Abstract
Woodlands in Iceland are characterized by shrub-like birch, a result of introgressive hybridization between diploid dwarf birch, Betula nana, and tetraploid downy birch, B. pubescens. Introgression occurs via triploid hybrids. We evaluated the fertility of triploid birch by examining pollen viability and seed germination. Pollen samples were collected from woodlands throughout Iceland from 99 plants, including 22 triploid hybrids. The germination of pollen from the triploid hybrids was about one third that of the diploid or tetraploid species (mean values: 9% vs. 26% and 29%). Most triploid plants had a pollen germination of less than 2%. However, some showed exceptionally high pollen fertility (six plants: 11–79%). Microscopic examination revealed normal pollen tube growth and elongation in hybrids with low germination, while other hybrids showed abnormal tube growth. Fluorescence microscopy indicated pollen viability in all ploidy groups, with green autofluorescence from the cytoplasmic contents and red fluorescence from the exine wall. The Aniline test of pollen viability showed that grains with three pores (normal, triporate grains) stained positively, but non-triporate grains were unstained and empty. Germination tests were performed on seeds collected from 246 plants, including 21 triploid hybrids. The germination percentage of seeds from triploid hybrid plants was about 20 times lower than that of the diploid or the tetraploid species (population means: 0–4% vs. 3–41% and 6–54%). The present study shows that triploid birch hybrids are not sterile. Both the paternal and maternal fertility of the hybrids should be sufficient to facilitate gene flow via backcrossing with the parental species.
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References
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al (2013) Hybridization and speciation. J Evol Biol 26:229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x
Abdelgadir HA, Johnson SD, Van Staden J (2012) Pollen viability, pollen germination and pollen tube growth in the biofuel seed crop Jatropha curcas (Euphobiaceae). S Afr J Bot 79:132–139. https://doi.org/10.1016/j.sajb.2011.10.005
Alexander MP (1969) Differential staining of aborted and non aborted pollen. Stain Technol 44:117–122. https://doi.org/10.3109/10520296909063335
Anamthawat-Jónsson K (2004) Preparation of chromosomes from plant leaf meristems for karyotype analysis and in situ hybridisation. Meth Cell Sci 25:91–95. https://doi.org/10.1007/s11022-004-5620-y
Anamthawat-Jónsson K (2012) Hybridisation, introgression and phylogeography of Icelandic birch. In: Anamthawat-Jónsson K (ed) Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems. In: Tech—Open Access Publisher, Croatia, pp 117–144. ISBN: 978-953-51-0217-5
Anamthawat-Jónsson K (2018) Triploid birch hybrids. Fluorescence imaging of birch mitosis and meiosis. Imaging Microscopy 20:18–21
Anamthawat-Jónsson K (2019) Hybrid introgression: the outcomes of gene flow in birch. ScienceAsia 45:203–211. https://doi.org/10.2306/scienceasia1513-1874.2019.45.203
Anamthawat-Jónsson K, Sigurdsson V (1998) Chromosome number of Icelandic Populus tremula. Nord J Bot 18:471–473
Anamthawat-Jónsson K, Thórsson ÆTh (2003) Natural hybridisation in birch: triploid hybrids between Betula nana and B. pubescens. Plant Cell Tiss Organ Cult 75:99–107. https://doi.org/10.1023/A:1025063123552
Anamthawat-Jónsson K, Tómasson T (1990) Cytogenetics of hybrid introgression in Icelandic birch. Hereditas 112:65–70. https://doi.org/10.1111/j.1601-5223.1990.tb00138.x
Anamthawat-Jónsson K, Tómasson T (1999) High frequency of triploid birch hybrid by Betula nana seed parent. Hereditas 130:191–193. https://doi.org/10.1111/j.1601-5223.1999.00191.x
Anderson E (1953) Introgressive hybridization. Biol Rev 28:280–307. https://doi.org/10.1111/j.1469-185X.1953.tb01379.x
Aradottir AL, Eysteinsson T (2005) Restoration of birch woodlands in Iceland. In: Stanturf JA, Madsen P (eds) Restoration of boreal and temperate forests. CRC Press, Boca Raton, pp 195–209. https://doi.org/10.1201/9780203497784.pt5
Aradottir AL, Halldorsson G (2018) Colonization of woodland species during restoration: seed or safe site limitation? Restor Ecol 26:S73–S83. https://doi.org/10.1111/rec.12645
Ashburner K, McAllister HA (2013) The genus Betula: a taxonomic revision of birches. Royal Botanic Garden Kew Publishing, London. ISBN: 978-184-24-6141-9
Atkinson MD (1992) Biological flora of the British Isles: Betula pendula Roth (B. verrucosa Ehrh.) and B. pubescens Ehrh. J Ecol 80:837–870. https://doi.org/10.2307/2260870
Atlagic J, Terzic S, Marjanovic-Jeromela A (2012) Staining and fluorescent microscopy methods for pollen viability determination in sunflower and other plant species. Ind Crop Prod 35:88–91. https://doi.org/10.1016/j.indcrop.2011.06.012
Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568. https://doi.org/10.1046/j.1365-294x.2001.01216.x
Boavida LC, Silva JP, Feijo JA (2001) Sexual reproduction in the cork oak (Quercus suber L). II. Crossing intra- and interspecific barriers. Sex Plant Reprod 14:143–152. https://doi.org/10.1007/s004970100100
Boucher D, Gauthier S, Thiffault N, Marchand W, Girardin M, Urli M (2020) How climate change might affect tree regeneration following fire at northern latitudes: a review. New For. https://doi.org/10.1007/s11056-019-09745-6
Bradshaw JA, Warkentin IG, Sodhi NS (2009) Urgent preservation of boreal carbon stocks and biodiversity. Trends Ecol Evol 24:541–548. https://doi.org/10.1016/j.tree.2009.03.019
Brooks J, Shaw G (1978) Sporopollenin: a review of its chemistry, palaeochemistry and geochemistry. Grana 17:91–97. https://doi.org/10.1080/00173137809428858
Burgarella C, Barnaud A, Kane NA, Jankowski F, Scarcelli N, Billot C et al (2019) Adaptive introgression: An untapped evolutionary mechanism for crop adaptation. Front Plant Sci 10: article 4. https://doi.org/10.3389/fpls.2019.00004
Chebli Y, Kroeger J, Geitmann A (2013) Transport logistics in pollen tubes. Mol Plant 6:1037–1052. https://doi.org/10.1093/mp/sst073
Chunco AJ (2014) Hybridization in a warmer world. Ecol Evol 4:2019–2031. https://doi.org/10.1002/ece3.1052
De Groot WJ, Thomas PA, Wein RW (1997) Betula nana L. and Betula glandulosa Michx. J Ecol 85:241–264. https://doi.org/10.2307/2960655
Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328. https://doi.org/10.1111/j.1365-313X.2005.02379.x
Edlund AF, Zheng Q, Lowe N, Kuseryk S, Ainsworth KL, Lyles RH et al (2016) Pollen from Arabidopsis thaliana and other Brassicaceae are functionally omniaperturate. Am J Bot 103:1006–1019. https://doi.org/10.3732/ajb.1600031
eFlora (2020a) Betula Linnaeus. Flora of North America, vol 3. Published on the Internet http://www.efloras.org. Accessed 15 Jan 2020. Missouri Botanical Garden, St. Louis, MO & Harvard University Herbaria, Cambridge, MA
eFlora (2020b) Betula Linnaeus. Flora of China, vol 4, p 304. Published on the Internet http://www.efloras.org. Accessed 15 Jan 2020. Missouri Botanical Garden, St. Louis, MO & Harvard University Herbaria, Cambridge, MA
Eidesen PB, Alsos IG, Brochmann C (2015) Comparative analyses of plastid and AFLP data suggest different colonization history and asymmetric hybridization between Betula pubescens and B. nana. Mol Ecol 24:3993–4009. https://doi.org/10.1111/mec.13289
Elkington TT (1968) Introgressive hybridization between Betula nana L. and B. pubescens Ehrh. in North-West Iceland. New Phytol 67:109–118. https://doi.org/10.1111/j.1469-8137.1968.tb05459.x
Ellstrand NC, Rieseberg LH (2016) When gene flow really matters: gene flow in applied evolutionary biology. Evol Appl l9:833–836. https://doi.org/10.1111/eva.12402
Fonseca AE, Westgate ME, Doyle RT (2002) Application of fluorescence microscopy and image analysis for quantifying dynamics of maize pollen shed. Crop Sci 42:2201–2206. https://doi.org/10.2135/cropsci2002.2201
Heiser CB Jr (1973) Introgression re-examined. Bot Rev 39:347–366. https://doi.org/10.1007/BF02859160
Hultén E, Fries M (1986) Atlas of North European Vascular Plants. Köningstein Koeltz Scientific Books
Husband BC (2004) The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biol J Linn Soc 82:537–546. https://doi.org/10.1111/j.1095-8312.2004.00339.x
Jóhannsson MH, Stephenson AG (1998) Variation in sporophytic and gametophytic vigor in wild and cultivated varieties of Curcubita pepo and their F1 and F2 generations. Sex Plant Reprod 11:265–271. https://doi.org/10.1007/s004970050
Kallio P, Niemi S, Sulkinoja M, Valanne T (1983) The Fennoscandian birch and its evolution in the marginal forest zone. Nordicana 47:101–110
Karlsdóttir L, Thórsson ÆTh, Hallsdóttir M, Sigurgeirsson A, Eysteinsson T, Anamthawat-Jónsson K (2007) Differentiating pollen of Betula species from Iceland. Grana 46:78–84. https://doi.org/10.1080/00173130701237832
Karlsdóttir L, Hallsdóttir M, Thórsson ÆTh, Anamthawat-Jónsson K (2008) Characteristics of pollen from natural triploid Betula hybrids. Grana 47:52–59. https://doi.org/10.1080/00173130801927498
Karlsdóttir L, Hallsdóttir M, Thórsson ÆTh, Anamthawat-Jónsson K (2009) Evidence of hybridisation between Betula pubescens and B. nana in Iceland during the early Holocene. Rev Palaeobot Palyn 156:350–357. https://doi.org/10.1016/j.revpalbo.2009.04.001
Karlsdóttir L, Hallsdóttir M, Eggertsson Ó, Thórsson ÆTh, Anamthawat-Jónsson K (2014) Birch hybridization in Thistilfjördur, North-east Iceland during the Holocene. Icel Agric Sci 27:95–109
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Boulder, p 583
Kristinsson H (1995) Post-settlement history of Icelandic forests. Icel Agric Sci 9:31–35
Kristinsson H, Thórhaldsdóttir ThE, Hlidberg JB (2018) Flóra Íslands—Blómplöntur og byrkningar [Flora of Iceland—Flowering plants and bryophytes]. Vaka-Helgafell, Reykjavík, pp 116, 374, 424 [In Icelandic]. ISBN 978-9979-2-2486-0
Lindenmayer DB (2019) Integrating forest biodiversity conservation and restoration ecology principles to recover natural forest ecosystems. New For 50:169–181. https://doi.org/10.1007/s11056-018-9633-9
Löf M, Madsen P, Metslaid M, Witzell J (2019) Restoring forests: regeneration and ecosystem function for the future. New For 50:139–151. https://doi.org/10.1007/s11056-019-09713-0
Löve Á, Löve D (1956) Cytotaxonomical conspectus of the Icelandic Flora. Acta Horti Gotobg 20:135–140
Minder AM, Widmer A (2008) A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Mol Ecol 17:1552–1563. https://doi.org/10.1111/j.1365-294X.2008.03709.x
Mitsumoto K, Yabusaki K, Aoyagi H (2009) Classification of pollen species using autofluorescence image analysis. J Biosci Bioeng 107:90–94. https://doi.org/10.1016/j.jbiosc.2008.10.001
Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. BioSystems 109:397–402. https://doi.org/10.1016/j.biosystems.2012.04.006
Pöhlker C, Huffman JA, Förster JD, Pöschl U (2013) Autofluorescence of atmospheric bioaerosols: spectral fingerprints and taxonomic trends of pollen. Atmos Meas Tech 6:3369–3392. https://doi.org/10.5194/amt-6-3369-2013
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501. https://doi.org/10.1146/annurev.ecolsys.29.1.467
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639. https://doi.org/10.1146/annurev.ecolsys.33.010802.150437
Roshchina VV (2012) Vital autofluorescence: application to the study of plant living cells. Int J Spectroscopy article ID 124672. https://doi.org/10.1155/2012/124672
Snorrason A, Traustason B, Kjartansson BT, Heidarsson L, Ísleifsson R, Eggertsson Ó (2016) Náttúrulegt birki á Íslandi—Ný úttekt á útbreiðslu þess og ástandi (The natural birch woodland in Iceland—a new assessment on distribution and state). Náttúrufræðingurinn 86:87–111 [In Icelandic]
Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. W.H. Freeman and Company, New York
Stebbins GL (1959) The role of hybridization in evolution. Proc Am Philos Soc 103:231–251
Stebbins GL (1971) Chromosomal evolution in higher plants, 1st edn. Addison-Wesley Publishing Co., New York
Tangmitcharoen S, Owens JN (1997) Pollen viability and pollen-tube growth following controlled pollination and their relation to low fruit production in teak (Tectonus grandis Linn. f.). Ann Bot-London 80:401–410. https://doi.org/10.1006/anbo.1996.0440
Thórsson Æ, Salmela E, Anamthawat-Jónsson K (2001) Morphological, cytogenetic, and molecular evidence for introgressive hybridization in birch. J Hered 92:404–408. https://doi.org/10.1093/jhered/92.5.404
Thórsson ÆTh, Pálsson S, Sigurgeirsson A, Anamthawat-Jónsson K (2007) Morphological variation among Betula nana (diploid), B. pubescens (tetraploid) and their triploid hybrids in Iceland. Ann Bot-London 99:1183–1193. https://doi.org/10.1093/aob/mcm060
Thórsson ÆTh, Pálsson S, Lascoux M, Anamthawat-Jónsson K (2010) Introgression and phylogeography of Betula nana (diploid), B. pubescens (tetraploid) and their triploid hybrids in Iceland inferred from cp-DNA haplotype variation. J Biogeogr 37:2098–2110. https://doi.org/10.1111/j.1365-2699.2010.02353.x
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hubner S S et al (2016) Hybridization and extinction. Evol Appl 9:892–908. https://doi.org/10.1111/eva.12367
Traustason B, Snorrason A (2008) Spatial distribution of forests and woodlands in Iceland in accordance with the CORINE land cover classification. Icel Agric Sci 21:39–47
Tsuda Y, Semerikov V, Sebastiani F, Vendramin GG, Lascoux M (2016) Multispecies genetic structure and hybridization in the Betula genus across Eurasia. Mol Ecol 26:589–605. https://doi.org/10.1111/mec.13885
Vaarama A, Valanne T (1973) On the taxonomy, biology and origin of Betula tortuosa Ledeb. Rep Kevo Subarct Res Stat10:70–84
Walker DA (2000) Hierarchical subdivision of Arctic tundra based on vegetation response to climate, parent material and topography. Global Change Biol 6:19–34. https://doi.org/10.1046/j.1365-2486.2000.06010.x
Walters SM (1964) Betulaceae. In: Tutin TG, Heywood VH, Burges NA et al (eds) Flora Europaea, vol 1. Cambridge University Press, Cambridge, pp 57–59
Wang Z-Y, Ge Y, Scott M, Spangenberg G (2004) Viability and longevity of pollen from transgenic and nontransgenic tall fescue (Festuca arundinacea) (Poaceae) plants. Am J Bot 91:523–530. https://doi.org/10.3732/ajb.91.4.523
Wang L, Lv X, Li H, Zhang M, Wang H, Jin B, Chen T (2013) Inhibition of apoplastic calmodulin impairs calcium homeostasis and cell wall modelling during Cedrus deodara pollen tube growth. PLOS ONE 8(2):e55411. https://doi.org/10.1371/journal.pone.0055411
Wielgolaski FE (2001) Vegetation sections in northern Fennoscandian mountain birch forests. In: Wielgolaski FE (ed) Nordic Mountain Birch Ecosystems. The Parthenon Publishing Group, New York, pp 23–34. UNESCO ISBN 92-3-103783-8
Willemse MThM (1972) Changes in the autofluorescence of the pollen wall during microsporogenesis and chemical treatments. Acta Bot Neerl 21:1–16. https://doi.org/10.1111/j.1438-8677.1972.tb00742.x
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053. https://doi.org/10.1046/j.1523-1739.2001.0150041039.x
Acknowledgements
The project was funded by the University of Iceland’s Research Fund. We would like to thank Dr. Aðalsteinn Sigurgeirsson, Deputy Director of the Icelandic Forest Service, for providing the seed germination facility at Mógilsá. We are also grateful to Dr. Ása Aradóttir, Director of Research, the Agricultural University of Iceland, for sharing with us her knowledge on the subject of birch woodland restoration in Iceland.
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Anamthawat-Jónsson, K., Karlsdóttir, L., Thórsson, Æ.T. et al. Naturally occurring triploid birch hybrids from woodlands in Iceland are partially fertile. New Forests 52, 659–678 (2021). https://doi.org/10.1007/s11056-020-09816-z
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DOI: https://doi.org/10.1007/s11056-020-09816-z