Species status and phylogeography of two closely related Coptolabrus species (Coleoptera: Carabidae) in South Korea inferred from mitochondrial and nuclear gene sequences

We investigated the species status and intraspecific phylogeography in South Korea of two ground beetle species, Coptolabrus jankowskii and Coptolabrus smaragdinus (Coleoptera: Carabidae), using statistical parsimony networks and nested clade analyses based on sequences from the mitochondrial cytochrome oxidase subunit I (COI) and nuclear phosphoenolpyruvate carboxykinase (PepCK) and wingless (Wg) genes. Although traditional parsimony tree construction generally failed to resolve interspecific relationships and construct biologically meaningful genealogies, analysis using statistical parsimony networks yielded statistically significant inter‐ and intraspecific genealogical structures. We found that although these two species represent a notable case of trans‐species polymorphisms in both mitochondrial and nuclear gene sequences, their status as separate species was evidenced by the nonrandom association between species and nested clades at various nesting levels. The exceptional occurrence of shared identical or very similar COI sequences was considered to be the result of introgressive hybridization. In addition, range expansion and fragmentation events across the Korean Peninsula and adjacent islands were inferred from nested clade phylogeographical analyses. The COI gene revealed the geographical divergence of major eastern and western clades and historical biogeographical events within each major clade, whereas the nuclear PepCK gene, which did not reveal corresponding east–west clades, indicated past fragmentation and range expansion across wide areas that may have been the result of older biogeographical events. Thus, phylogeographical inferences drawn from analyses of mitochondrial and nuclear genes can reveal different and potentially complementary information about phylogeographical processes.

[1]  M. Hare Prospects for nuclear gene phylogeography , 2001 .

[2]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[3]  K. Crandall,et al.  Evaluation of methods for detecting recombination from DNA sequences: Computer simulations , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[4]  R. Burton INTRASPECIFIC PHYLOGEOGRAPHY ACROSS THE POINT CONCEPTION BIOGEOGRAPHIC BOUNDARY , 1998, Evolution; international journal of organic evolution.

[5]  T. Okazaki,et al.  Genetic Relationships of Japanese and Korean Bagrid Catfishes Inferred from Mitochondrial DNA Analysis , 1999 .

[6]  K. Crandall,et al.  Intraspecific gene genealogies: trees grafting into networks. , 2001, Trends in ecology & evolution.

[7]  Gráinne McGuire,et al.  TOPAL 2.0: improved detection of mosaic sequences within multiple alignments , 2000, Bioinform..

[8]  T. Sota Radiation and reticulation: extensive introgressive hybridization in the carabid beetles Ohomopterus inferred from mitochondrial gene genealogy , 2002, Population Ecology.

[9]  J. Rasplus,et al.  Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri , 2004, Molecular ecology.

[10]  J. Hey,et al.  X chromosome evidence for ancient human histories. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[11]  K. Crandall,et al.  GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes , 2000, Molecular ecology.

[12]  田明义 Illustrated Catalogue of the Genus Carabus of the World (Coleoptera, Carabidae) , 2005 .

[13]  R. Ishikawa,et al.  Phylogeny and life‐history evolution in Carabus (subtribe Carabina: Coleoptera, Carabidae) based on sequences of two nuclear genes , 2004 .

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

[15]  Y. Sohn,et al.  Stratigraphy, petrochemistry and Quaternary depositional record of the Songaksan tuff ring, Jeju Island, Korea , 2003 .

[16]  M. Bagley,et al.  Mitochondrial and nuclear DNA sequence variability among populations of rainbow trout (Oncorhynchus mykiss) , 1998, Molecular ecology.

[17]  A. Brower Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  C. Sing,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. , 1992, Genetics.

[19]  R. Nielsen,et al.  Multilocus Methods for Estimating Population Sizes, Migration Rates and Divergence Time, With Applications to the Divergence of Drosophila pseudoobscura and D. persimilis , 2004, Genetics.

[20]  A. Templeton,et al.  Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. , 1995, Genetics.

[21]  E. Boerwinkle,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. , 1987, Genetics.

[22]  A. Vogler,et al.  Extensive trans‐species mitochondrial polymorphisms in the carabid beetles Carabus subgenus Ohomopterus caused by repeated introgressive hybridization , 2001, Molecular ecology.

[23]  J. Neigel,et al.  Intraspecific Phylogeography: The Mitochondrial DNA Bridge Between Population Genetics and Systematics , 1987 .

[24]  Tadao Matsumoto,et al.  Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp. , 2004, Molecular phylogenetics and evolution.

[25]  R. Harrison,et al.  Nuclear gene genealogies reveal historical, demographic and selective factors associated with speciation in field crickets. , 2003, Genetics.

[26]  Professor Dr. Hans-Ulrich Thiele Carabid Beetles in Their Environments , 1977, Zoophysiology and Ecology.

[27]  A. Templeton,et al.  The role of nuclear genes in intraspecific evolutionary inference: genealogy of the transferrin gene in the brown trout. , 2002, Molecular biology and evolution.

[28]  K. Nagao,et al.  Palaeoclimatic and chronostratigraphic interpretations from strontium, carbon and oxygen isotopic ratios in molluscan fossils of Quaternary Seoguipo and Shinyangri Formations, Cheju Island, Korea , 1999 .

[29]  A. Vogler,et al.  Incongruence of mitochondrial and nuclear gene trees in the Carabid beetles Ohomopterus. , 2001, Systematic biology.

[30]  Y. Takehana,et al.  Geographic Variation and Diversity of the Cytochrome b Gene in Wild Populations of Medaka (Oryzias latipes) from Korea and China , 2004, Zoological science.

[31]  Michael C Whitlock,et al.  The incomplete natural history of mitochondria , 2004, Molecular ecology.

[32]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[33]  Henrik Kaessmann,et al.  DNA sequence variation in a non-coding region of low recombination on the human X chromosome , 1999, Nature Genetics.

[34]  A. Templeton,et al.  Out of Africa again and again , 2002, Nature.

[35]  N. Pierce,et al.  CODIVERSIFICATION IN AN ANT‐PLANT MUTUALISM: STEM TEXTURE AND THE EVOLUTION OF HOST USE IN CREMATOGASTER (FORMICIDAE: MYRMICINAE) INHABITANTS OF MACARANGA (EUPHORBIACEAE) , 2004, Evolution; international journal of organic evolution.

[36]  Y. Takehana,et al.  Genetic Structure of Korean Wild Populations of the Medaka Oryzias latipes Inferred from Allozymic Variation , 2004, Zoological science.

[37]  A. Templeton,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping or DNA sequencing. V. Analysis of case/control sampling designs: Alzheimer's disease and the apoprotein E locus. , 1995, Genetics.

[38]  P. J. Darlington,et al.  Carabidae of Mountains and Islands: Data on the Evolution of Isolated Faunas, and on Atrophy of Wings , 1943 .

[39]  L Lacey Knowles,et al.  Statistical phylogeography. , 2002, Molecular ecology.

[40]  A. Vogler,et al.  Reconstructing species phylogeny of the carabid beetles Ohomopterus using multiple nuclear DNA sequences: heterogeneous information content and the performance of simultaneous analyses. , 2003, Molecular phylogenetics and evolution.

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

[42]  A. Templeton,et al.  The role of molecular genetics in speciation studies. , 1994, EXS.

[43]  A. Templeton Using phylogeographic analyses of gene trees to test species status and processes , 2001, Molecular ecology.

[44]  Y. Imura Classification of the subtribe Carabina (Coleoptera, Carabidae) based on molecular phylogeny , 2002 .

[45]  C. Sing,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. , 1993, Genetics.

[46]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[47]  Alan R Templeton,et al.  Statistical phylogeography: methods of evaluating and minimizing inference errors , 2004, Molecular ecology.

[48]  T. Okazaki,et al.  Genetic Differentiation of Piscivorous Chub (genus Opsariichthys) in Japan, Korea and Russia , 2002, Zoological science.

[49]  Y. Imura,et al.  Molecular Phylogeny and Evolution of Carabid Ground Beetles , 2004, Springer Japan.

[50]  CODIVERSIFICATION IN AN ANT‐PLANT MUTUALISM , 2004 .

[51]  Brian D. Farrell,et al.  Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. , 2001, Molecular phylogenetics and evolution.

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

[53]  Dirk Husmeier,et al.  TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments , 2004, Bioinform..

[54]  H. Sakai,et al.  Speciation and Dispersal of Tribolodon Species (Pisces, Cyprinidae) around the Sea of Japan , 2002, Zoological science.