Climate oscillation during the Quaternary associated with landscape heterogeneity promoted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia

We investigated the biogeographic history of Kalopanax septemlobus, one of the most widespread temperate tree species in East Asia, using a combined phylogeographic and palaeodistribution modelling approach. Range‐wide genetic differentiation at nuclear microsatellites (G′ST = 0.709; 2205 samples genotyped at five loci) and chloroplast DNA (GST = 0.697; 576 samples sequenced for 2055 bp at three fragments) was high. A major phylogeographic break in Central China corresponded with those of other temperate species and the spatial delineation of the two temperate forest subkingdoms of East Asia, consistent with the forests having been isolated within both East and West China for multiple glacial–interglacial cycles. Evidence for multiple glacial refugia was found in most of its current range in China, South Japan and the southernmost part of the Korean Peninsula. In contrast, lineage admixture and absence of private alleles and haplotypes in Hokkaido and the northern Korean Peninsula support a postglacial origin of northernmost populations. Although palaeodistribution modelling predicted suitable climate across a land‐bridge extending from South Japan to East China during the Last Glacial Maximum, the genetic differentiation of regional populations indicated a limited role of the exposed sea floor as a dispersal corridor at that time. Overall, this study provides evidence that differential impacts of Quaternary climate oscillation associated with landscape heterogeneity have shaped the genetic structure of a wide‐ranging temperate tree in East Asia.

[1]  Hang Sun,et al.  Chloroplast phylogeography of Terminalia franchetii (Combretaceae) from the eastern Sino-Himalayan region and its correlation with historical river capture events. , 2011, Molecular phylogenetics and evolution.

[2]  Y. Qiu,et al.  Plant molecular phylogeography in China and adjacent regions: Tracing the genetic imprints of Quaternary climate and environmental change in the world's most diverse temperate flora. , 2011, Molecular phylogenetics and evolution.

[3]  Y. Isagi,et al.  Lineage admixture during postglacial range expansion is responsible for the increased gene diversity of Kalopanax septemlobus in a recently colonised territory , 2011, Heredity.

[4]  S. Rossiter,et al.  Identifying the effects of the Pleistocene on the greater horseshoe bat, Rhinolophus ferrumequinum, in East Asia using ecological niche modelling and phylogenetic analyses , 2011 .

[5]  Hiroshi Takahashi,et al.  Disjunct distribution of chloroplast DNA haplotypes in the understory perennial Veratrum album ssp. oxysepalum (Melanthiaceae) in Japan as a result of ancient introgression. , 2010, The New phytologist.

[6]  Da‐Yong Zhang,et al.  Nuclear and chloroplast DNA phylogeography reveal two refuge areas with asymmetrical gene flow in a temperate walnut tree from East Asia. , 2010, The New phytologist.

[7]  Rempei Suwa,et al.  Phylogeography of Ophiorrhiza japonica (Rubiaceae) in continental islands, the Ryukyu Archipelago, Japan , 2010 .

[8]  Mark Monmonier,et al.  Maximum‐Difference Barriers: An Alternative Numerical Regionalization Method* , 2010 .

[9]  M. Ashcroft Identifying refugia from climate change , 2010 .

[10]  Y. Isagi,et al.  How did the exposed seafloor function in postglacial northward range expansion of Kalopanax septemlobus? Evidence from ecological niche modelling , 2010, Ecological Research.

[11]  J. Marthick,et al.  Chloroplast evidence for geographic stasis of the Australian bird‐dispersed shrub Tasmannia lanceolata (Winteraceae) , 2010, Molecular ecology.

[12]  Y. Ide,et al.  Contrasting patterns of nuclear microsatellite genetic structure of Fraxinus mandshurica var. japonica between northern and southern populations in Japan , 2010 .

[13]  Seong‐Joong Kim,et al.  Vegetation changes in western central region of Korean Peninsula during the last glacial (ca. 21.1–26.1 cal kyr BP) , 2010 .

[14]  W. Ye,et al.  Genetic variation of Ardisia crenata in south China revealed by nuclear microsatellite , 2010 .

[15]  J. Stewart,et al.  Refugia revisited: individualistic responses of species in space and time , 2010, Proceedings of the Royal Society B: Biological Sciences.

[16]  M. Stephens,et al.  Inferring weak population structure with the assistance of sample group information , 2009, Molecular ecology resources.

[17]  Y. Qiu,et al.  Molecular phylogeography of East Asian Kirengeshoma (Hydrangeaceae) in relation to quaternary climate change and landbridge configurations. , 2009, The New phytologist.

[18]  Pablo Librado,et al.  DnaSP v5: a software for comprehensive analysis of DNA polymorphism data , 2009, Bioinform..

[19]  Y. Qiu,et al.  Did glacials and/or interglacials promote allopatric incipient speciation in East Asian temperate plants? Phylogeographic and coalescent analyses on refugial isolation and divergence in Dysosma versipellis. , 2009, Molecular phylogenetics and evolution.

[20]  N. Tomaru,et al.  Genetic divergence in nuclear genomes between populations of Fagus crenata along the Japan Sea and Pacific sides of Japan , 2009, Journal of Plant Research.

[21]  Ping Chen,et al.  History and evolution of alpine plants endemic to the Qinghai‐Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae) , 2009, Molecular ecology.

[22]  Zhiduan Chen,et al.  Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere , 2009 .

[23]  Y. Qiu,et al.  Phylogeography of two East Asian species in Croomia (Stemonaceae) inferred from chloroplast DNA and ISSR fingerprinting variation. , 2008, Molecular phylogenetics and evolution.

[24]  C. Dobeš,et al.  Phylogeography of a living fossil: pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion. , 2008, Molecular phylogenetics and evolution.

[25]  Gordon Luikart,et al.  LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method , 2008, BMC Bioinformatics.

[26]  Zhekun Zhou,et al.  Phylogeny and biogeography of the genus Ainsliaea (Asteraceae) in the Sino-Japanese region based on nuclear rDNA and plastid DNA sequence data. , 2007, Annals of botany.

[27]  M. Möller,et al.  High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam , 2007, Molecular ecology.

[28]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[29]  Chull-Hwan Chung Vegetation response to climate change on Jeju Island, South Korea, during the last deglaciation based on pollen record , 2007 .

[30]  Pedro Jordano,et al.  Can Population Genetic Structure Be Predicted from Life‐History Traits? , 2007, The American Naturalist.

[31]  Joey Shaw,et al.  Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. , 2007, American journal of botany.

[32]  Jody Hey,et al.  Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics , 2007, Proceedings of the National Academy of Sciences.

[33]  W. Collins,et al.  The Community Climate System Model Version 3 (CCSM3) , 2006 .

[34]  T. Nakashizuka,et al.  Microsatellite loci for a sparsely distributed species, Kalopanax pictus (Araliaceae) in Japanese temperate forests , 2006 .

[35]  Tom Fawcett,et al.  An introduction to ROC analysis , 2006, Pattern Recognit. Lett..

[36]  A. Momohara,et al.  Phylogeography of the genus Cardiandra based on genetic variation in cpDNA sequences , 2006, Journal of Plant Research.

[37]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[38]  Mike Steel,et al.  Estimating the Relative Order of Speciation or Coalescence Events on a Given Phylogeny , 2006, Evolutionary bioinformatics online.

[39]  Y. Ide,et al.  Wide‐range analysis of genetic structure of Betula maximowicziana, a long‐lived pioneer tree species and noble hardwood in the cool temperate zone of Japan , 2005, Molecular ecology.

[40]  P. Hedrick A STANDARDIZED GENETIC DIFFERENTIATION MEASURE , 2005, Evolution; international journal of organic evolution.

[41]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[42]  R. Petit,et al.  Conserving biodiversity under climate change: the rear edge matters. , 2005, Ecology letters.

[43]  S. Kalinowski hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness , 2005 .

[44]  E. Heyer,et al.  Geographic Patterns of (Genetic, Morphologic, Linguistic) Variation: How Barriers Can Be Detected by Using Monmonier's Algorithm , 2004, Human biology.

[45]  T. Hsu,et al.  Phylogeography of the component species of broad-leaved evergreen forests in Japan, based on chloroplast DNA variation , 2004, Journal of Plant Research.

[46]  P. Taberlet,et al.  The power and promise of population genomics: from genotyping to genome typing , 2003, Nature Reviews Genetics.

[47]  J. Tate,et al.  Paraphyly of Tarasa (Malvaceae) and Diverse Origins of the Polyploid Species , 2003 .

[48]  D. K. Lee,et al.  A Morphometric Analysis of the Eastern Asian Kalopanax Septemlobus (Thunb.) Koidz. (Araliaceae) , 2003 .

[49]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[50]  C. Schlötterer,et al.  microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets , 2003 .

[51]  L. Excoffier,et al.  A simulated annealing approach to define the genetic structure of populations , 2002, Molecular ecology.

[52]  D. Irwin PHYLOGEOGRAPHIC BREAKS WITHOUT GEOGRAPHIC BARRIERS TO GENE FLOW , 2002, Evolution; international journal of organic evolution.

[53]  I. Prentice,et al.  Diversity of temperate plants in east Asia , 2001 .

[54]  S. P. Harrison,et al.  Palaeovegetation (Communications arising): Diversity of temperate plants in east Asia , 2001, Nature.

[55]  A. Kremer,et al.  SGS--Spatial Genetic Software: a computer program for analysis of spatial genetic and phenotypic structures of individuals and populations. , 2001, The Journal of heredity.

[56]  Jimin Sun,et al.  Stratigraphic Evidence for the Uplift of the Tibetan Plateau between ∼1.1 and ∼0.9 myr Ago , 2000, Quaternary Research.

[57]  R. Ricklefs,et al.  Large-scale processes and the Asian bias in species diversity of temperate plants , 2000, Nature.

[58]  Mark P. Simmons,et al.  Gaps as characters in sequence-based phylogenetic analyses. , 2000, Systematic biology.

[59]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[60]  R. Bradley Paleoclimatology: Reconstructing Climates of the Quaternary , 1999 .

[61]  R. Petit,et al.  Identifying Populations for Conservation on the Basis of Genetic Markers , 1998 .

[62]  T. Nakashizuka,et al.  Spatial and temporal dispersal of Kalopanax pictus seeds in a temperate deciduous forest, central Japan , 1998, Plant Ecology.

[63]  G. Hewitt Some genetic consequences of ice ages, and their role in divergence and speciation , 1996 .

[64]  M. Kimura Quaternary Paleogeography of the Ryukyu Arc , 1996 .

[65]  R. Petit,et al.  High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco , 1996, Theoretical and Applied Genetics.

[66]  J. Goudet FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics , 1995 .

[67]  R. Petit,et al.  A set of universal primers for amplification of polymorphic non‐coding regions of mitochondrial and chloroplast DNA in plants , 1995, Molecular ecology.

[68]  H. Harpending,et al.  Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. , 1994, Human biology.

[69]  A. Momohara Floral and paleoenvironmental history from the late Pliocene to middle Pleistocene in and around central Japan , 1994 .

[70]  W. Li,et al.  Statistical tests of neutrality of mutations. , 1993, Genetics.

[71]  H. Harpending,et al.  Population growth makes waves in the distribution of pairwise genetic differences. , 1992, Molecular biology and evolution.

[72]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[73]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[74]  M. Nei Molecular Evolutionary Genetics , 1987 .

[75]  M. Tsukada Map of Vegetation during the Last Glacial Maximum in Japan , 1985, Quaternary Research.

[76]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[77]  Yoshio Tateno,et al.  Accuracy of estimated phylogenetic trees from molecular data , 1983, Journal of Molecular Evolution.

[78]  W. F. Thompson,et al.  Rapid isolation of high molecular weight plant DNA. , 1980, Nucleic acids research.

[79]  Hans-Rolf Gregorius,et al.  The concept of genetic diversity and its formal relationship to heterozygosity and genetic distance , 1978 .

[80]  Arthur Cronquist,et al.  Floristic Regions of the World , 1978 .

[81]  M. Nei Analysis of gene diversity in subdivided populations. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[82]  J. Pritchard,et al.  Documentation for structure software : Version 2 . 3 , 2009 .

[83]  Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/joc.1276 VERY HIGH RESOLUTION INTERPOLATED CLIMATE SURFACES FOR GLOBAL LAND AREAS , 2005 .

[84]  S. Muse Examining rates and patterns of nucleotide substitution in plants , 2004, Plant Molecular Biology.

[85]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[86]  I. Prentice,et al.  Palaeovegetation. Diversity of temperate plants in east Asia. , 2001, Nature.

[87]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.

[88]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[89]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..