water study seedlings

Seedlings of four Hawaiian Metrosideros taxa (left to right) awaiting treatment, in drought treatment, and in water-logging treatment.

This work follows several field-, greenhouse/garden-, and environmental chamber-based experiments designed to identify key abiotic factors impacting the resilience of individual taxa to challenging environments.  These experimental studies reveal significant variation among taxa in the tolerance of seedlings to water-logging, high phosphorus, high light, UV radiation, temperature, and the mechanical stress of rushing water.  The strength of differentiation among taxa in tolerance to abiotic stress generally increases with both elevation and harshness of the environment (indicated by mean mortality rate of outplanted seedlings), which coincides with the greater genetic isolation of taxa observed at higher elevations and in extreme environments.

Biotic factors that may impact resilience in Hawaiian Metrosideros and that have been examined in our lab include kin recognition, fungal pathogens (in collaboration with researchers at USDA-ARS), and fungal endophytes.  Our studies have demonstrated variation among Metrosideros taxa in all three, although the functional significance of variation in fungal endophyte communities remains to be explored.

Metrosideros phylogeny: Through a phylogenetic analysis based on a subset of single-copy nuclear genes (Pillon et al., 2014), we recently proposed an expansion of genus Metrosideros to include Carpolepis of New Caledonia and Tepualia of South America (Pillon et al. 2015).  Subsequent analysis of 40 nuclear genes for Metrosideros and allied groups with an emphasis on Hawaiian taxa suggests that the genus arrived in Hawaii 3.1 (2.5-3.7) MYA.  Relationships within Hawaii, however, remain unresolved (Dupuis et al. 2019).

Clermontia tuberculata at Waikamoi

Clermontia tuberculata at Waikamoi

Diversification in other Tropical Plant Groups – With support from the Gordon and Betty Moore Foundation, I led an effort to identify DNA-barcoding genes from the nuclear genome that would be useful for recent plant radiations, targeting the species-rich groups Clermontia (Campanulaceae) and Cyrtandra (Gesneriaceae) in Hawaii.  In addition to identifying DNA barcodes from Roche 454 pyrosequencing of pooled-species runs (Pillon et al., 2013), we were able to reconstruct cytoplasmic-DNA-based and nuclear-DNA-based evolutionary relationships among populations and taxa within Hawaii to reveal significantly greater coalescence times in nuclear genes (Pillon et al. 2013), significant phylogenetic discordance among nuclear genes (Pillon et al. 2013), and high-resolution insights into the colonization and hybridization patterns of these groups on Hawaii Island (Johnson et al. 2019).  Work on these two plant groups is ongoing; e.g., studies of reproductive isolating barriers in Cyrtandra (Johnson et al. 2015) and parallel niche-space evolution across islands (current).  I have also collaborated on a study of cryptic adaptive radiation in trees in New Caledonia (Pillon et al., 2014) and phylogenetic analyses and the documentation of new records within non-Hawaiian plant groups (Pillon et al., 2014; Hopkins et al., 2015; Pillon et al., 2018).

Kaala summit views