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.
Intraspecific hybrid zones involving long-lived woody species are rare and can provide insights into the genetic basis of earlydiverging 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 Hawaiʻi 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 Hawaiʻi 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, F 1 s 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.
BackgroundDNA barcoding of land plants has relied traditionally on a small number of markers from the plastid genome. In contrast, low-copy nuclear genes have received little attention as DNA barcodes because of the absence of universal primers for PCR amplification.ResultsFrom pooled-species 454 transcriptome data we identified two variable intron-less nuclear loci for each of two species-rich genera of the Hawaiian flora: Clermontia (Campanulaceae) and Cyrtandra (Gesneriaceae) and compared their utility as DNA barcodes with that of plastid genes. We found that nuclear genes showed an overall greater variability, but also displayed a high level of heterozygosity, intraspecific variation, and retention of ancient alleles. Thus, nuclear genes displayed fewer species-diagnostic haplotypes compared to plastid genes and no interspecies gaps.ConclusionsThe apparently greater coalescence times of nuclear genes are likely to limit their utility as barcodes, as only a small proportion of their alleles were fixed and unique to individual species. In both groups, species-diagnostic markers from either genome were scarce on the youngest island; a minimum age of ca. two million years may be needed for a species flock to be barcoded. For young plant groups, nuclear genes may not be a superior alternative to slowly evolving plastid genes.
Aim The diversity and composition of species pools within oceanic archipelagos is determined by a combination of colonization, abiotic tolerance, in situ diversification, biotic interactions and extinction. The signature of biogeographic events and evolutionary processes, however, may be masked by recent coalescence and hybridization between closely related species. We used the species‐rich plant genus Cyrtandra (Gesneriaceae) to investigate the roles of colonization and hybridization in shaping community assemblages on the geologically young Hawai'i Island. Location Hawaiian Islands. Taxon Cyrtandra (Gesneriaceae). Methods We sampled 29 Cyrtandra taxa and putative hybrids across the main Hawaiian Islands and generated single nucleotide polymorphisms (SNPs) from nine single‐copy nuclear genes. Maximum likelihood and Bayesian inference were used to reconstruct phylogenetic relationships, divergence times were estimated using secondary calibrations and island ages, and ancestral area estimation was done using likelihood models. Lastly, we used a Bayesian population assignment test and principal components analysis to infer population genetic structure. Results Cyrtandra colonization of the main Hawaiian Islands appears to have followed the progression rule, whereby the oldest high Hawaiian Islands (Kaua'i and O'ahu) were colonized first, followed by colonization of the younger islands as habitat became available. Hawai'i Island was colonized four times, with two dispersal events from O'ahu and two from Maui Nui. The different colonization events gave rise to significantly uneven numbers of species, and hybridization among the incipient lineages was detected in the form of intermediate genotypes. Main conclusions Our investigation into community assembly in a species‐rich plant genus on a geologically young oceanic island revealed a history of multiple colonizations and hybridization among colonizing lineages. The rapid diversification (3.5 species/My) of one of four Cyrtandra lineages on Hawai'i Island may be the result of hybridization between genetically diverse lineages that stem from independent colonization events. Multiple colonization events followed by a merging of lineages may be particularly common during early‐stage community assembly on islands and, through the generation of genetic variation, may be especially important for species diversification.
The genus Metrosideros (Myrtaceae) comprises 50-60 species found largely across the Pacific Islands. The relationships within this genus, including the circumscriptions of the subgenera Mearnsia and Metrosideros and their relationships with the other members of the tribe Metrosidereae (namely the New Caledonian endemic genus Carpolepis and the South American Tepualia), are poorly understood. Phylogenetic analyses were carried out using previously published ITS sequences, covering most species of the tribe, and new sequences of five single-copy nuclear genes with a reduced taxon sampling. The independent and combined analyses of the five nuclear genes using a range of approaches, including Bayesian single-gene, concatenated (MrBayes), concordance (BUCKy) and coalescent (*BEAST) analyses, yielded different topologies, indicating important conflicts among phylogenies based on individual genes. The deep relationships within the tribe Metrosidereae remain poorly resolved, but our results indicate that the species of Carpolepis and Tepualia are likely nested in the genus Metrosideros. A broad circumscription of the genus Metrosideros is therefore adopted, and the new combinations Metrosideros laurifolia var. demonstrans, Metrosideros tardiflora and Metrosideros vitiensis are here published.
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