[en] Introduction: The dramatic fluctuations of climate conditions since the late Tertiary era have resulted in major species range shifts. These movements were conditioned by geographic barriers and species dispersal capacities. In land plants, gene flow occurs through the movement of male gametes (sperm cells, pollen grains), which carry nDNA, and diaspores (spores, seeds), which carry both cpDNA and nDNA, making them an ideal model to compare the imprints of past climate change on the spatial genetic structures of different genomic compartments. Based on a meta-analysis of cpDNA and nDNA sequence data in western Europe, we test the hypotheses that nDNA genetic structures are similar in bryophytes and spermatophytes due to the similar size of spores and pollen grains, whereas genetic structures derived from the analysis of cpDNA are significantly stronger in spermatophytes than in bryophytes due to the substantially larger size of seeds as compared to spores. Methods: Sequence data at 1-4 loci were retrieved for 11 bryophyte and 17 spermatophyte species across their entire European range. Genetic structures between and within southern and northern populations were analyzed through F and N statistics and Mantel tests. Results and discussion: Gst and Nst between southern and northern Europe derived from cpDNA were significantly higher, and the proportion of significant tests was higher in spermatophytes than in bryophytes. This suggests that in the latter, migrations across mountain ranges were sufficient to maintain a homogenous allelic structure across Europe, evidencing the minor role played by mountain ranges in bryophyte migrations. With nDNA, patterns of genetic structure did not significantly differ between bryophytes and spermatophytes, in line with the hypothesis that spores and pollen grains exhibit similar dispersal capacities due to their size similarity. Stronger levels of genetic differentiation between southern and northern Europe, and within southern Europe, in spermatophytes than in bryophytes, caused by higher long-distance dispersal capacities of spores as compared to seeds, may account for the strikingly higher levels of endemism in spermatophytes than in bryophytes in the Mediterranean biodiversity hotspot.
Disciplines :
Genetics & genetic processes
Author, co-author :
Fichant, Timothée ; Université de Liège - ULiège > Faculté des Sciences > Doct. scienc. (biol. organ. écol.)
Ledent, Alice ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - Unité aCREA-Ulg (Conseils et Recherches en Ecologie Appliquée)
Vanderpoorten, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - Unité aCREA-Ulg (Conseils et Recherches en Ecologie Appliquée)
Language :
English
Title :
Dispersal capacities of pollen, seeds and spores: insights from comparative analyses of spatial genetic structures in bryophytes and spermatophytes
Andersen M. C. (1992). An analysis of variability in seed settling velocities of several wind-dispersed asteraceae. Am. J. Bot. 79 (10), 1087–1091. doi: 10.1002/j.15372197.1992.tb13702.x
Arditti J. Ghani A. K. A. (2000). Tansley Review No. 110. Numerical and physical properties of orchid seeds and their biological implications. New Phytol. 145 (3), 367–421. doi: 10.1046/j.14698137.2000.00587.x
Arjona Y. Nogales M. Heleno R. Vargas P. (2018). Long-distance dispersal syndromes matter: diaspore–trait effect on shaping plant distribution across the Canary Islands. Ecography (Copenhagen) 41 (5), 805–814. doi: 10.1111/ecog.02624
Bhagwat S. A. Willis K. J. (2008). Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits. J. biogeography 35 (3), 464–482. doi: 10.1111/j.13652699.2007.01861.x
Bullock J. M. Shea K. Skarpaas O. (2006). Measuring plant dispersal: an introduction to field methods and experimental design. Plant Ecol. 186 (2), 217–234. doi: 10.1007/s11258-006-91245
Clobert J. Baguette M. Benton T. G. Bullock J. M. (2012). Dispersal Ecology and Evolution (Oxford: Oxford University Press). doi: 10.1093/acprof:oso/9780199608898.001.0001
Comes H. P. Kadereit J. W. (1998). The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3 (11), 432–438. doi: 10.1016/S1360-1385(98)01327-2
Désamoré A. Laenen B. Stech M. Papp B. Hedenäs L. Mateo R. et al. (2012). How do temperate bryophytes face the challenge of a changing environment? Lessons from the past and predictions for the future. Global Change Biol. 18 (9), 2915–2924. doi: 10.1111/j.1365-2486.2012.02752.x
Edgar R. C. (2004). MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinf. 5 (1), 113–113. doi: 10.1186/1471-2105-5-113
Evans A. de Kort H. Brys R. Duffy K. J. Jersáková J. Kull T. et al. (2023). Historical biogeography and local adaptation explain population genetic structure in a widespread terrestrial orchid. Ann. Bot. 131 (4), 623–634. doi: 10.1093/aob/mcad010
Gouy M. Guindon S. Gascuel O. (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27 (2), 221–224. doi: 10.1093/molbev/msp259
Grundmann M. Ansell E. W. Russell S. J. Koch M. A. Vogel J. C. (2007). Genetic structure of the widespread and common Mediterranean bryophyte Pleurochaete squarrosa (Brid.) Lindb. (Pottiaceae) – evidence from nuclear and plastidic DNA sequence variation and allozymes. Mol. Ecol. 16 (4), 709–722. doi: 10.1111/j.1365294X.2007.03181.x
Hao K. Tian Z.-X. Wang Z.-C. Huang S.-Q. (2020). Pollen grain size associated with pollinator feeding strategy. Proc. R. Society. B Biol. Sci. 287 (1933), 20201191–20201191. doi: 10.1098/rspb.2020.1191
Hardy O. J. Vekemans X. (2002). spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. notes. 2 (4), 618–620. doi: 10.1046/j.1471-8286.2002.00305.x
Hewitt G. M. (1996). Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Society. 58 (3), 247–276. doi: 10.1111/j.1095-8312.1996.tb01434.x
Hewitt G. M. (1999). Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68 (1–2), 87–112. doi: 10.1006/bijl.1999.0332
Hewitt G. (2000). The genetic legacy of the Quaternary ice ages. Nat. (London) 405 (6789), 907–913. doi: 10.1038/35016000
Hewitt G. (2003). “‘18 - Ice ages: Species distributions, and evolution’,” in Evolution on Planet Earth. Eds. Rothschild L. J. Lister A. M. (London: Academic Press), 339–361. doi: 10.1016/B978-012598655-7/50045-8
Hewitt G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. Biol. Sci. 359 (1442), 183–195. doi: 10.1098/rstb.2003.1388
Hirose Y. Osada K. (2016). Terminal settling velocity and physical properties of pollen grains in still air. Aerobiologia 32 (3), 385–394. doi: 10.1007/s10453-015-9408-0
Hodgetts N. Lockhart N. (2020). Checklist and country status of European bryophytes – update 2020 (Gaeltacht, Ireland: Irish Wildlife Manuals, No. 84. National Parks and Wildlife Service, Department of Arts, Heritage).
Hutsemékers V. Shaw A. J. Szvovenyi P. Gonzalez-Mancebo J. M. Muñoz J. Vanderpoorten A. (2011). Oceanic islands are not sinks of biodiversity in spore-producing plants. Proc. Natl. Acad. Sci. - PNAS 108 (47), 18989–18994. doi: 10.1073/pnas.1109119108
Katul G. G. Porporato A. Nathan R. Siqueira M. Soons M. B. Poggi D. et al. (2005). Mechanistic analytical models for long-distance seed dispersal by wind. Am. Nat. 166 (3), 368–381. doi: 10.1086/432589
Korpelainen H. Pohjamo M. Laaka-Lindberg S. (2005). ‘How efficiently does bryophyte dispersal lead to gene flow?’. J. Hattori Botanical Lab. 97, 195–205.
Kyrkjeeide M. O. Hassel K. Flatberg K. I. Shaw A. J. Brochmann C. Stenøien H. K. (2016). Long-distance dispersal and barriers shape genetic structure of peatmosses (Sphagnum) across the Northern Hemisphere. J. biogeography 43 (6), 1215–1226. doi: 10.1111/jbi.12716
Laenen B. Désamoré A. Devos N. Shaw A. J. Carine M. A. Gonzalez-Mancebo J. M. et al. (2011). Macaronesia: a source of hidden genetic diversity for post-glacial recolonization of western Europe in the leafy liverwort Radula lindenbergiana: Hidden diversity in Macaronesia. J. biogeography 38 (4), 631–639. doi: 10.1111/j.1365-2699.2010.02440.x
Laenen B. Machac A. Gradstein S. R. Shaw B. Patiño J. Désamoré A. et al. (2016). Geographical range in liverworts: does sex really matter? J. biogeography 43 (3), 627–635. doi: 10.1111/jbi.12661
Ledent A. Désamoré A. Laenen B. Mardulyn P. McDaniel S. F. Zanatta F. et al. (2019). No borders during the post-glacial assembly of European bryophytes. Ecol. Lett. 22 (6), 973–986. doi: 10.1111/ele.13254
Lopez-Alvarado J. Farris E. (2022). Ecology and evolution of plants in the mediterranean basin: perspectives and challenges’. Plants (Basel) 11 (12), 1584. doi: 10.3390/plants11121584
Lumibao C. Y. Hoban S. M. McLachlan J. (2017). Ice ages leave genetic diversity “hotspots” in Europe but not in Eastern North America. Ecol. Lett. 20 (11), 1459–1468. doi: 10.1111/ele.12853
Médail F. Diadema K. (2009). Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J. biogeography 36 (7), 1333–1345. doi: 10.1111/j.1365-2699.2008.02051.x
Morgan E. J. Kaiser-Bunbury C. N. Edwards P. J. Fleischer-Dogley F. Kettle C. J. (2017). Tracing coco de mer’s reproductive history: Pollen and nutrient limitations reduce fecundity. Ecol. Evol. 7 (19), 7765–7776. doi: 10.1002/ece3.3312
Mouton L. Patiño J. Carine M. Rumsey F. Menezes de Sequeira M. González-Mancebo J. M. et al. (2023). Patterns and drivers of beta diversity across geographic scales and lineages in the Macaronesian flora. J. biogeography 50 (5), 858–869. doi: 10.1111/jbi.14580
Ness R. W. Kraemer S. A. Colegrave N. Keightley P. D. (2016). Direct estimate of the spontaneous mutation rate uncovers the effects of drift and recombination in the Chlamydomonas reinhardtii plastid genome. Mol. Biol. Evol. 33 (3), 800–808. doi: 10.1093/molbev/msv272
Paradis E. Schliep K. (2019). pe 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 (3), 526–528. doi: 10.1093/bioinformatics/bty633
Patiño J. Carine M. Fernández-Palacios J. M. Otto R. Schaefer H. Vanderpoorten A. (2014b). The anagenetic world of spore-producing land plants. New Phytol. 201 (1), 305–311. doi: 10.1111/nph.12480
Patiño J. Guilhaumon F. Triantis K. A. Gradstein S. R. Hedenäs L. González-Mancebo J. M. et al. (2013). Accounting for data heterogeneity in patterns of biodiversity: an application of linear mixed effect models to the oceanic island biogeography of spore-producing plants. Ecography (Copenhagen) 36(8), 904–913. doi: 10.1111/j.1600-0587.2012.00020.x
Patiño J. Vanderpoorten A. (2018). ‘Bryophyte biogeography’. Critical Reviews in Plant Sciences 37, 175–209.
Patiño J. Weigelt P. Weigelt P. Solymos P. Guilhaumon F. Kreft H. Triantis K. et al. (2014a). Differences in species-area relationships among the major lineages of land plants: a macroecological perspective. Global Ecol. biogeography 23 (11), 1275–1283. doi: 10.1111/geb.12230
Petit R. J. Aguinalde I. de Beaulieu J. L. Bittkau C. Brewer S. Cheddadi R. et al. (2003). Glacial refugia; hotspots but not melting pots of genetic diversity. Sci. (American Assoc. Advancement Science) 300 (5625), 1563–1565. doi: 10.1126/science.1083264
Petit R. J. Duminil J. Fineschi S. Hampe A. Salvini D. Vendramin G. G. et al. (2005). Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol. Ecol. 14 (3), 689–701. doi: 10.1111/j.1365-294X.2004.02410.x
Pohjamo M. Laaka-Lindberg S. Ovaskainen O. Korpelainen H. (2006). Dispersal potential of spores and asexual propagules in the epixylic hepatic Anastrophyllum hellerianum. Evolutionary Ecol. 20 (5), 415–430. doi: 10.1007/s10682-006-0011-2
Pons O. Petit R. J. (1996). Measuring and testing genetic differentiation with ordered versus unordered alleles. Genet. (Austin) 144 (3), 1237–1245. doi: 10.1093/genetics/144.3.1237
Pressel S. Duckett J. G. (2019). ‘Do motile spermatozoids limit the effectiveness of sexual reproduction in bryophytes? Not in the liverwort Marchantia polymorpha’. J. systematics evolution: JSE 57 (4), 371–381. doi: 10.1111/jse.12528
Ritland K. (1996). Estimators for pairwise relatedness and individual inbreeding coefficients. Genetical Res. 67 (2), 175–185. doi: 10.1017/S0016672300033620
Ros R. M. Mazimpaka V. Abou-Salama U. Aleffi M. Blockeel T. L. Brugués M. et al. (2007). Hepatics and anthocerotes of the mediterranean, an annotated checklist. Cryptogamie Bryologie 28 (4), 351–437.
Ros R. M. Mazimpaka V. Abou-Salama U. Aleffi M. Blockeel T. L. Brugués M. et al. (2013). Mosses of the mediterranean, an annotated checklist. Cryptogamie. Bryologie 34 (2), 99–283. doi: 10.7872/cryb.v34.iss2.2013.99
Santos dos J. Galarda Varassin I. Cunha Muschner V. Ovaskainen O. (2018). Estimating seed and pollen dispersal kernels from genetic data demonstrates a high pollen dispersal capacity for an endangered palm species. Am. J. Bot. 105 (11), 1802–1812. doi: 10.1002/ajb2.1176
Stojanović D. Aleksić J. M. Jančić I. Jančić R. (2015). A Mediterranean medicinal plant in the continental Balkans: A plastid DNA-based phylogeographic survey of Salvia officinalis (Lamiaceae) and its conservation implications. Willdenowia 45 (1), 103–118. doi: 10.3372/wi.45.45112
Talavera G. Castresana J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biol. 56 (4), 564–577. doi: 10.1080/10635150701472164
Tranchida-Lombardo V. Cafasso D. Cristaudo A. Cozzolino S. (2011). Phylogeographic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium. Ann. Bot. 107 (3), 427–436. doi: 10.1093/aob/mcq256
Vekemans X. Hardy O. J. (2004). New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. ecology. 13 (4), 921–935. doi: 10.1046/j.1365-294X.2004.02076.x
Zanatta F. Patiño J. Lebeau F. Massinon M. Hylander K. Degreef J. et al. (2016). Measuring spore settling velocity for an improved assessment of dispersal rates in mosses. Ann. Bot. 118 (2), 197–206. doi: 10.1093/aob/mcw092
Zanatta F. Engler R. Collart F. Broennimann O. Mateo R. G. Papp B. et al. (2020). Bryophytes are predicted to lag behind future climate change despite their high dispersal capacities. Nat. Commun. 11 (1), 5601–5601. doi: 10.1038/s41467-020-19410-8
Zotz G. Weichgrebe T. Happatz H. Einzmann H. (2016). Measuring the terminal velocity of tiny diaspores. Seed Sci. Res. 26 (3), 222–230. doi: 10.1017/S0960258516000155
Van Zuijlen K. Nobis M. P. Hedenäs L. Hodgetts N. Calleja Alarcón J. A. et al. (2023). Bryophytes of Europe Traits (BET) data set: A fundamental tool for ecological studies. J. vegetation Sci. 34 (2), e13179. doi: 10.1111/jvs.13179
