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Phylogeny and Biogeography of Pacific Rubus Subgenus

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Phylogeny and Biogeography of Pacific Rubus Subgenus Phylogeny and Biogeography ofPacific Rubus Subgenus ldaeobatus (Rosaceae) Species: Investigating the Origin ofthe Endemic Hawaiian Raspberry R. macraei1 Clifford W Morden,2,4 Donald E. Gardner, 3 and Dana A. Weniger2 Abstract: The endemic Hawaiian raspberries Rubus hawaiensis and R. macraei (both subgenus Idaeobatus) had been thought to be closely related species until recent molecular studies demonstrated otherwise. These studies suggest that they are the products of separate colonizations to the Hawaiian Islands. Affin­ ities of R. hawaiensis to R. speaabilis of western North America were clearly confirmed. However, no clear relation to R. macraei has been published. This study was initiated to examine species of subg. Idaeobatus from the surrounding Pacific region as well as species from other subgenera to better evaluate bio­ geographic and phylogenetic affinities of R. macraei by means of chromosome analysis and molecular data using the chloroplast gene ndhF. Results show that R. macraei clusters in a clade with species of blackberries, subg. Rubus, and of these it is most closely linked to R. ursinus. Chromosomally, R. macraei is 2n = 6x = 42, a number that would be a new report for subg. ldaeobatus. How­ ever, polyploidy is cornmon in subg. Rubus. Analyses indicate that R. macraei and R. hawaiensis are derived from separate colonizations from North America and that similarities between them are due to convergent evolution in the Hawaiian environment. THE GENUS Rubus (Rosaceae) is a large and species (Jennings 1988, Iwatsubo et al. 1995, taxonomically complex assemblage of species Thompson 1997, Wagner et al. 1999). The consisting of several hundred sexual species most recent global treatment of Rubus was by to perhaps thousands of apomictic micro- Focke (1910, 1911, 1914), where the genus was divided into 12 subgenera and numer­ ous sections and series. The two largest of Focke's subgenera included the raspberries 1 This work was funded by National Biological Ser­ (subgenus Idaeobatus) and the blackberries vice Research Funding and the Department of Botany, (subg. Rubus = Eubatus Focke). Focke origi­ University of Hawai'i at Manoa. Manuscript accepted 3 nally placed 117 species into subg. Idaeobatus, June 2002. a number that has since increased to 135 2 Department of Botany and Center for Conservation Research and Training, University of Hawai'i at Manoa, species (Thompson 1997). In subg. Rubus, the Honolulu, Hawai'i 96822. number has risen from Focke's original 132 J USGS-Biological Resources Division, Pacific Island species to approximately 400 sexual species Ecosystems Research Center, Department of Botany, and thousands of described apomictic spe­ University of Hawai'i at Manoa, Honolulu, Hawai'i cies (Jennings 1988, Iwatsubo et al. 1995). 96822. 4 Address for correspondence: 3190 Maile Way, Frequent hybridization and reproduction University of Hawai'i at Manoa, Honolulu, Hawai'i through apomixis has made the designation of 96822 (phone: 808-956-9636; fax: 808-956-3923; E-mail: distinct species difficult in this genus (Nybom [email protected]). and Schaal 1990, Nybom and Hall 1991, Kraft et al. 1996). This situation is further Pacific Science (2003), vol. 57, no. 2:181-197 complicated by a large amount of phenotypic © 2003 by University of Hawai'i Press plasticity (Nybom and Schaal 1990, Nybom All rights reserved and Hall 1991, Kraft et al. 1996). 181 182 PACIFIC SCIENCE· April 2003 Two species of Rubus are endemic to the DNA (RAPD) markers to examine genetic Hawaiian Islands, R. hawaiensis and R. macraei variation among some species in two Rubus (Wagner et a1. 1999). Both species were subgenera and found that R. macraei did not placed in subg. Idaeobatus, section Idaeanthi, group with other Idaeobatus species, but rather series spectabiles by Focke (1911) and share a grouped with species of subg. Rubus separate number of notable morphological features. from a cluster containing subg. Idaeobatus Both species are woody in habit, possess species. However, their analysis utilized few shredding bark, have reduced prickle con­ species of these subgenera and involved many centrations, possess compound leaves with individuals derived from artificial crosses re­ three leaflets, flowers that are pink to dusky sulting in inter- and intrasubgeneric hybrids. rose-colored, and drupelets that are dark red Further, R. hawaiensis was not included in this to purple (Wagner et a1. 1999). The high analysis to allow comparison with R. macraei. degree of morphological similarity supports Two recent studies based on sequence the hypothesis that these two species are analysis of chloroplast and nuclear DNA have closely related to one another and as a result provided insight into the phylogenetic frame­ were thought to be derived from R. spectabilis, work of this genus. Examination of the chlo­ the common salmonberry from western roplast ndhF region (Howarth et a1. 1997) has North America (Hillebrand 1888, Fosberg shown the region to possess levels ofvariation 1948, Wagner et al. 1999). The differences appropriate to address questions at the species between these two species are few compared and subgeneric levels. They examined nine with the similarities. Rubus macraei tends species from subg. Idaeobatus including both to grow in a prostrate decumbent manner Hawaiian species as well as R. spectabilis. Their while R. hawaiensis grows upward with erect results surprisingly showed that the two Ha­ branches that may become arching. Other waiian species were not closely related to each morphological differences include the thick­ other. As suspected, R. hawaiensis clustered ness of the leaves, length of the terminal closely with R. spectabilis, but R. macraei did leaflet, and the coloration of the abaxial sur­ not group closely with any other species in faces of the leaves (Wagner et a1. 1999; subg. Idaeobatus. These findings were further C.W.M., pers. obs.). Although these species corroborated by Alice and Campbell (1999) are occasionally found growing sympatrically, in their investigation of phylogenetic rela­ no hybrids between them are known, yet tionships within Rubus using the internal natural hybrids between R. hawaiensis and the transcribed spacer (ITS) region ofthe nuclear invasive R. rosifolius (both subg. Idaeobatus) ribosomal DNA cistron. Alice and Campbell have been documented (Randell 2000). (1999) also showed that the two Hawaiian Given the wide morphological variation species are distantly related although R. mac­ found in this genus, alternative approaches raei clustered closely to a number of other have been employed to gain insight into this species of subg. Idaeobatus. Aside from a close difficult group, including paper chromatogra­ affinity with R. spectabilis, R. hawaiensis did not phy fingerprinting (Haskell and Garrie 1966), cluster with any distinct group. They found a isozyme techniques (Cousineau and Donnelly high similarity in the sequences of R. macraei 1989), and characterization of anthocyanin and R. ursinus, a common blackberry hybrid pigments (Jennings and Carmichael 1980). species along the North American West Nybom et a1. (1990) and Waugh et a1. (1990) Coast from northern Mexico to British Co­ first employed molecular tools to study the lumbia. Recent investigations by Alice (2002) variability in Rubus species using Southern with ITS sequences likewise showed a close hybridization analysis and DNA fingerprint­ association between R. ursinus and R. macraei. ing, respectively. However, neither method Chromosome studies have shown that provided the resolution necessary to examine the base number in Rubus is x = 7 (Graham relationships among species and subgenera of and McNicol 1995, Iwatsubo et a1. 1995, this complex genus. Graham and McNicol Hummer 1996, Thompson 1997). Although (1995) used randomly amplified polymorphic polyploidy is common, there is little evi- Rubus Systematics and Origin of R. macraei . Morden et al. 183 dence of aneuploidy in the genus. Species of MATERIALS AND METHODS subg. Idaeobatus are largely diploid (2n = 14) DNA Extraction and Sequence Analysis with occasional reports of tetraploids (2n = 28) and rarely higher numbers (Thompson Following the classification scheme of Focke 1997). Chromosome counts performed on R. (1910, 1911, 1914), 30 species of Rubus, hawaiensis have confirmed its diploid config­ mostly from the Pacific region and repre­ uration (Thompson 1995), but to date there senting five subgenera, were sampled (Table have been no counts of R. maeraei available. 1). An emphasis was placed on the subg. Subg. Rubus has a high frequency of poly­ Idaeobatus due to Focke's inclusion of both ploidy among the many species that have Hawaiian endemic species in this subgenus. been reported, and R. ursinus has counts Species were chosen for their proximity to ranging from hexaploid to dodecaploid migratory bird flight routes, chromosome (2n = 42 to 84) (Thompson 1997). number, and use in previous studies. Rubus The focus of the research reported here assamensis (subg. Malachobatus) and R. tricolor was to explore the biogeography of Rubus (subg. Dalibardastrum) were included because species in the northern Pacific region and to these species clustered close to R. maeraei in clarify relationships among these species by the ITS analysis of Alice and Campbell analyzing ndhF sequence variation. The ndhF (1999). Morgan et a1. (1994) have shown gene has recently become of interest for sys­ Fallugia to be closely related to Rubus, thus F. tematic analyses and was used here to exam­ paradoxa
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