Evolution of South African brambles (Rubus L.) – new insights from molecular markers
DOI:
https://doi.org/10.38201/btha.abc.v53.i1.8Keywords:
apomixis, reticulate evolution, introgression, clonal spread, hybridisationAbstract
Background: South African brambles (Rubus L., Rosaceae) represent a complex group of six native species and at least 12 introduced taxa with different ploidy levels and varying tendencies to hybridisation. The role of hybridisation, introgression and apomixis in the ongoing evolution has been hypothesised based on morphological observations, but it has not been rigorously studied to date, and nor has the phylogeny of the group.
Objectives and methods: This paper aims to reveal the evolutionary patterns and mechanisms in South African brambles by employing three types of molecular markers: plastid and nuclear ribosomal DNA sequences, and nuclear microsatellites.
Results: The data confirmed the tetraploid R. thaumasius A.Beek and diploid R. ludwigii Eckl. & Zeyh. as distinct native species, while the other four native species are shown to be closely related and likely derived from three ancestors.
Conclusion: Ancient hybridisation and limited gene flow between regions (particularly between winter- and summer-rainfall zones) appear to be the main drivers of current patterns in the tetraploid R. pinnatus Willd. and hexaploid R. rigidus Sm. Current hybridisation is also likely, although rare. The mechanism of ‘octoploid bridge’ is proposed, which overcomes the ploidy reproduction barrier between R. pinnatus (or other tetraploids) and R. rigidus. No gene flow was detected between native and alien taxa, but clonal duplications were discovered in the R. bergii × pinnatus hybrid, which implies the possibility of apomictic spread of homoploid hybrids formed between native and introduced brambles and the potential for a new invasion. On the other hand, heteroploid hybrids (R. bergii × rigidus) are formed recurrently and spread only vegetatively.
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References
Alice, L. & Campbell, C., 1999, ‘Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences’, American Journal of Botany 86(1), 81–97, https://doi.org/10.2307/2656957.
Alice, L.A., Goldman, D.H., Macklin, J.A. & Moore, G., 2015, ‘Rubus’, in Flora of North America, Editorial Committee (ed.) Flora of North America North of Mexico, vol. 9, New York and Oxford, http://www.efloras.org/florataxon.aspx?flora_id=1&taxon_id=128837.
Ayres, D.R., Zaremba, K. & Strong, D.R., 2004, ‘Extinction of a common native species by hybridization with an invasive congener’, Weed Technology 18, 1288–1291, http://www.jstor.org/stable/3989636.
Bandelt, H.J., Forster, P. & Rohl, A., 1999, ‘Median-joining networks for inferring intraspecific phylogenies’, Molecular Biology and Evolution 16(1), 37–48, https://doi.org/10.1093/oxfordjournals.molbev.a026036.
Carter, K.A., Liston, A., Bassil, N.V., Alice, L.A., Bushakra, J.M., Sutherland, B.L., Mockler, T.C., Bryant, D.W. & Hummer, K.E., 2019, ‘Target capture sequencing unravels Rubus evolution’, Frontiers in Plant Science 10, 1–18, https://doi.org/10.3389/fpls.2019.01615.
Clark, L. V. & Jasieniuk, M., 2012, ‘Spontaneous hybrids between native and exotic Rubus in the Western United States produce offspring both by apomixis and by sexual recombination’, Heredity 109, 320–328, https://doi.org/10.1038/hdy.2012.45.
Doyle, J.J. & Doyle, J.L., 1987, ‘A rapid DNA isolation procedure for small quantities of fresh leaf tissue’, Phytochemical Bulletin 19:11–15.
Dunning, L.T. & Savolainen, V., 2010, ‘Broad-scale amplification of matK for DNA barcoding plants, a technical note’, Botanical Journal of the Linnean Society 164(1), 1–9, https://doi.org/10.1111/j.1095-8339.2010.01071.x.
Ellstrand, N.C. & Schierenbeck, K.A., 2006, ‘Hybridization as a stimulus for the evolution of invasiveness in plants?’, Euphytica 148, 35–46, https://doi.org/10.1007/s10681-006-5939-3.
Fehrer, J., Krak, K. & Chrtek, J., 2009, ‘Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise’, BMC Evolutionary Biology 9, 239, https://doi.org/10.1186/1471-2148-9-239.
Graham, J., Smith, K., MacKenzie, K., Jorgenson, L., Hackett, C. & Powell, W., 2004, ‘The construction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic-SSR and EST-SSR markers’, Theoretical and Applied Genetics 109(4), 740–749, https://doi.org/10.1007/s00122-004-1687-8.
Graham, J., Smith, K., Tierney, I., MacKenzie, K. & Hackett, C.A., 2006, ‘Mapping gene H controlling cane pubescence in raspberry and its association with resistance to cane botrytis and spur blight, rust and cane spot’, Theoretical and Applied Genetics 112(5), 818–831, https://doi.org/10.1007/s00122-005-0184-z.
Gustafsson, C.E., 1934, ‘Rubi africani’, Arkiv för Botanik 26A, 1–68.
Henderson, L., 2011, ‘Rubus species – brambles, blackberries and others’, SAPIA News 19, 1–9.
Huson, D.H. & Bryant, D., 2006, ‘Application of phylogenetic networks in evolutionary studies’, Molecular biology and evolution 23(2), 254–67, https://doi.org/10.1093/molbev/msj030.
Király, G., Sochor, M. & Trávníček, B., 2017, ‘Reopening an old chapter: a revised taxonomic and evolutionary concept of the Rubus montanus group’, Preslia 89, 309–331, https://doi.org/10.23855/preslia.2017.309.
Kurtto, A., Weber, H.E., Lampinen, R. & Sennikov, A.N. (eds), 2010, ‘Atlas florae Europaeae. Distribution of vascular plants in Europe, vol. 15: Rosaceae (Rubus)’, Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, Helsinki.
Matsuyama, S., Morimoto, M., Harata, T., Nanami, S. & Itoh, A., 2018, ‘Hybridization rate and genotypic diversity of apomictic hybrids between native (Taraxacum japonicum) and introduced (T. officinale) dandelions in western Japan’, Conservation Genetics 19, 181–191, https://doi.org/10.1007/s10592-017-1014-y.
Meirmans, P.G. & Van Tienderen, P.H., 2004, ‘Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms’, Molecular Ecology Notes 4(4), 792–794, https://doi.org/10.1111/j.1471-8286.2004.00770.x.
Nolte, A.W. & Tautz, D., 2010, ‘Understanding the onset of hybrid speciation’, Trends in Genetics 26, 54–58.
Ochieng, J.A., Oyoo, M.E., Gesimba, R.M., Korir, P.C., Okwiri Ojwang’, P.P. & Owuoche, J.O., 2018, ‘Genetic diversity of blackberry (Rubus subgenus Rubus Watson) in selected counties in Kenya using simple sequence repeats (SSRs) markers’, African Journal of Biotechnology 17(39), 1247–1264, https://doi.org/10.5897/ajb2018.16613.
Ochieng, J.A., Gesimba, R.M., Oyoo, M.E., Korir, P.C., Owuoche, J.O. & Miheso, M., 2019, ‘Morphological characterization of blackberry (Rubus subgenus Rubus Watson) genetic resources in Kenya’, African Journal of Plant Science. 13(11), 297–308, https://doi.org/10.5897/ajps2018.1703.
Parepa, M., Fischer, M., Krebs, C. & Bossdorf, O., 2014, ‘Hybridization increases invasive knotweed success’, Evolutionary Applications 7(3), 413–420, https://doi.org/10.1111/eva.12139.
Peakall, R. & Smouse, P.E., 2012, ‘GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update’, Bioinformatics 28(19), 2537–2539, https://doi.org/10.1093/bioinformatics/bts460.
Pfennig, K.S., Kelly, A.L. & Pierce, A.A., 2016, ‘Hybridization as a facilitator of species range expansion’, Proceedings of the Royal Society B: Biological Sciences 283, 20161329, http://dx.doi.org/10.1098/rspb.2016.1329.
Ramsey, J. & Schemske, D.W., 1998, ‘Pathways, mechanisms, and rates of polyploid formation in flowering plants’, Annual Review of Ecology and Systematics 29, 467–501, https://doi.org/10.1146/annurev.ecolsys.29.1.467.
Rieseberg, L., 1995, ‘The role of hybridization in evolution: old wine in new skins’, American Journal of Botany 82, 944–953.
Šarhanová, P., Sharbel, T.F., Sochor, M., Vašut, R.J., Dančák, M. & Trávníček, B., 2017, ‘Hybridization drives evolution of apomicts in Rubus subgenus Rubus: evidence from microsatellite markers’, Annals of Botany 120, 317–328, https://doi.org/10.1093/aob/mcx033.
Šarhanová, P., Vašut, R.J., Dančák, M., Bureš, P. & Trávníček, B., 2012. ‘New insights into the variability of reproduction modes in European populations of Rubus subgen. Rubus: how sexual are polyploid brambles?’, Sexual Plant Reproduction 25, 319–335, https://doi.org/DOI 10.1007/s00497-012-0200-9.
Sochor, M., Hroneš, M. & Manning, J.C., 2022, ‘Guide to the genus Rubus L. (Rosaceae) in South Africa – disentangling a taxonomic Gordian knot with the help of ploidy and reproductive data’, South African Journal of Botany 147, 511–567, https://doi.org/10.1016/j.sajb.2022.01.044.
Sochor, M., Šarhanová, P., Pfanzelt, S. & Trávníček, B., 2017, ‘Is evolution of apomicts driven by the phylogeography of the sexual ancestor? Insights from European and Caucasian brambles (Rubus, Rosaceae)’, Journal of Biogeography 4, 2717–2728, https://doi.org/10.1111/jbi.13084.
Sochor, M. & Trávníček, B., 2016, ‘Melting pot of biodiversity: first insights into the evolutionary patterns of the Colchic bramble flora (Rubus subgenus Rubus, Rosaceae)’, Botanical Journal of the Linnean Society 181, 610–620, https://doi.org/10.1111/boj.12436.
Sochor, M., Trávníček, B. & Manning, J.C., 2018, ‘Biosystematic revision of the native and naturalised species of Rubus L. (Rosaceae) in the Cape Floristic Region, South Africa’, South African Journal of Botany 118, 241–259, https://doi.org/10.1016/j.sajb.2018.07.015.
Sochor, M., Vašut, R.J., Sharbel, T.F. & Trávníček, B., 2015, ‘How just a few makes a lot: Speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae)’, Molecular Phylogenetics and Evolution 89, 13–27, https://doi.org/10.1016/j.ympev.2015.04.007.
Stirton, C.H., 1981, ‘Notes on the taxonomy of Rubus in southern Africa’, Bothalia 13(3), 331–332.
Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J., 1991, ‘Universal primers for amplification of 3 noncoding regions of chloroplast DNA’, Plant Molecular Biology 17, 1105–1109, https://doi.org/10.1007/Bf00037152.
Van de Beek, A., 2014, ‘Rubus costifolius and R. bergii in the National Herbarium of Victoria’, Muelleria 32, 52–57, https://doi.org/10.5962/p.295687.
Van de Beek, A., 2021, ‘Rubi Capenses: a further contribution to the knowledge of the genus Rubus (Rosaceae) in South Africa’, Phytotaxa 515(1), 1–71, https://doi.org/10.11646/phytotaxa.515.1.1.
Weber, H. E., 1996, ‘Former and modern taxonomic treatment of the apomictic Rubus complex’, Folia Geobotanica Phytotaxonomica 31, 373–380.
White, T.J., Bruns, T., Lee, S. & Taylor, J.W., 1990, ‘Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics’, in M.A. Innis, D.H. Gelfand, J.J. Sninsky, & T.J. White (eds), PCR Protocols: A Guide to Methods and Applications, pp. 315–322, Academic Press, New York.
Woodhead, M., McCallum, S., Smith, K., Cardle, L., Mazzitelli, L. & Graham, J., 2008, ‘Identification, characterisation and mapping of simple sequence repeat (SSR) markers from raspberry root and bud ESTs’, Molecular Breeding 22(4), 555–563, https://doi.org/10.1007/s11032-008-9198-y.
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