Phylogeny and Biogeography of the Arbutoideae (Ericaceae): Implications for the Madrean-Tethyan Hypothesis

Phylogenetic relationships within subfamily Arbutoideae (Ericaceae) were estimated using parsimony and maximum likelihood analyses of sequence data from the ITS region and part of the large subunit of nuclear ribosomal DNA. The data support the monophyly of Arctostaphylos, Arctous, and Comarostaphylis, but suggest that Arbutus is not monophyletic, with Mediterranean Basin species more closely related to the clade containing Arctostaphylos, Arctous, Comarostaphylis, Ornithostaphylos, and Xylococcus than to the western North American species of Arbutus. Calibration of branch lengths with the fossil record suggests that a vicariance event occurred among members of the Arbutoideae between western North America and the Mediterranean Basin at the Paleogene/Neogene boundary, consistent with the Madrean-Tethyan hypothesis. Vicariance biogeography is of considerable interest to many botanists, and the question of disjunct mediterranean floras has been given substantial attention (see Liston 1997 for a review). Studies from the Pinaceae (Liston et al. 1999), Datiscaceae (Liston et al. 1989a; Liston et al. 1992) and this study suggest that the occurrence of disjunct taxa can be explained by vicariance in the middle Tertiary. Other studies from the Asteraceae (Liston et al. 1989b; Liston and Kadereit 1995) and Styracaceae (Fritsch 1996) instead suggest that mediterranean disjuncts may be the result of more recent dispersal events, or convergent evolution. The phylogenetic and biogeographic relationships of taxa comprising mediterranean floras are proving to be complex, and it is likely that there will be low levels of correlated history among the different groups investigated. However, as more data are gathered from taxa exhibiting North American/Mediterranean Basin disjunctions, a clearer understanding of the flora’s historical biogeography will be gained. Various hypotheses have been suggested for the origin of disjunct taxa found in the mediterranean climates of western North America and the Mediterranean Basin (see Fritsch 1996 for a review). Axelrod (1973, 1975) hypothesized that a continuous, sclerophyllous, dry-adapted flora existed between western North America (‘‘Madrean’’) and Eurasia (‘‘Tethyan’’) until the end of the Oligocene (ca. 25 MYA). It is generally accepted (McKenna 1975, 1983; Wolfe 1975; Tiffney 1985b; and references therein) that western Europe and North America were in contact until late Eocene time (ca. 40 MYA). However, Axelrod suggests that even as North America continued moving westward during the Oligocene, drops in sea level and the presence of microcontinents and volcanic islands maintained the potential for gene flow across a still narrow Atlantic Ocean until the Paleogene/Neogene boundary (see also Tiffney 1985b). Alternatively, Raven (1973) and Wolfe (1975) have suggested that the present-day distribution of elements appearing to belong to a Madrean-Tethyan flora could be the result of convergent adaptation to similar dry climates, or the result of long-distance dispersal. For a group to be consistent with the Madrean-Tethyan hypothesis, disjunct taxa should (1) show a sistergroup relationship and (2) exhibit an estimated divergence time greater than approximately 25 million years, corresponding to the Paleogene/Neogene boundary (Fritsch 1996). The Arbutoideae is a distinct and natural group within the Ericaceae based on fruit and flower morphology, as well as anatomy and phytochemistry (Cox 1948; Stevens 1971). Six genera are commonly recognized; Arbutus, Arctostaphylos, Arctous, Comarostaphylis, Ornithostaphylos, and Xylococcus (Small 1914; Adams 1940; Stevens 1971; Diggs and Breckon 1981). The Arbutoideae are dry-adapted sclerophyllous taxa and most of the diversity in the group is in regions of mediterranean climate in western North America (Table 1). Exceptions to this primary distribution include the circumarctic Arctous alpina, circumboreal Arctostaphylos uva-ursi, and four species of Arbutus that occur in mediterranean regions of Europe, North Africa, and the Middle East. 132 [Volume 26 SYSTEMATIC BOTANY TABLE 1. Genera comprising the Arbutoideae with species number and general distributions. Taxon # of species Distribution Arbutus L. ca. 11 West coast of N. America through Mexico and Central America; western Europe through the Mediterranean region, northern Africa and parts of the Middle East. Arctostaphylos Adans. ca. 62 Northern hemisphere distribution that consists mainly of the circumboreal A. uva-ursi. The center of diversity is the California floristic province. Arctous Nied. 2 Circumarctic distribution. Comarostaphylis Zucc. 9 Southern California to northern Baja California and from the Mexican highlands to Central America. Ornithostaphylos Small 1 Southern California to northern Baja California. Xylococcus Nutt. 1 Southern California to northern Baja California. Arbutus is characterized by baccate fruit, with multiple ovules per locule, and papillose fruit surface (Small 1914; Diggs and Breckon 1981; Sørensen 1995). Three species of Arbutus occur in the Mediterranean region from North Africa to the Middle East; A. unedo, A. andrachne, and A. x andrachnoides. The latter is hypothesized to be of hybrid origin between A. unedo and A. andrachne (Callan 1941). Arbutus canariensis is endemic to the Canary Islands. The remaining eight species of Arbutus occur in the Western Hemisphere. Of these, A. xalapensis, A. texana, A. peninsularis, A. tessellata, A. arizonica, A. occidentalis, and A. madrensis have a Neotropical distribution with A. xalapensis being the most widespread and variable. Arbutus menziesii extends from British Columbia to Baja California along the West Coast of North America. Because of the disjunct distribution between mediterranean climates of western North America and the Mediterranean Basin, Axelrod (1975) cited Arbutus as a component of the Madrean-Tethyan flora. Arctostaphylos has a northern hemispheric distribution that consists mainly of the circumboreal Arctostaphylos uva-ursi. The peak of distribution for Arctostaphylos is the California Floristic Province where all 62 species occur. Arctostaphylos is characterized by a drupaceous fruit with a smooth surface with nutlets that are usually separable, as well as inflorescences that begin development at the end of the growing season, but over-winter to bloom the following season (nascent inflorescences; Wells 1992). The wide range of character states within Arctostaphylos may account for the previous inclusion of Arctous, Comarostaphylis, Ornithostaphylos, and Xylococcus. Arctous ranges from tundra to alpine and subalpine habitats, and of the two species of Arctous, A. alpina makes up most of the circumarctic distribution. Although Arctous has, at times, been subsumed within Arctostaphylos (Candolle 1839; Klotzsch 1851; Walpers 1852; Hooker 1876; Parry 1884; Gray 1886; Webb 1972; Wilber and Luteyn 1978), distinguishing characters include deciduous foliage, lack of recurved appendages on the anthers and lack of nascent inflorescences (Drude 1891; Small 1914; Eastwood 1934; Adams 1940; Hitchcock 1959; Watson 1965; Stevens 1971). The nine species of Comarostaphylis occur in subtropical chaparral and oak-pine forests of Central America, Mexico and the southwestern United States. Comarostaphylis, at times placed within Arctostaphylos (Candolle 1839; Parry 1884; Gray 1886; Drude 1891; Watson 1965; Wilber and Luteyn 1978), is distinguished by drupaceous fruit with a papillose surface and lack of nascent inflorescences (Walpers 1852; Small 1914; Eastwood 1934; Adams 1940; Stevens 1971; Diggs and Breckon 1981). The monotypic Ornithostaphylos occurs in chaparral from northern Baja California to southern California. Like Comarostaphylis, Ornithostaphylos has, at times, been treated as Arctostaphylos (Parry 1884; Watson 1965; Wilber and Luteyn 1978). However, characters such as opposite or whorled leaves, carpels each containing two locules and two seeds, and a unique, much branched inflorescence give support to its generic circumscription (Small 1914; Adams 1940; Stevens 1971). The monotypic Xylococcus has often been included within Arctostaphylos (Walpers 1852; Hooker 1876; Parry 1884; Gray 1886; Drude 1891; Watson 1965; Wilber and Luteyn 1978), but can be distinguished by corolla, filament, and fruit morphology (Small 1914; Eastwood 1934; Adams 1940; Stevens 1971). Xylococcus has a similar distribution to that of Ornithostaphylos but its range extends farther 2001] 133 HILEMAN ET AL.: ARBUTOIDEAE PHYLOGENY & BIOGEOGRAPHY TABLE 2. Taxa included in phylogenetic analysis based on the ITS region and partial 28S sequence data. P 5 V. T. Parker, V 5 M. C. Vasey, M 5 S. Markos, LH 5 Lenz and Henrickson, SFSU 5 Herbarium at San Francisco State University, OSU 5 Herbarium at Oregon State University, RSA 5 Herbarium at Rancho Santa Anna, HBG 5 Huntington Botanic Garden. Taxa indicated with * were included in the maximum likelihood analysis. Taxon Specimen GenBank Acc. ITS GenBank Acc. LSU