Abstract
This study aimed to reveal the evolutionary timescale and processes underlying the diversity of Rubus in the Japanese Archipelago. We conducted molecular phylogenetic analyses of most native species (35 species), along with previously published data from 116 foreign species, based on nuclear ribosomal internal transcribed spacer (ITS) and chloroplast DNA sequences. Most of the northern species of Japan, that is, Rubus chamaemorus, R. pedatus, R. vernus, R. pseudojaponicus, and R. ikenoensis, were found to belong to anciently diverged lineages; in particular, R. ikenoensis formed a unique lineage distinct from other species. The other species diverged into two evolutionary groups. One included subg. Malachobatus, Chamaebatus, and sects. Pungentes, Idaeanthi, and Parvifolii (subg. Idaeobatus), which was further divided into two clades in the chloroplast phylogenies. Although the phylogenetic structures within this group were unresolved, R. sieboldii has been proven to be recently derived. The second group represented a well-supported clade, comprising sects. Microphylli, Corchorifolii, Peltati, and Rosifolii (subg. Idaeobatus) and suggested early Miocene diversification of this Asian lineage associated with character specialization in vegetative reproduction and leaf shape. This clade was further resolved into lower clades primarily representing the sectional classifications, although the placement of the earliest diverged species, R. sumatranus, R. peltatus, R. corchorifolius, and R. chingii, was incongruent among gene trees. At the lower taxonomic levels, R. illecebrosus, R. grayanus, and the thornless species of sect. Microphylli showed earlier divergence.
Similar content being viewed by others
References
Alice LA, Campbell CS (1999) Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Amer J Bot 86:81–97. https://doi.org/10.2307/2656957
Alice L, Eriksson T, Eriksen B, Christopher S (2001) Hybridization and gene flow between distantly related species of Rubus (Rosaceae): evidence from nuclear ribosomal DNA internal transcribed spacer region sequences. Syst Bot 26:769–778. https://doi.org/10.1043/0363-6445-26.4.769
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x
Bozukov V, Palmarev E, Petkova A (2008) The fossil macroflora of the Vulche Pole Molasse formation (SE Bulgaria). Phytol Balc 14:173–184
Carter KA, Liston A, Bassil NV, Alice LA, Bushakra JM, Sutherland BL, Mockler TC, Bryant DW, Hummer KE (2019) Target capture sequencing unravels Rubus evolution. Frontiers Pl Sci 10:1–18. https://doi.org/10.3389/fpls.2019.01615
DeVore ML, Pigg KB (2007) A brief review of the fossil history of the family Rosaceae with a focus on the Eocene Okanogan Highlands of eastern Washington State, USA, and British Columbia, Canada. Pl Syst Evol 266:45–57. https://doi.org/10.1007/s00606-007-0540-3
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Edler D, Klein J, Antonelli A, Silvestro D (2021) raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Meth Ecol Evol 12:373–377. https://doi.org/10.1111/2041-210X.13512
Eriksson T, Donoghue MJ, Hibbs MS (1998) Phylogenetic analysis of Potentilla using DNA sequences of nuclear ribosomal internal transcribed spacers (ITS), and implications for the classification of Rosoideae (Rosaceae). Pl Syst Evol 211:155–179. https://doi.org/10.1007/BF00985357
Eriksson T, Hibbs MMS, Yoder ADA, Delwiche CFC, Donoghue MMJ (2003) Phylogeny of Rosoideae (Rosaceae) based on sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA and the trnL/F region of chloroplast DNA. Int J Pl Sci 164:197–211. https://doi.org/10.1086/346163
Eriksson O, Bremer B (1993) Genet Dynamics of the clonal plant Rubus saxatilis. J Ecol 81:533–542. https://doi.org/10.2307/2261531
Focke WO (1910) Species Ruborum. Monographiae generis Rubi podromus. Pars I. Biblioth Bot 17:1–120
Focke WO (1911) Species Ruborum. Monographiae generis Rubi prodromus. Pars II. Biblioth Bot 17:121–223
Focke WO (1914) Species Ruborum. Monographiae generis Rubi prodromus. Pars III. Biblioth Bot 17:121–223
Gouy M, Guindon S, Gascuel O (2010) Sea view version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molec Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Hotta M (1974) History and geography of plants: evolutionary biology in plants III. Sanseido, Tokyo (in Japanese)
Howarth DG, Gardner DE, Morden CW (1997) Phylogeny of Rubus subgenus Idaeobatus (Rosaceae) and its implications toward colonization of the Hawaiian islands. Syst Bot 22:433–441. https://doi.org/10.2307/2419819
Huang YJ, Jacques FMB, Liu YSC, Su T, Ferguson DK, Xing YW, Zhou ZK (2015) Rubus (Rosaceae) diversity in the late Pliocene of Yunnan, southwestern China. Geobios 48:439–448. https://doi.org/10.1016/j.geobios.2015.08.001
Hummer KE (2019) Rubus diversity. HortScience 31:182–183. https://doi.org/10.21273/hortsci.31.2.182
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molec Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Iwatsubo Y, Naruhashi N (1991) Karyomorphological and cytogenetical studies of Rubus parvifolius, R. coreanus and R. × hiraseanus (Rosaceae). Cytologia 56:151–156. https://doi.org/10.1508/cytologia.56.151
Iwatsubo Y, Naruhashi N (1993) Cytogenetical study of Rubus × tawadanus (Rosaceae). Cytologia 58:217–221
Iwatsubo Y, Aoki M, Mishima M, Naruhashi N (1996) Cytogenetic relationship between Rubus croceacanthus and R. minusculus (Rosaceae). Cytologia 61:163–167. https://doi.org/10.1508/cytologia.61.163
Jinno T (1958) Cytogenetic and cytoecological studies on some Japanese species of Rubus I. Chromosomes. Bot Mag (Tokyo) 71:15–23. https://doi.org/10.1266/jjg.33.201
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lu LD (1983) A study on the genus Rubus of China. Acta Phytotax Sin 21:13–25 (in Chinese)
Lu LD (1985) Rubus. In: Yü DJ, Lu LT, Gu CZ, Guan KJ, Li CL (eds) Flora Reipublicae Popularis Sinicae, vol 37. Science Press, Beijing, pp 10–218 (in Chinese)
Lu LD, Boufford DE (2003) Rubus Linnaeus. In: Wu ZY, Raven PH (eds) Flora of China 9. Science Press, Beijing, pp 195–285
Maruyama S, Isozaki Y, Kimura G, Terabayashi M (1997) Paleogeographic maps of the Japanese islands: plate tectonic synthesis from 750 Ma to the present. Island Arc 6:121–142
Michael K (2006) Clarification of basal relationships in Rubus (Rosaceae) and the origin of Rubus chamaemorus. Masters Theses & Specialist Projects. Paper 250. Available at: https://digitalcommons.wku.edu/theses/250
Mimura M, Mishima M, Lascoux M, Yahara T (2014) Range shift and introgression of the rear and leading populations in two ecologically distinct Rubus species. BMC Evol Biol 14:209. https://doi.org/10.1186/s12862-014-0209-9
Miyashita T, Kunitake H, Yotsukura N, Hoshino Y (2015) Assessment of genetic relationships among cultivated and wild Rubus accessions using AFLP markers. Sci Hort 193:165–173. https://doi.org/10.1016/j.scienta.2015.07.004
Morden CW, Gardner DE, Weniger DA (2003) Phylogeny and biogeography of pacific Rubus subgenus Idaeobatus (Rosaceae) species: investigating the origin of the endemic Hawaiian raspberry R. macraei. Pacific Sci 57:181–197. https://doi.org/10.1353/psc.2003.0018
Naruhashi N (1968) Notes on Japanese Rubus 1. Acta Phytotax Geobot 23:25–27 (in Japanese)
Naruhashi N (1971) Notes on Japanese Rubus 2. Acta Phytotax Geobot 25:4–9 (in Japanese)
Naruhashi N (2001) Rubus L. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan IIb, angiospermae dicotyledoneae archichlamydeae (b). Kodansha, Tokyo
Naruhashi N (2010) Taxonomical notes on Asiatic Rubus (Rosaceae) (5) Rubus yoshinoi and R. kulinganus. J Phytogeogr Taxon 58:43–46
Naruhashi N, Satomi N (1972) The distribution of Rubus in Japan. I. Distribution maps. Annual Rep Bot Gard Fac Sci Kanazawa Univ 6:1–12
Nesme X (1985) Respective effects of endocarp, testa and endosperm, and embryo on the germination of raspberry (Rubus idaeus L.) seeds. Canad J Pl Sci 65:125–130. https://doi.org/10.4141/cjps85-017
Okada A, Kikuchi S, Hoshino Y, Kunitake H, Mimura M (2020) Phylogeny and trait variation of Japanese Rubus subgenus Ideaobatus. Sci Hort 264:109150. https://doi.org/10.1016/j.scienta.2019.109150
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Pavlyutkin BI, Chekryzhov IY, Petrenko TI (2011) The Voznovo formation: the reflection of the early Oligocene stage in the geological history of East Sikhote-Alin. Russ J Pacific Geo 5:47–63. https://doi.org/10.1134/S1819714011010052
Posada D (2008) jModelTest: phylogenetic model averaging. Molec Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
R Core Team (2020) R: a language and environment for statistical computing (Version 4.0. 0). R Foundation for Statistical Computing, Vienna. Available at: https://www.R-project.org/
Revell LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Meth Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Ryynänen A (1972) Arctic bramble (Rubus arcticus L.), a new cultivated plant. Ann Agric Fenn 11:170–173
Šarhanová P, Sharbel TF, Sochor M, Vašut RJ, Dančák M, Trávníček B (2017) Hybridization drives evolution of apomicts in Rubus subgenus Rubus: evidence from microsatellite markers. Ann Bot (Oxford) 120:317–328. https://doi.org/10.1093/aob/mcx033
Sochor M, Vašut RJ, Sharbel TF, Trávníček B (2015) How just a few makes a lot: speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Molec Phylogen Evol 89:13–27. https://doi.org/10.1016/j.ympev.2015.04.007
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Suzuki W (1987) Comparative ecology of Rubus species (Rosaceae) I. Ecological distribution and life history characteristics of three species, R. palmatus var. coptophyllus, R. microphyllus and R. crataegifolius. Pl Spec Biol 2:85–100
Suzuki W (1990) 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 5:263–275
Suzuki W (1997) Germination responses of Rubus palmatus var. coptophyllus and Rubus parvifolius seeds with different burial durations to a variable light and temperature regime. Ecol Res 12:167–174. https://doi.org/10.1007/BF02523782
Tang CQ, Matsui T, Ohashi H, Dong YF, Momohara A, Herrando-Moraira S, Qian S, Yang Y, Ohsawa M, Luu HT, Grote PJ, Krestov PV, Ben LePage Werger M, Robertson K, Hobohm C, Wang CY, Peng MC, Chen X, Wang HC, Su WH, Zhou R, Li S, He LY, Yan K, Zhu MY, Hu J, Yang RH, Li WJ, Tomita M, Wu ZL, Yan HZ, Zhang GF, He H, Yi SR, Gong H, Song K, Song D, Li XS, Zhang ZY, Han P, Bin Shen LQ, Huang DS, Luo K, López-Pujol J (2018) Identifying long-term stable refugia for relict plant species in East Asia. Nat Commun 9:1–14. https://doi.org/10.1038/s41467-018-06837-3
Wang Y, Chen Q, Chen T, Tang H, Liu L, Wang X (2016) Phylogenetic insights into Chinese Rubus (Rosaceae) from multiple chloroplast and nuclear DNAs. Frontiers Pl Sci 7:1–13. https://doi.org/10.3389/fpls.2016.00968
Wen J, Nie ZL, Ickert-Bond SM (2016) Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. J Syst Evol 54:469–490. https://doi.org/10.1111/jse.12222
Yang J, Yoon HS, Pak JH (2012) Phylogeny of Korean Rubus (Rosaceae) based on the second intron of the LEAFY gene. Canad J Pl Sci 92:461–472. https://doi.org/10.4141/cjps2011-180
Zhang SD, Jin JJ, Chen SY, Chase MW, Soltis DE, Li HT, Yang JB, Li DZ, Yi TS (2017) Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytol 214:1355–1367. https://doi.org/10.1111/nph.14461
Acknowledgements
We are grateful to Dr. Goro Kokubugata, Dr. Nobuyuki Tanaka, Mitsuru Ayabe, and Takahito Ideno for their help with the collection of leaf samples from botanical gardens, and to Dr. Hisato Kunitake, Dr. Yoichiro Hoshino, Michiharu Kato, and Dr. Shuri Kato for providing samples for this study. We also thank Ayana Okada and Akiko Hisamatsu for their support and contribution to the laboratory work. Dr. Hiroshi Yoshimaru, Kensuke Yoshimura, Yasuko Kawamata, and Chisako Furusawa are gratefully acknowledged for providing DNA samples and sequence data from the DNA-barcoding project. Our colleague, Dr. James Worth, kindly provided valuable comments that greatly improved the manuscript. We would like to thank Editage (www.editage.com) for English language editing.
Funding
This study received financial support from the Japanese Society for the Promotion of Science (JSPS KAKENHI Grant Numbers 20248017, 25292098, and 17K07571).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they do have no conflict of interest.
Additional information
Handling editor: Yunpeng Zhao.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. List of samples.
Online Resource 2. Primers used in this study.
Online Resource 3. List of data from published studies.
Online Resource 4. Best-fit models of substitution.
Online Resource 5. ITS phylogenies based on BI and ML methods.
Online Resource 6. Chloroplast phylogenies based on BI and ML methods.
Online Resource 7. Partial chloroplast phylogenies based on BI and ML methods.
Online Resource 8. Marginal likelihood estimates of each molecular clock model.
Online Resource 9. The results of ancestral trait reconstruction.
Rights and permissions
About this article
Cite this article
Kikuchi, S., Mimura, M., Naruhashi, N. et al. Phylogenetic inferences using nuclear ribosomal ITS and chloroplast sequences provide insights into the biogeographic origins, diversification timescales and trait evolution of Rubus in the Japanese Archipelago. Plant Syst Evol 308, 20 (2022). https://doi.org/10.1007/s00606-022-01810-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-022-01810-6