Multiple origins and the population genetic structure of Rubus takesimensis (Rosaceae) on Ulleung Island: Implications for the genetic consequences of anagenetic speciation


Autoři: JiYoung Yang aff001;  Jae-Hong Pak aff001;  Masayuki Maki aff002;  Seung-Chul Kim aff003
Působiště autorů: Department of Biology, Research Institute for Dok-do and Ulleung-do Island, Kyungpook National University, Daegu, Gyeongsangbuk-do, Korea aff001;  Botanical Gardens, Tohoku University, Sendai, Miyagi, Japan aff002;  Department of Biological Sciences, Sungkyunkwan University, Suwon, Gyeonggi-do, Korea aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222707

Souhrn

To determine the origin and genetic consequences of anagenesis in Rubus takesimensis on Ulleung Island, Korea, we compared the genetic diversity and population structure of R. takesimensis with those of its continental progenitor R. crataegifolius. We broadly sampled a total of 315 accessions in 35 populations and sequenced five noncoding regions of chloroplast DNA. Rubus takesimensis emerged as nonmonophyletic and several geographically diverse continental populations were likely responsible for the origin of R. takesimensis; the majority of R. takesimensis accessions were sisters to the clade containing accessions of R. crataegifolius, primarily from the Korean peninsula, while rare accessions from three populations shared common ancestors with the ones from the southern part of the Korean peninsula, Jeju Island, and Japan. A few accessions from the Chusan population originated independently from the Korean peninsula. Of 129 haplotypes, 81 and 48 were found exclusively in R. crataegifolius and R. takesimensis, respectively. We found unusually high genetic diversity in two regions on Ulleung Island and no geographic population structure. For R. crataegifolius, two major haplotype groups were found; one for the northern mainland Korean peninsula, and the other for the southern Korean peninsula and the Japanese archipelago. Compared with populations of R. crataegifolius sampled from Japan, much higher haplotype diversity was found in populations from the Korean peninsula. The patterns of genetic consequences in R. takesimensis need to be verified for other endemic species based on chloroplast DNA and independent nuclear markers to synthesize emerging patterns of anagenetic speciation on Ulleung Island.

Klíčová slova:

Biology and life sciences – Genetics – Heredity – Genetic mapping – Haplotypes – Population genetics – Phylogeography – Evolutionary biology – Genetic polymorphism – Population biology – Biogeography – Ecology – Ecological metrics – Species diversity – Earth sciences – Geomorphology – Topography – Landforms – Islands – Geography – Ecology and environmental sciences – People and places – Geographical locations – Asia – Japan – Korea


Zdroje

1. Stuessy TF, Jakubowsky G, Gomez RS, Pfosser M, Schluter PM, Fer T, et al. Anagenetic evolution in island plants. J Biogeo. 2006;33: 1259−1265.

2. Stuessy TF. Evolution of specific and genetic diversity during ontogeny of island floras: the importance of understanding process for interpreting island biogeographic patterns. In: Ebach MC, Tangney RS, editors. Biogeography in a changing world. Boca Raton: CRC Press; 2007. pp. 117−133.

3. Stuessy TF, Takayama K, López-Sepúlveda P, Crawford DJ. Interpretation of patterns of genetic variation in endemic plant species of oceanic islands. Bot J Linn Soc. 2014;174: 276−288. doi: 10.1111/boj.12088 26074627

4. Eliasson U. Studies in Galapagos Plants. XIV. The genus Scalesia Arn. Opera Botanica. 1974;36: 1−117.

5. Schilling EE, Panero JL, Eliasson UH. Evidence from chloroplast DNA restriction site analysis on the relationships of Scalesia (Asteraceae: Heliantheae). Am J Bot. 1994;81: 248−254.

6. Wagner WL, Herbst DR, Sohmer SH. Manual of the flowering plants of Hawaii, vol. 1. 2nd ed. Honolulu: University of Hawaii and Bishop Museum Press; 1999.

7. Nielsen LR. Molecular differentiation within and among island populations of the endemic plant Scalesia affinis (Asteraceae) from the Galapagos Islands. Heredity. 2004;93: 434−442. doi: 10.1038/sj.hdy.6800520 15280895

8. Böhle UR, Hilger HH, Martin WF. Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc Natl Acad Sci USA. 1996;93: 11740−11745. doi: 10.1073/pnas.93.21.11740 8876207

9. Kim S-C, Crawford DJ, Francisco-Ortega J, Santos-Guerra A. A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proc Natl Acad Sci USA. 1996;93: 7743−7748. doi: 10.1073/pnas.93.15.7743 8755546

10. Kim S-C, Crawford DJ, Jansen RK. Phylogenetic relationships among the genera of subtribe Sonchinae (Asteraceae): Evidence from ITS sequences. Syst Bot. 1996;221: 417−432.

11. Jorgensne TH, Olesen JM. Adaptive radiation of island plants: evidence from Aeonium (Crassulaceae) of the Canary Islands. Persepct Plant Evol. 2001;4: 29−42.

12. Mort ME, Soltis DE, Soltis PS, Francisco-Ortega J, Santos-Guerra A. Phylogenetic and evolution of the Macaronesian clade of Crassulaceae inferred from nuclear and chloroplast sequence data. Syst Bot. 2002;27: 271−288.

13. Kim S-C, McGowen MR, Lubinsky P, Barber JC, Mort ME, Santos-Guerra A. Timing and tempo of early and successive adaptive radiations in Macaronesia. PLoS ONE. 2008;3: 32139.

14. Sang T, Crawford DJ, Kim S-C, Stuessy TF. Radiation of the endemic genus Dendroseris (Asteraceae) in the Juan Fernandez Islands: evidence from sequences of the ITS regions of nuclear ribosomal DNA. Am J Bot. 1994;81: 1494−1501.

15. Sang T, Crawford DJ, Stuessy TF, Silva M. ITS sequences and the phylogeny of the genus Robinsonia (Asteraceae). Syst Bot. 1995;20: 55−64.

16. López-Sepúlveda P, Takayama K, Greimler J, Crawford DJ, Peñailillo P, Baeza M, et al. Speciation and biogeography of Erigeron (Asteraceae) in the Juan Fernández Archipelago, Chile, based on AFLPs and SSRs. Syst Bot. 2015;40: 888−899.

17. Takayama K., Lopez-sequlveda P, Greimler J, Crawford DJ, Penailillo P, Baeza M, et al. Relationships and genetic consequences of contrasting modes of speciation among endemic species of Robinsonia (Asteraceae, Senecioneae) of the Juan Fernandez Archipelago, Chile, based on AFLPS and SSRs. New Phytol. 2015;205: 415−428. doi: 10.1111/nph.13000 25209139

18. Ito M, Ono M. Allozyme diversity and the evolution of Crepidiastrum (Composiate) on the Bonin (Ogasawara) Islands. Bot Mag (Tokyo). 1990;103: 449−459.

19. Setoguchi H, Watanabe I. Intersecional gene flow between insular endemics of Ilex (Aquifoliaceae) on the Bonin Islands and the Ryukyu Islands. Am J Bot. 2000;87: 793−810. 10860910

20. López-Sepúlveda P, Takayama K, Greimler J, Peñailillo P, Crawford DJ, Baeza M, et al. Genetic variation (AFLPs and nuclear microsatellites) in two anagenetically derived endemic species of Myrceugenia (Myrtaceae) on the Juan Fernández Islands, Chile. Am J Bot. 2013;100: 722−734. doi: 10.3732/ajb.1200541 23510759

21. López-Sepúlveda P, Takayama K, Greimler J, Crawford DJ, Peñailillo P, Baeza M, et al. Progressive migration and anagenesis in Drimys confertifolia of the Juan Fernández Archipelago, Chile. J Plant Res. 2015;128: 73−90. doi: 10.1007/s10265-014-0666-7 25292282

22. López-Sepúlveda P, Takayama K, Crawford DJ, Greimler J, Peñailillo P, Baeza M, et al. Biogeography and genetic consequences of anagenetic speciation of Rhaphithamnus venustus (Verbenaceae) in the Jun Fernández Archipelago, Chile: insight from AFPL and SSR markers. Plant Spec Biol. 2017;32: 223−237.

23. Pfosser M, Jakubowsky G, Schlüter PM, Fer T, Kato H, Stuessy TF, et al. Evolution of Dystaenia takesimana (Apiaceae), endemic to Ullung Island, Korea. Plant Syst Evol. 2006;256: 159−170.

24. Takyama K, Sun B-Y, Stuessy TF. Genetic consequences of anagenetic speciation in Acer okamotoanum (Sapindaceae) on Ulleung Island, Korea. Ann Bot. 2012;109: 321−330. doi: 10.1093/aob/mcr280 22056411

25. Takyama K, Sun B-Y, Stuessy TF. Anagenetic speciation in Ullung Island, Korea: genetic diversity and structure in the island endemic species, Acer takesimense (Sapindaceae). J Plant Res. 2013;126: 323−333. doi: 10.1007/s10265-012-0529-z 23090156

26. Takayama K, Sun B-Y, Stuessy TF. Genetic consequences of anagenetic speciation in endemic angiosperms of Ullung Island. J Jpn Bot Suppl. 2016;91: 83−98.

27. Kim YK. Petrology of Ulreung volcanic island, Korea–part 1. Geology. J Japanese Assoc Mineral Petrol Econ Geol. 1985;80: 128−135.

28. Thompson MM. Chromosome numbers of Rubus species at the national clonal germplasm repository. HortScience. 1995;30: 1447−1452.

29. Alice LA, Campbell CS. Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Am J Bot. 1999;86: 81−97. 21680348

30. Naruhashi N. Morphology of 34 Japanese Rubus species. Acta Hortic. 1980;112:177−181.

31. Suzuki W. Comparative ecology of Rubus Species (Rosaceae) II. Reproductive characteristics of three Rubus species, R. palmatus var. coptophyllus, R. microphyllus and R. crataegifolius. Pl Spec Biol. 1990;5: 263−275.

32. Weber HE. Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobot Phytotax. 1996;31: 373−380.

33. Yang JY, Pak JH. Phylogeney of Korean Rubus (Rosaceae) based on ITS (nrDNA) and trnL/F intergenic region (cpDNA). J Plant Biol. 2006;49: 44−54.

34. Yang JY, Yoon HS, Pak JH. Phylogeny of Korean Rubus (Rosaceae) based on the second intron of the LEAFY gene. Can J Plant Sci. 2012;92: 461−472.

35. Nakai T. Notulae ad plants Japoniae et Koreae XVII. Bot Mag (Tokyo). 1918; 32: 104−105.

36. Lee W, Yang JY, Jung K-S, Pak J-H, Maki M, Kim S-C. Chloroplast DNA assessment of anagenetic speciation in Rubus takesimensis (Rosaceae) on Ulleung Island, Korea. J Plant Biol. 2017;60: 163−174.

37. Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol Biol. 1991;17: 1105−1109. doi: 10.1007/bf00037152 1932684

38. Shaw J, Lickey EB, Schilling EE, Small RL. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am J Bot. 2007;94: 275−288. doi: 10.3732/ajb.94.3.275 21636401

39. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. "ClustalW and ClustalX version 2". Bioinformatics. 2007;23: 2947–2948. doi: 10.1093/bioinformatics/btm404 17846036

40. Maddison WP, Maddison DR. MacClade version 3.04 Analysis of phylogeny and character evolution. Massachusetts: Sinauer Associates; 1992.

41. Swofford DL. PAUP*: Phylogenetic analysis using parsimony (and other method). Version 4.0b10. Massachusetts: Sinauer Associates; 2002.

42. Nguyen L-T, Schmidt H-A, Haeseler Av, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol Biol Evol. 2015;32: 268−274. doi: 10.1093/molbev/msu300 25371430

43. Simmon MP, Ochoterena H. Gaps as characters in sequence based phylogenetic analyses. Syst Biol. 2000;49: 369−381. 12118412

44. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39: 783−791. doi: 10.1111/j.1558-5646.1985.tb00420.x 28561359

45. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10: 564−567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

46. Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9: 1657−1659. 11050560

47. Hart MW, Sunday J. Things fall apart: biological species form unconnected parsimony networks. Biol Lett. 2007;3: 509−512. doi: 10.1098/rsbl.2007.0307 17650475

48. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25: 1451−1452. doi: 10.1093/bioinformatics/btp187 19346325

49. Schneider S, Excoffier L. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 1999;152: 1079−1089. 10388826

50. Harpending HC. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol. 1994;66: 591−600. 8088750

51. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123: 585−595. 2513255

52. Fu XY, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993;133: 693−709. 8454210

53. Fu XY. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147: 915−925. 9335623

54. Pons O, Petit R. Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics. 1996;144: 1237−1245. 8913764

55. Pfosser M, Guzy-Wróbelska J, Sun BY, Stuessy TF, Sugawara T, Fujii N. The origin of species of Acer (Sapindaceae) endemic to Ullung Island, Korea. Syst Bot. 2002;27: 351−367.

56. Kim P. (Lee BG; translator). The History of the Three Kingdoms (Samguk Sagi). Seoul: Withersbook; 2015.

57. Kim P. (Shultz EJ, Kang HHW; translator). The Silla Annals of the Samguk Sagi. Seoul: Academy of Korean Studies Press; 2012.

58. Han J-S. A study on the local government system in the middle period of Silla dynasty focused on ancient tomb in Ulleungdo. A Collection of Treatises of Korean Studies. 2014; 41: 131–167.

59. Barker NP, Howis S, Nordenstam B, Källersjö M, Eldenäs P, Griffioen C, et al. Nuclear and chloroplast DNA-based phylogenies of Chrysanthemoides Tourn. ex Medik. (Calenduleae; Asteraceae) reveal extensive incongruence and generic paraphyly, but support the recognition of infraspecific taxa in C. monilifera. S Afr J Bot. 2009;75: 560−572.

60. Manos PS, Zhou ZK, Cannon CH. Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. Int J. Plant Sci. 2001;162: 1361−1379.

61. Denk T, Grimm GW. The oaks of western Eurasia: traditional classifications and evidence from two nuclear markers. Taxon. 2010;59: 351−366.

62. Simeone MC, Piredda R, Papini A, Vessella F, Schirone B. Application of plastid and nuclear markers to DNA barcoding of Euro-Mediterranean oaks (Quercus, Fagaceae): problems, prospects and phylogenetic implications. Bot J Linn Soc.2013;172: 478−499.

63. Takayama K, López-Sepúlveda P, Greimler J, Crawford DJ, Peñailillo P, Baeza M, et al. Genetic consequences of cladogenetic vs. anagenetic speciation in endemic plants on oceanic islands. AoB Plants. 2015;7: plv102.

64. Oh S-H. Sea, wind, or bird: origin of Fagus multinervis (Fagaceae) inferred from chloroplast DNA sequences. Korean J Pl Taxon. 2015;45: 213−220.

65. Lee W, Pak JH. Intraspecific sequence variation of trnL/F intergenic region (cpDNA) in Sedum takesimense Nakai (Crassulaceae) and aspects of geographic distribution. Korean J Pl Taxon. 2010;40: 157−162.

66. Sochor M, Vasut RJ, Sharbel TF, Travnicek B. How just a few makes a lot: Speciation via reticulation and apomixes on example of European brambles (Rubus subgen. Rubus, Rosaceae). Mol Phylogenet Evol. 2015;899: 13−27.

67. Asker SE, Jerling L. Apomixis in Plants. London: CRC press; 1992.

68. Birky CW Jr. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics. 1996;144: 427−237. 8878706

69. Horandle E, Paun O. Patterns and sources of genetic diversity in apomictic plants: implications for evolutionary potentials. In: Horandl E, Grossniklaus U, van Dijk PJ, Sharbel TF, editors. Apomixis: evolution, mechanisms and perspectives. Rugell: A.R.G. Gantner Verlag; 2007. pp. 169−174.

70. Majesky L, Vasut RJ, Kitner M, Schranz ME, Koch M, Kiefer C, et al. The pattern of genetic variability in apomictic clones of Taraxacum officinale indicates the alternation of asexual and sexual histories of apomicts. PLoS ONE. 2012;7: e41868. doi: 10.1371/journal.pone.0041868 22870257

71. Majesky L, Vasut RJ, Kitner M. Genotypic diversity of apomictic microspecies of the Taraxacum scanicum group (Taraxacum sect. Erythrosperma). Plant Syst Evol. 2015;301: 2105−2124.

72. Sochor M, Travnicek B. Melting pot of biodiversity: first insights into the evolutionary patterns of the Colchic bramble flora (Rubus subgenus Rubus, Rosaceae). Bot J Linn Soc. 2016;181: 610−620.

73. Rogstad SH, Nybom H, Schaal BA. The tetrapod ‘DNA fingerprinting’ M13 repeat probe reveals genetic diversity and clonal growth in quaking aspen (Populus tremuloides, Salicaceae). Plant Syst Evol. 1991;175: 115−123.

74. Sarhanova P, Sharbel TF, Sochor M, Vasut RJ, Dancak M, Travnicek B. Hybridization drives evolution of apomicts in Rubus subgenus Rubus: evidence from microsatellite markers. Ann Bot. 2017;120: 317−328. doi: 10.1093/aob/mcx033 28402390

75. Herrera CM. A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr. 1984;54: 1–23.

76. Snow B, Snow D. Birds and berries: A study of an ecological interaction. London: T&AD Poyser Ltd; 1988. pp. 60−63.

77. Murray KG, Winnett-Murray K, Cromie EA, Minor M, Meyers E. The influence of seed packaging and fruit color on feeding preferences of American robins. Vegetatio. 1993;107/108: 217–226.

78. Levey DJ. Methods of seed processing by birds and seed deposition patterns. In: Estrada A, Fleming TH, editors. Frugivores and seed dispersal, Dordrecht: Junk; 1986. pp. 147–158.

79. Kollmann J, Steinger T, Ray BA. Evidence of sexuality in European Rubus (Rosaceae) species based on AFLP and allozyme analysis. Am J Bot. 2000;87: 1592−1598. 11080109

80. Jordano P. Migrant birds are the main seed dispersers of blackberries in southern Spain. Oikos. 1982;38: 183–193.

81. Rejmanek M. Invasion of Rubus praecox (Rosaceae) is promoted by the native tree Aristotelia chilensis (Elaeocarpaceae) due to seed dispersal facilitation. Gayana Bot. 2015;72: 27–33.

82. Cha JS, Kim KA, Kim HJ, Park HC. The Avifauna in Ulleungdo. J Korean Nat. 2010;3: 151−157.

83. Yu J-P, Jin S-D, Kim W-B, Kang J-H, Kim I-K, Kang T-H, et al. Characteristics of birds community in Ulleung Island, Korea. J Asia Pac Biodivers. 2013;6: 175−187.

84. Hamrick JL, Godt MJW. Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS, editors. Plant population genetics, breeding and genetic resources. Massachusetts: Sinauer Associates; 1989. pp. 43−63.

85. Hamrick JL, Godt MJW. Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc. 1996;351: 1291−1298.

86. Antonius K, Nybom H. DNA Fingerprinting reveals significant amounts of genetic variation in a wild raspberry Rubus idaeus population. Mol Ecol. 1994;3: 177−180.

87. Qi XS, Chen C, Comes HP, Sakaguchi S, Liu YH, Tanaka N, et et al. Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphylluum (Cercidiphyllaceae). New Phytol. 2012;196: 617−630. doi: 10.1111/j.1469-8137.2012.04242.x 22845876

88. Sakaguchi S, Qiu YX, Liu YH, Qi XS, Kim SH, Han J, et al. Climate oscillation during the Quaternary associated with landscape heterogeneity prompted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Mol Ecol. 2012;21: 3823−3838. doi: 10.1111/j.1365-294X.2012.05652.x 22646502

89. Lee JH, Lee DH, Choi BH. Phylogeography and genetic diversity of East Asian Neolisttea sericea (Lauraceae) based on variations in chloroplast DNA sequences. J Plant Res. 2013;126: 193−202. doi: 10.1007/s10265-012-0519-1 22990429

90. Li EX, Yi S, Qiu YX, Guo JT, Comes HP, Fu CX. Phylogeography of two East Asian species in Croomia (Stemonaceae) inferred from chloroplast DNA and ISSR fingerprinting variation. Mol Phylogenet Evol. 2008;49: 702−714. doi: 10.1016/j.ympev.2008.09.012 18849001

91. Qiu YX, Sun Y, Zhang XP, Lee J, Fu CX, Comes HP. Molecular phylogeography of East Asian Kirengeshoma (Hydrangeaceae) in relation to Quaternary climate change and landbridge configurations. New Phytol. 2009;183: 480−495. doi: 10.1111/j.1469-8137.2009.02876.x 19496955

92. Qi XS, Yuan N, Comes HP, Sakaguchi S, Qiu YX. A strong ‘filter’ effect of the East China Sea land bridge for East Asia’s temperate plant species: inferences from molecular phylogeography and ecological niche modeling of Platycrater arguta (Hydrangeaceae). BMC Evol Biol. 2014;14: 41. doi: 10.1186/1471-2148-14-41 24593236

93. Wang JF, Gong X, Chiang YC, Kuroda C. Phylogenetic patterns and disjunct distribution in Ligularia hodgsonii Hook. (Asteraceae). J Biogeogr. 2013;40: 1741−1754.

94. Crawford DJ, Stuessy TF. Cryptic variation, molecular data, and the challenge of conserving plant diversity in oceanic archipelagos: the critical role of plant systematics. Korean J Pl Taxon. 2016;46: 129−148.


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden