Molecular phylogeny and biogeography of Picea (Pinaceae): Implications for phylogeographical studies using cytoplasmic haplotypes

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Abstract

The center of diversity is not necessarily the place of origin, as has been established by many plant molecular phylogenies. Picea is a complicated but very important genus in coniferous forests of the Northern Hemisphere, with a high species diversity in Asia. Its phylogeny and biogeography were investigated here using sequence analysis of the paternally inherited chloroplast trnC-trnD and trnT-trnF regions and the maternally inherited mitochondrial nad5 intron 1. We found that the North American P. breweriana and P. sitchensis were basal to the other spruces that were further divided into three clades in the cpDNA phylogeny, and that the New World species habored four of five mitotypes detected, including two ancestral ones and three endemics. These results, combined with biogeographic analyses using DIVA and MacClade and fossil evidence, suggest that Picea originated in North America, and that its present distribution could stem from two times of dispersal from North America to Asia by the Beringian land bridge, and then from Asia to Europe. Most of the northeastern Asian species and the European P. abies could arise from a recent radiation given the very low interspecific genetic differentiation and pure mitotype of them. Considering that the ancestral mtDNA polymorphism can be preserved in many descendant species, even distantly related ones, we suggest that more species, at least the closely related ones, should be sampled in the phylogeographical study using cytoplasmic haplotypes if possible. In addition, we also discussed the evolution and phylogenetic utility of morphological characters in Picea.

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

References (111)

  • M.R. Ahuja

    Recent advances in molecular genetics of forest trees

    Euphytica

    (2001)
  • B. Aldén

    Taxonomy and geography of the genus

    Int. Dendr. Soc. Yearb.

    (1987)
  • D.I. Axelrod

    The Eocene Thunder Mountain flora of central Idaho

    Univ. Calif. Publ. Geol. Sci.

    (1998)
  • H.J. Bandelt et al.

    Median-joining networks for inferring intraspecific phylogenies

    Mol. Biol. Evol.

    (1999)
  • E.G. Bobrow

    Generis Picea Historia et Systematica

    Nov. Syst. Pl. Vasc.

    (1970)
  • U.R. Böhle et al.

    Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae)

    Proc. Natl. Acad. Sci. USA

    (1996)
  • L.Y. Budantsev

    The fossil flora of the Paleogene climatic optimum in northeastern Asia

  • C. Colleau

    Anatomie comparée des feuilles de Picea

    Cellule

    (1968)
  • B. Demesure et al.

    A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants

    Mol. Ecol.

    (1995)
  • J.J. Doyle et al.

    A rapid DNA isolation procedure for small quantities of fresh leaf tissue

    Phytochem. Bull.

    (1987)
  • J.J. Doyle

    Trees within trees: genes and species, molecules and morphology

    Syst. Biol.

    (1997)
  • A. Farjón

    Pinaceae: Drawings and Descriptions of the Genera Abies, Cedrus, Pseudolarix, Keteleeria, Nothotsuga, Tsuga, Cathaya, Pseudotsuga, Larix and Picea

    (1990)
  • Farjón, A., 2001. World Checklist and Bibliography of Conifers, Second edn. Royal Bot. Gard., Kew,...
  • J.S. Farris et al.

    Testing significance of incongruence

    Cladistics

    (1995)
  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • Fowler, D.P., Roche, L., 1976. Genetics of Engelmann spruce. Forest Service Research Paper, USDA...
  • D.P. Fowler

    The hybrid black × sitka spruce, implications to phylogeny of the genus Picea

    Can. J. For. Res.

    (1983)
  • D.P. Fowler

    The hybrid white × sitka spruce: species crossability

    Can. J. For. Res.

    (1987)
  • M.P. Frankis

    Generic inter-relationships in Pinaceae

    Notes Roy. Bot. Gard. Edinb.

    (1988)
  • L. Fu et al.

    Picea

  • O. Gascuel

    BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data

    Mol. Biol. Evol.

    (1997)
  • A.G. Gorden

    The taxonomy and genetics of Picea rubens and its relationship to Picea mariana

    Can. J. Bot.

    (1976)
  • F. Gugerli et al.

    Haplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western Alps

    Mol. Ecol.

    (2001)
  • S. Guindon et al.

    A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood

    Syst. Biol.

    (2003)
  • G.M. Hewitt

    The genetic legacy of the Quaternary ice ages

    Nature

    (2000)
  • G.M. Hewitt

    Genetic consequences of climatic oscillations in the Quaternay

    Philos. Trans. R. Soc. Lond. B

    (2004)
  • V.D. Hipkins et al.

    Organelle genome in conifers: structure, evolution, and diversity

    For. Genet.

    (1994)
  • J. Huang et al.

    Estimation of the age of extant Ephedra using chloroplast rbcL sequence data

    Mol. Biol. Evol.

    (2003)
  • J.P. Huelsenbeck et al.

    Bayesian inference of phylogeny and its impact on evolutionary biology

    Science

    (2001)
  • J.P. Jaramillo-Correa et al.

    Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer

    Mol. Ecol.

    (2004)
  • J.P. Jaramillo-Correa et al.

    Mitochondrial genome recombination in the zone of contact between two hybridizing conifers

    Genetics

    (2005)
  • J.P. Jaramillo-Correa et al.

    Cross-species amplification of mitochondrial DNA sequence-tagged-site markers in conifers: the nature of polymorphism and variation within and among species in Picea

    Theor. Appl. Genet.

    (2003)
  • S. Jeandroz et al.

    A set of primers for amplification of mitochondrial DNA in Picea abies and other conifer species

    Mol. Ecol. Not.

    (2002)
  • A.D. Johansen et al.

    Mitochondrial haplotype distribution, seed dispersal and patterns of postglacial expansion of ponderosa pine

    Mol. Ecol.

    (2003)
  • K. Kobayashi et al.

    DNA identification of Picea species of the last Glacial Age in northern Japan

    Jpn. J. Hist. Bot.

    (2000)
  • J. Kusumi et al.

    Phylogenetic relationships in Taxodiaceae and Cupressaceae sensu stricto based on matK gene, chlL gene, trnL-trnF IGS region, and trnL intron sequences

    Am. J. Bot.

    (2000)
  • J. Kusumi et al.

    Molecular evolution of nuclear genes in Cupressaceae, a group of conifer trees

    Mol. Biol. Evol.

    (2002)
  • A. Kvarnheden et al.

    A cdc2 homologue and closely related processed retropseudogenes from Norway spruce

    Plant Mol. Biol.

    (1995)
  • F.T. Ledig et al.

    Relationships among the spruces (Picea, Pinaceae) of southwestern North America

    Syst. Bot.

    (2004)
  • B.A. LePage

    The evolution, biogeography and palaeoecology of the Pinaceae based on fossil and extant representatives

    Acta Hort.

    (2003)
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