Molecular phylogeny and biogeography of Picea (Pinaceae): Implications for phylogeographical studies using cytoplasmic haplotypes
Introduction
Severe climatic oscillations associated with glacial cycles in the arctic during the late Tertiary and throughout the Quaternary resulted in great changes in species distributions and population structure (Böhle et al., 1996, Qian and Ricklefs, 2000, Liu et al., 2002, Petit et al., 2003, Hewitt, 2004). Meanwhile, descendent sea levels created land connections for intercontinental exchanges of flora and fauna, especially boreal species (Tiffney, 1985a, Tiffney, 1985b, Wen, 1999, Xiang et al., 2005). With the advance and retreat of ice sheets, species went extinct over large parts of their range, and some populations dispersed to new locations or survived in refugia and then expanded again (Hewitt, 2000, Stewart and Lister, 2001). This repeated process would on the one hand stimulate adaptation and allopatric speciation (Hewitt, 2004), whereas, on the other, provide the opportunities for hybridization between recolonized populations, even reproductively unisolated species (Abbott and Brochmann, 2003). The reticulate evolution, and biological radiation resulted from climatic, ecological and geological changes bring many difficulties to the evolutionary and biogeographical studies of some taxa with long generation times, widespread distributions and low morphological divergence.
The genus Picea A. Dietrich (spruce) is a prominent component of the boreal, montane and sub-alpine forests in the Northern Hemisphere. It includes 28–56 species depending on different systems of classification used (Farjón, 1990, Ledig et al., 2004), and most of them are confined to Eastern Asia. Farjón (2001) recognized 34 spruce species in his conifer checklist, of which 24 natively occur in Asia, 8 in North America and 2 in Europe. Monophyly of Picea has never been debated (Wright, 1955, Prager et al., 1976, Frankis, 1988, Price, 1989, Sigurgeirsson and Szmidt, 1993), but infrageneric classification of the genus remains quite controversial (Liu, 1982, Schmidt, 1989, Farjón, 1990, Farjón, 2001, Fu et al., 1999), owing to morphological convergence and parallelism (Wright, 1955), and high interspecific crossability (Ogilvie and von Rudloff, 1968, Manley, 1972, Gorden, 1976, Fowler, 1983, Fowler, 1987, Perron et al., 2000). In addition, little is known about phylogenetic relationships of most species, especially the geographically restricted species growing in the montane regions of southwest China (LePage, 2001). Moreover, the origin and biogeography of Picea have drawn great interest from both geologists and biologists (Wright, 1955, Aldén, 1987, Page and Hollands, 1987, LePage, 2001, LePage, 2003), but they are still far from being resolved. For example, the two major hypotheses for the origin and evolution of North American spruces, both suggesting a dispersal from Asia (Wright, 1955, Nienstaedt and Teich, 1972), are in conflict with the finding of Sigurgeirsson and Szmidt (1993) that Picea might have an origin in North America. Therefore, a resolved phylogeny is very important for interpreting not only biogeographical patterns but also the morphological evolution in Picea.
Using the cpDNA-RFLP analysis, Sigurgeirsson and Szmidt (1993) constructed the first molecular phylogeny of spruces at the genus level, but relationships of many species were not resolved. In particular, the result of this study may be not very accurate due, as mentioned by the authors themselves, to limitations of RFLPs for detecting changes, such as the risk of non-homology of characters. A DNA-sequence based phylogeny of the whole genus Picea has not yet been obtained due possibly to the shortage of good markers. In recent years, the combined analysis of multiple genes from one or more genomes has been successfully used in robust reconstructions of complex phylogenies, and thus shed more light on biogeographical histories of many plant groups (e.g., Kusumi et al., 2002, Xiang et al., 2005). To resolve interspecific relationships, sequences of nuclear ribosomal DNA internal transcribed spacers (nrDNA ITS) and the chloroplast trnT-trnF region are most widely used (Wang et al., 1999, Wei and Wang, 2003, Shaw et al., 2005). However, the development of DNA markers in conifers has been hampered by: (1) a large nuclear genome with highly complex gene families (Kvarnheden et al., 1995, Kinlaw and Neale, 1997, Murray, 1998), which frequently give rise to the problem of gene paralogy; (2) a mitochondrial genome with the slow molecular evolution rate and high level of infraspecific polymorphism (Ahuja, 2001); and (3) a long nrDNA ITS region, which is too intragenomically variable in length to be used in investigating species phylogenies (Maggini et al., 1998, Wei et al., 2003, Campbell et al., 2005). So most previous molecular phylogenetic studies in conifers, especially at the genus level, were based on chloroplast gene markers (Sigurgeirsson and Szmidt, 1993, Wang et al., 1999, Wang et al., 2003, Kusumi et al., 2000, Wei and Wang, 2003).
In Pinaceae, the chloroplast, mitochondrial and nuclear genomes are paternally, maternally and biparentally inherited, respectively (Stine and Keathley, 1990, Sutton et al., 1991, Hipkins et al., 1994, Mogensen, 1996, Ahuja, 2001). Distinct phylogenies may be obtained from genes of the different genomes as a result of different inheritance pathways and responses to processes such as lineage sorting, gene duplication/deletion, and hybrid speciation (Doyle, 1997, Maddison, 1997, Wang et al., 2000). A good understanding of the inconsistency from distinct genomes will provide more valuable implications for the evolutionary process. Here, we reconstruct the molecular phylogeny of Picea using sequences of two cpDNA regions trnT-trnF and trnC-trnD. The later comprises the trnC-petN intergenic spacer (IGS), petN gene, petN-psbM IGS, psbM gene and psbM-trnD IGS and has shown great potential in phylogenetic analysis at low taxonomic level (Lee and Wen, 2004, Shaw et al., 2005). Considering that the variation region in the first intron of nad5, a mitochondrial gene encoding subunit 5 of NADH dehydrogenase, used in the phylogeographic study of black spruce and red spruce is monomorphic in the other spruces and conifers surveyed by Jaramillo-Correa et al. (2003), we also sequence this region to obtain the genetic information of maternal lineages. Based on the joint cp- and mt-DNA analysis, we discuss the evolutionary history, biogeography and the evolution of morphological characters of this complicated genus.
Section snippets
Plant materials
We sampled all of the 34 spruce species recognized in Farjón, 1990, Farjón, 2001 except Picea aurantiaca, an endangered species endemic to West Sichuan, China, which has been treated as a variety of P. asperata (Fu et al., 1999). Many species were represented by several individuals, and a total of 103 individuals were analyzed. Cathaya argyrophylla Chun et Kuang and two Pinus species, P. strobus L. and P. thunbergii Parl., were chosen as outgroups considering the close relationships among
Sequence characterization
For the two cpDNA regions we analyzed, most Picea species do not have intraspecific variations based on the sampled individuals. Intraspecific variations were only detected from P. brachytyla, P. koraiensis, P. likiangensis, P. meyeri and P. schrenkiana, and nearly all of them are autapomorphies such as one substitution or indel (Fig. 1). Length of the trnC-trnD region is relatively conserved in the 33 Picea species sampled, ranging from 2324 (P. sitchensis and P. smithiana) to 2339 bp (P. glauca
Phylogeny and biogeography of the genus Picea: Implications for phylogeographical studies
Monophyly of Picea has long been commonly accepted (Wright, 1955, von Rudloff, 1967, Rushforth, 1987, Frankis, 1988, Sigurgeirsson and Szmidt, 1993), but the subdivision of the genus into subgenera, sections and series is greatly debated since most classification systems were formulated on few, easily scored characters from gross morphology (e.g., Colleau, 1968, Sudo, 1968, Bobrow, 1970, Schmidt-Vogt, 1977, Liu, 1982). Willkomm (1887) divided Picea into two sections, Eupicea and Omorika. Liu
Acknowledgments
The authors thank the two anonymous reviewers for their insightful comments and suggestions on the manuscript. We also thank Drs. Mark Chase and Aljos Farjón of Royal Botanic Garden, Kew, UK for providing DNA samples of 5 Picea species; Dr. Zsolt Debreczy of the International Dendrological Research Institute, Wellesley, MA (USA) for his kind help in collecting leaf materials of some North American spruces; Dr. F. Thomas Ledig of USDA Forest Service, and Department of Plant Science, University
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