Abstract
Although the genetic structures of populations in several model organisms have been studied even at the genomic level, quite a few ecologically important or evolutionary interesting species, such as endemic species on oceanic islands, exist whose genetic variations have not yet been studied. Genetic studies of those species may add new insights to our knowledge of evolution, especially when accompanied with ecological and geological knowledge of the species. In this study, we analyzed the genetic variation of two related species of Hamamelidaceae, Distylium racemosum and Distylium lepidotum, living in different habitats and possessing distinctive morphological characteristics. Distylium racemosum is one of the dominant trees of broad-leaved evergreen forests in Japan, and D. lepidotum is a dominant shrub in dry scrub endemic to the Ogasawara Islands. We analyzed the nucleotide variation at 112 protein-coding loci in 95 samples for the two Distylium species and inferred population structure and demographic history on the basis of these data. Our results showed that the samples from two Distylium species were genetically clustered into the following three groups: D. racemosum, D. lepidotum in the Chichijima Island, and D. lepidotum in the Hahajima Island. Furthermore, D. racemosum appears to have diverged first approximately 10 million years ago (MYA), and, then, the split of two populations of D. lepidotum occurred around 1 MYA. Additionally, we detected a few candidate loci that may contribute to adaptation of the species or local populations by exploring the pattern of the variation within and between species using the FST-outlier approach.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abe T (2006) Threatened pollination systems in native flora of the Ogasawara (Bonin) islands. Ann Bot 98:317–334. https://doi.org/10.1093/aob/mcl117
Aoki K, Ueno S, Kamijo T, Setoguchi H, Murakami N, Kato M, Yd T (2014) Genetic differentiation and genetic diversity of Castanopsis (Fagaceae), the dominant tree species in Japanese broadleaved evergreen forests, revealed by analysis of EST-associated microsatellites. PLoS One 9:e87429. https://doi.org/10.1371/journal.pone.0087429
Bogle AL, Philbrich CT (1980) A generic atlas of Hamamelidaceous pollens. Contrib Gray Herb Harvard Univ 210:29–103
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Bybee SM, Bracken-Grissom H, Haynes BD et al (2011) Targeted amplicon sequencing (TAS): a scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biol Evol 3:1312–1323. https://doi.org/10.1093/gbe/evr106
Bürstenbinder K, Möller B, Plötner R, Stamm G, Hause G, Mitra D, Abel S (2017) The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol 173:1692–1708. https://doi.org/10.1104/pp.16.01743
Chiang Y-C, Hung K-H, Schaal BA et al (2006) Contrasting phylogeographical patterns between mainland and island taxa of the Pinus luchuensis complex. Mol Ecol 15:765–779. https://doi.org/10.1111/j.1365-294X.2005.02833.x
Crawford DJ, Stuessy TF, Haines DW et al (1992) Allozyme diversity within and divergence among four species of Robinsonia (asteraceae: Senecioneae), a genus endemic to the Juan Fernandez Islands, Chile. Am J Bot 79:962–966. https://doi.org/10.1002/j.1537-2197.1992.tb13680.x
Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
DeJoode DR, Wendel JF (1992) Genetic diversity and origin of the Hawaiian Islands cotton, Gossypium tomentosum. Am J Bot 79:1311–1319. https://doi.org/10.2307/2445059
De La Torre AR, Li Z, Van de Peer Y, Ingvarsson PK (2017) Contrasting rates of molecular evolution and patterns of selection among gymnosperms and flowering plants. Mol Biol Evol 34:1363–1377. https://doi.org/10.1093/molbev/msx069
Duminil J, Fineschi S, Hampe A et al (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672. https://doi.org/10.1086/513490
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Elisens WJ (1992) Genetic divergence in Galvezia (Scrophulariaceae): evolutionary and biogeographic relationships among South American and Galápagos species. Am J Bot 79:198–206. https://doi.org/10.1002/j.1537-2197.1992.tb13638.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9:e1003905. https://doi.org/10.1371/journal.pgen.1003905
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant Mmarkers: a Bayesian perspective. Genetics 180:977–993. https://doi.org/10.1534/genetics.108.092221
Francisco-Ortega J, Santos-Guerra A, Kim S-C, Crawford DJ (2000) Plant genetic diversity in the Canary Islands: a conservation perspective. Am J Bot 87:909–919. https://doi.org/10.2307/2656988
Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327. https://doi.org/10.1038/hdy.1997.46
García-Verdugo C, Sajeva M, Mantia TL et al (2015) Do island plant populations really have lower genetic variation than mainland populations? Effects of selection and distribution range on genetic diversity estimates. Mol Ecol 24:726–741. https://doi.org/10.1111/mec.13060
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond Ser B Biol Sci 351:1291–1298. https://doi.org/10.1098/rstb.1996.0112
Hudson RR (2002) Generating samples under a Wright–Fisher neutral model of genetic variation. Bioinformatics 18:337–338. https://doi.org/10.1093/bioinformatics/18.2.337
Ito M (1998) Origin and evolution of endemic plants of the Bonin (Ogasawara) Islands. Res Popul Ecol 40:205–212. https://doi.org/10.1007/BF02763405
Ito M, Soejima A, Ono M (1998) Genetic diversity of the endemic plants of the Bonin (Ogasawara) Islands. In: Stuessy TF, Ono M (eds) Evolution and speciation of island plants. Cambridge University Press, Cambridge, pp 141–154
Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925. https://doi.org/10.1104/pp.103.031237
Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893–903
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A, Fennell T et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu L, Li C, Liang Z, Yu H (2018a) Characterization of multiple C2 domain and transmembrane region proteins in Arabidopsis. Plant Physiol 176:2119–2132. https://doi.org/10.1104/pp.17.01144
Liu L, Li C, Song S et al (2018b) FTIP-dependent STM trafficking regulates shoot meristem development in Arabidopsis. Cell Rep 23:1879–1890. https://doi.org/10.1016/j.celrep.2018.04.033
MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62:689–703. https://doi.org/10.1111/j.1365-313X.2010.04181.x
Manabe T, Nishimura N, Miura M, Yamamoto S (2000) Population structure and spatial patterns for trees in a temperate old-growth evergreen broad-leaved forest in Japan. Plant Ecol 151:181–197. https://doi.org/10.1023/A:1026512404110
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Ohba H (2001) Hamamelidaceae. In: Iwatsuki K, Boufford DE, Ohba H (eds) Flora of Japan, Vol 2b: Archichlamydeae (b). Kodansya, Tokyo, pp 5–9
Okino K, Shimakawa Y, Nagaoka S (1994) Evolution of the Shikoku Basin. J Geomagn Geoelectr 46:463–479. https://doi.org/10.5636/jgg.46.463
Ono M (1991) The flora of the Bonin (Ogasawara) Islands. Aliso 13:95–105. https://doi.org/10.5642/aliso.19911301.04
Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ (2014) PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol 31:1929–1936. https://doi.org/10.1093/molbev/msu136
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Savolainen O, Pyhäjärvi T (2007) Genomic diversity in forest trees. Curr Opin Plant Biol 10:162–167. https://doi.org/10.1016/j.pbi.2007.01.011
Shimizu Y (1994) Ogasawara syotou hahajima rettou no syokusei – kansei teibokurin no bunpu sosei kouzou wo tyuushinnni. Komazawa Geogr 30:17–68 (in Japanese)
Shimizu Y, Tabata H (1991) Forest structures, composition, and distribution on a Pacific Island, with reference to ecological release and speciation. Pac Sci 45:28–49
Stuessy TF, Takayama K, López-Sepúlveda P, Crawford DJ (2014) Interpretation of patterns of genetic variation in endemic plant species of oceanic islands. Bot J Linn Soc 174:276–288. https://doi.org/10.1111/boj.12088
Su Y, Wang T, Deng F (2010) Contrasting genetic variation and differentiation on Hainan Island and the Chinese mainland populations of Dacrycarpus imbricatus (Podocarpaceae). Biochem Syst Ecol 38:576–584. https://doi.org/10.1016/j.bse.2010.07.003
Suetsugu N, Higa T, Kong S-G, Wada M (2015) PLASTID MOVEMENT IMPAIRED1 and PLASTID MOVEMENT IMPAIRED1-RELATED1 mediate photorelocation movements of both chloroplasts and nuclei1. Plant Physiol 169:1155–1167. https://doi.org/10.1104/pp.15.00214
Sugai K, Setsuko S (2016) Novel microsatellite markers for Distylium lepidotum (Hamamelidaceae) endemic to the Ogasawara Islands. BMC Res Notes:9. https://doi.org/10.1186/s13104-016-2137-9
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tanouchi H, Yamamoto S (1995) Structure and regeneration of canopy species in an old-growth evergreen broad-leaved forest in Aya District, southwestern Japan. Vegetatio 117:51–60. https://doi.org/10.1007/BF00033258
Tsukada M (1985) Map of vegetation during the last glacial maximum in Japan. Quat Res 23:369–381. https://doi.org/10.1016/0033-5894(85)90041-9
Umino S, Nakano S (2007) Geology of the Chichijima Retto District. Qadrangle Series, 1:50,0000, Geological Survey of Japan. AIST (in Japanese with English abstract)
Umino S, Ishizuka O, Kanayama K (2016) Geology of the Hahajima Retto District. Quadrangle Series, 1:50,000, Geological Survey of Japan, AIST, 46 p(in Japanese with English abstract 2 p.)
Xie L, Yi T-S, Li R, Li D-Z, Wen J (2010) Evolution and biogeographic diversification of the witch-hazel genus (Hamamelis L., Hamamelidaceae) in the Northern Hemisphere. Mol Phylogenet Evol 56:675–689. https://doi.org/10.1016/j.ympev.2010.02.018
Yoshida T, Tamekuni M, Yahara T, Inomata N, Tachida H (2014) Demographic history of a common pioneer tree, Zanthoxylum ailanthoides, reconstructed using isolation-with-migration model. Tree Genet Genomes 10:1213–1222. https://doi.org/10.1007/s11295-014-0755-8
Zhang H and Endress PK (2003) Hamamelidaceae. In: Wu ZY, Raven PH and Hong DY (eds) Flora of China, Vol 9 Pittosporaceae through Connaraceae, Science Press, Beijing, and Missouri Botanical Garden, St. Louis), pp. 28–30.
Acknowledgments
We thank two anonymous reviewers and the Associate Editor for their thoughtful comments on an earlier version of this manuscript. We thank Atsuya Kamei, Makiko Mimura, Atsushi Sakai, and Naoyuki Nishimura for helping us to collect samples used in this study.
Data archiving statement
The sequences data from this study have been submitted to the DDBJ Sequence Read Archive (SRA) (https://www.ddbj.nig.ac.jp/dra/index.html) under Accession No. DRA008576.
Funding
This research was partially supported by the JSPS, grant numbers JP26291082 (HT), JP16H02553 (HT), and 16K07466 (JK) and 2331067 (SS) and the Environment Research and Technology Development Fund of the Ministry of the Environment, Japan (4-1402, SS).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y. Tsumura
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Hitomi Yagi and Jie Xu contributed to this work equally.
Electronic supplementary material
ESM 1
(DOCX 2972 kb)
Rights and permissions
About this article
Cite this article
Yagi, H., Xu, J., Moriguchi, N. et al. Population genetic analysis of two species of Distylium: D. racemosum growing in East Asian evergreen broad-leaved forests and D. lepidotum endemic to the Ogasawara (Bonin) Islands. Tree Genetics & Genomes 15, 77 (2019). https://doi.org/10.1007/s11295-019-1386-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-019-1386-x