UC Berkeley

The genus Artemisia

Biogeography and chemosystematics in a phylogenetic context (Phylochemistry)

By Christopher Rollin Hobbs

Doctor of Philosophy in Integrative Biology

University of California, Berkeley

Professor Bruce G. Baldwin, Chair

Artemisia is the most diverse genus in tribe Anthemideae, consisting of 350 to 500 species (Hillebrand, 1888; Vallès & McArthur, 2001; Vallès et al., 2003). These wind-pollinated herbaceous and shrubby taxa, including mugworts, sagebrushes, and wormwoods, occur widely in the Northern Hemisphere and sparingly in southern South America and sub- Saharan Africa. I studied the biogeography of the genus with an emphasis on the three Hawaiian taxa in the context of world-wide distribution.

I sought to determine whether Hawaiian Artemisia (Compositae-Anthemideae), with lowland and subalpine species, represents such an example by investigating the origin and relationships of the Hawaiian taxa.

Molecular phylogenetic analyses of Hawaiian Artemisia were conducted using nuclear ribosomal transcribed spacers, chloroplast DNA intergenic spacers, and morphology. Timing of divergence events associated with inferred dispersals was estimated with calibration from fossil pollen records. Historical biogeographic analyses based on molecular trees and ecological modeling of distributions of extant taxa were used to aid interpretation of geographic and habitat shifts associated with diversification and long-distance dispersal.

The findings indicate that the Hawaiian-endemic species (A. australis, A. kauaiensis, and A. mauiensis) constitute a clade that is sister to southeast Asian A. chinensis, which, like the Hawaiian endemics, has ribbed fruit walls and, unlike other members of Artemisia: except A. kauaiensis, has a distinct pappus, often associated with dispersal ability in Compositae. The clade encompassing A. chinensis and Hawaiian Artemisia was resolved to be most likely of Asian origin.

An ecological shift in Hawaiian Artemisia from tropical coastal habitats to drier and colder subalpine slopes is consistent with evidence from recent studies by Tkach and others, and data reported here, for repeated colonisation of the arctic by diverse lineages of Artemisia. Artemisia appears to be prone to such anticlimatic ecological shifts, which may explain this exceptional example of an ancestrally lowland tropical lineage in the Hawaiian high-montane flora.

Since the genus Artemisia has an abundance of secondary metabolites (SM), from a variety of distinct biosynthetic pathways, I sought to determine if these compounds had biogeographical signal, and were more influenced by environment, or mostly under genetic control and conserved. The odor compounds, or volatile organic constituents (VOCs), with up to 200 possible in one species was characterized by gas chromatograph/mass spectroscopy, and are a strong characteristic of the genus. Based on their odors, they seem to be distinct and varied within individual species.

First I sought to determine if compounds from all major constituent classes (alkaloids, terpenes, fatty acids, phenolic compounds) were under environmental or genetic control. The use of SM for solving taxonomic problems is called chemotaxonomy or chemosystematics. Use of SM in systematics, by tradition called chemosystematics, has been extensive for more than a half century and predates macromolecular approaches.

A comprehensive search of the chemosystematics literature was undertaken, and a previously published dataset of 24 leaf fatty acids for 123 taxa from all major gymnosperm clades (cycads, ginkgos, gnetophytes, and conifers) was compared with trees from rbcL chloroplast sequence data for the same taxa using comparative analyses in R to determine phylogenetic signal and to evaluate the mode of evolution of the chemical traits. Strong evolutionary constraint of the fatty acid data adds weight to the idea that fatty acids are more suitable for use as characters in phylogenetic analyses than non-structural secondary compounds. The relative benefits and drawbacks of chemical data are briefly discussed, along with potential problems in their collection, extraction, analysis, and interpretation.

Volatile organic constituents are prominent in the genus Artemisia, and many of these volatile compounds such as thujone and 1,8-cineol, are associated with defensive behavior such as anti- herbivory, anti-encroachment, and antimicrobial effects in plants. I sought to test the hypothesis that these toxic compounds might be lost in island settings over evolutionary time because of a demonstrable lack of herbivores and other encroaching species within the time frame of early colonization. I show show a dramatic example of island tameness in plants in Artemisia. In the 74 species sampled across the genus, 10 abundant and widely-studied, toxic terpene compounds that are known to inhibit seed germination, root development, and herbivore feeding9 demonstrate repeated loss, in two separate island lineages in the Hawaiian and Canary Islands. This is the first phylogeny-based study demonstrating this in plants, whereas island tameness has been widely discussed in animals, and well-known examples such as the dodo of Mauritius, Galápagos island iguanas are common knowledge. The tameness of the Falkland Island wolf, was noted by Darwin.