Analyses of Hybrid Viability across a Hybrid Zone between Two Alnus Species Using Microsatellites and cpDNA Markers

. 2020 Jul 09 ; 11 (7) : . [epub] 20200709

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32659930

Diploid Alnus glutinosa s. str. and autotetraploid A. rohlenae form a narrow hybrid zone in a study area in southern Serbia, which results in triploid hybrid formation. The vast majority of previous studies have been focused on studies of maternal plants, but the offspring resulting from their crossing have not been much studied. Here, we use the variability of microsatellites and chloroplast DNA between these species and their putative hybrids to create an overall picture of the development of the hybrid zone and its predicted type. To elucidate the gene transfer within both species, the origins of individual ploidies and especially the role of triploid hybrids, a germination experiment was carried out linked with a flow cytometry study of the resulting seedlings. The tension zone model seems to offer the most adequate explanation of our observations, with selection against triploid hybrids and the spatial positioning of the hybrid zone. Despite selection against them, the triploid hybrids play an important role in the exchange of genes between the two species and therefore serve as a bridge for introgression. The presence of fertile triploids is essential for enriching the haplotype diversity between these species and for the development of new genetic lineages.

Zobrazit více v PubMed

Barton N.H., Hewitt G.M. Analysis of hybrid zones. Annu. Rev. Ecol. Evol. Syst. 1985;16:113–148. doi: 10.1146/annurev.es.16.110185.000553. DOI

Ross R.I., Agren J.A., Pannell J.R. Exogenous selection shapes germination behavior and seedling traits of populations at different altitudes in a Senecio hybrid zone. Ann. Bot. 2012;110:1439–1447. doi: 10.1093/aob/mcs211. PubMed DOI PMC

Abbott R.J., Brennan A.C. Altitudinal gradients, plant hybrid zones and evolutionary novelty. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014;369:20130346. doi: 10.1098/rstb.2013.0346. PubMed DOI PMC

Arnold M.L. Natural Hybridization and Evolution. Oxford University Press; Oxford, UK: 1997. p. 215.

Wang H., McArthur E.D., Sanderson S.C., Graham J.H., Freeman D.C. Narrow hybrid zone between two subspecies of big sagebrush (Artemisia tridentata: Asteraceae). IV. Reciprocal transplant experiments. Evolution. 1997;51:95–102. PubMed

Rieseberg L.H., Carney S.E. Plant Hybridization (Tansley Review, 102) New Phytol. 1998;140:599–624. doi: 10.1046/j.1469-8137.1998.00315.x. PubMed DOI

Milne R.I., Terzioglu S., Abbott R.J. A hybrid zone dominated by fertile F1s: Maintenance of species barriers in Rhododendron. Mol. Ecol. 2003;12:2719–2729. doi: 10.1046/j.1365-294X.2003.01942.x. PubMed DOI

Chapman M.A., Forbes D.G., Abbott R.J. Pollen competition among two species of Senecio (Asteraceae) that form a hybrid zone on Mt. Etna, Sicily. Am. J. Bot. 2005;92:730–735. doi: 10.3732/ajb.92.4.730. PubMed DOI

Rosenthal D.M., Schwarzbach A.E., Donovan L.A., Raymond O., Rieseberg L.H. Phenotypic differentiation between three ancient hybrid taxa and their parental species. Int. J. Plant Sci. 2002;163:387–398. doi: 10.1086/339237. DOI

Johnston J.A., Arnold M.L., Donovan L.A. High hybrid fitness at seed and seedling life history stages in Louisiana Irises. J. Ecol. 2003;91:438–446. doi: 10.1046/j.1365-2745.2003.00774.x. DOI

Barton N.H., Gale R.S. Genetic analysis of hybrid zones. In: Harrison R.G., editor. Hybrid Zones and the Evolutionary Process. Oxford University Press; New York, NY, USA: 1993. pp. 13–45.

Arnold M.L., Hodges S.A. Are natural hybrids fit or unfit relative to their parents. Trends Ecol. Evol. 1995;10:67–71. doi: 10.1016/S0169-5347(00)88979-X. PubMed DOI

Mandák B. Germination requirements of invasive and non-invasive Atriplex species: A comparative study. Flora. 2003;198:45–54. doi: 10.1078/0367-2530-00075. DOI

Douda J., Doudová J., Hodková E., Vít P., Krak K., Mandák B. Population history explains the performance of an annual herb—Within and beyond its European species range. J. Ecol. 2019;108:958–968. doi: 10.1111/1365-2745.13323. DOI

Douda J., Doudová J., Drašnarová A., Kuneš P., Hadincová V., Krak K., Zákravský P. Mandák B: Migration patterns of subgenus Alnus in Europe since the Last Glacial Maximum. A systematic review. PLoS ONE. 2014;9:e88709. doi: 10.1371/journal.pone.0088709. PubMed DOI PMC

Havrdová A., Douda J., Krak K., Vít P., Hadincová V., Zákravský P., Mandák B. Higher genetic diversity in recolonized areas than in refugia of Alnus glutinosa triggered by continent-wide lineage admixture. Mol. Ecol. 2015;24:4759–4777. doi: 10.1111/mec.13348. PubMed DOI

Mandák B., Vít P., Krak K., Trávníček P., Havrdová A., Hadincová V., Zákravský P., Jarolímová V., Bacles C.F.E., Douda J. Flow cytometry, microsatellites and niche models reveal the origins and geographical structure of Alnus glutinosa populations in Europe. Ann. Bot. 2016;117:107–120. doi: 10.1093/aob/mcv158. PubMed DOI PMC

Vít P., Douda J., Krak K., Havrdová A., Mandák B. Two new polyploid species closely related to Alnus glutinosa in Europe and North Africa—An analysis based on morphometry, karyology, flow cytometry and microsatellites. Taxon. 2017;66:567–583. doi: 10.12705/663.4. DOI

Šmíd J., Vít P., Douda J., Krak K., Mandák B. Distribution, hybridisation and morphological variation of Alnus rohlenae (Betulaceae) an endemic species of the Balkan Peninsula. Eur. J. For. Res. under review.

Korpelainen H. The evolutionary processes of mitochondrial and chloroplast genomes differ from those of nuclear genomes. Naturwissenschaften. 2004;91:505–518. doi: 10.1007/s00114-004-0571-3. PubMed DOI

Schönswetter P., Lachmayer M., Lettner C., Prehsler D., Rechnitzer S., Reich D.S., Sonnleitner M., Wagner I., Hülber K., Schneeweiss G.M., et al. Sympatric diploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps are separated along an altitudinal gradient. J. Plant Res. 2007;120:721–725. doi: 10.1007/s10265-007-0108-x. PubMed DOI

Doležel J., Greilhuber J., Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2007;2:2233–2244. doi: 10.1038/nprot.2007.310. PubMed DOI

Shaw J., Lickey E.B., Schilling E.E., Small R.L. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am. J. Bot. 2007;94:275–288. doi: 10.3732/ajb.94.3.275. PubMed DOI

Drašnarová A., Krak K., Vít P., Doudová J., Douda J., Hadincová V., Zákravský P., Mandák B. Cross-amplification and multiplexing of SSR markers for Alnus glutinosa and A. incana. Tree Genet. Genomes. 2014;10:865–873. doi: 10.1007/s11295-014-0727-z. DOI

Lepais O., Bacles C.F.E. De novo discovery and multiplexed amplification of microsatellite markers for black alder (Alnus glutinosa) and related species using SSR-enriched shotgun pyrosequencing. J. Hered. 2011;102:627–632. doi: 10.1093/jhered/esr062. PubMed DOI

Gosling P.G., McCartan S.A., Peace A.J. Seed dormancy and germination characteristics of common alder (Alnus glutinosa L.) indicate some potential to adapt to climate change in Britain. Int. J. For. Res. 2009;82:573–582. doi: 10.1093/forestry/cpp024. DOI

Hall T.A. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999;41:95–98.

Villesen P. FaBox: An online Fasta Sequence Toolbox. [(accessed on 5 July 2019)];2007 Available online: http://www.birc.au.dk/software/fabox.

Ingvarsson P., Ribstein S., Taylor D. Molecular evolution of insertions and deletion in the chloroplast genome of Silene. Mol. Biol. Evol. 2003;20:1737–1740. doi: 10.1093/molbev/msg163. PubMed DOI

Simmons M.P., Ochoterena H. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 2000;49:369–381. doi: 10.1093/sysbio/49.2.369. PubMed DOI

Müller K. SeqState: Primer design and sequence statistics for phylogenetic DNA datasets. Appl. Bioinform. 2005;4:65–69. doi: 10.2165/00822942-200504010-00008. PubMed DOI

Swofford D.L. PAUP* Version 4.0 b10. Phylogenetic Analysis Using Parsimony (* and Other Methods) Sinauer; Sunderland, MA, USA: 2002.

Ronquist F., Huelsenbeck J.P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI

Nylander J.A.A. MrModeltest v2. Evolutionary Biology Centre, Uppsala University; Uppsala, Sweden: 2004. Program Distributed by the Author.

Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C.-H., Xie N., Suchard M.A., Rambaut A., Drummond A.J. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLOS Comput. Biol. 2014;10:e1003537. doi: 10.1371/journal.pcbi.1003537. PubMed DOI PMC

Drummond A.J., Rambaut A. Beast: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007;7:214. doi: 10.1186/1471-2148-7-214. PubMed DOI PMC

Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed Phylogenetics and Dating with Confidence. PLoS Biol. 2006;4:e88. doi: 10.1371/journal.pbio.0040088. PubMed DOI PMC

Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901. doi: 10.1093/sysbio/syy032. PubMed DOI PMC

Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 1978;89:583–590. PubMed PMC

Hardy O.J., Vekemans X. SPAGeDi: A versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes. 2002;2:618–620. doi: 10.1046/j.1471-8286.2002.00305.x. DOI

Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC

Clark L.V., Jasieniuk M. POLYSAT: An R package for polyploid microsatellite analysis. Mol. Ecol. Resour. 2011;11:526–566. doi: 10.1111/j.1755-0998.2011.02985.x. PubMed DOI

R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2014. [(accessed on 20 June 2019)]; Available online: http://www.R-project.org/

Earl D.A., von Holdt B.M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 2012;4:359–361. doi: 10.1007/s12686-011-9548-7. DOI

Nordborg M., Hu T.T., Ishino Y., Jhaveri J., Toomajian C., Zheng H., Bakker E., Calabrese P., Gladstone J., Goyal R., et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 2005;3:e196. doi: 10.1371/journal.pbio.0030196. PubMed DOI PMC

Jakobsson M., Rosenberg N.A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:1801–1806. doi: 10.1093/bioinformatics/btm233. PubMed DOI

Rosenberg N.A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes. 2004;4:137–138. doi: 10.1046/j.1471-8286.2003.00566.x. DOI

Anderson E.C., Thompson E.A. A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002;160:1217–1229. PubMed PMC

Hothorn T., Kneib T., Bühlmann P. Conditional transformation models by example. In: Muggeo V.M.R., Capursi V., Boscaino G., Lovison G., editors. Proceedings of the 28th International Workshop on Statistical Modelling, 8–12 July 2013. Universitá Degli Studi Di Palermo; Palermo, Italy: 2013. pp. 15–26.

Burton T.L., Husband B.C. Fecundity and offspring ploidy in matings among diploid, triploid and tetraploid Chamerion angustifolium (Onagraceae): Consequences for tetraploid establishment. Heredity. 2001;87:573–582. doi: 10.1046/j.1365-2540.2001.00955.x. PubMed DOI

Ramsey J., Schemske D.W. Pathways, mechanisms, and rates of polyploidy formation in flowering plants. Annu. Rev. Ecol. Syst. 1998;29:467–501. doi: 10.1146/annurev.ecolsys.29.1.467. DOI

Anamthawat-Jónsson K., Thórsson A.T. Natural hybridisation in birch: Triploid hybrids between Betula nana and B. pubescens. Plant Cell Tiss. Org. 2003;75:99–107. doi: 10.1023/A:1025063123552. DOI

Fehrer J., Krahulcová A., Krahulec F., Chrtek J., Jr., Rosen-Baumová R., Bräutigam S. Evolutionary as-pects in Hieracium subgenus Pilosella. In: Hörandl E., Grossniklaus U., van Dijk P., Sharbel T., editors. Apomixis: Evolution, Mechanisms and Perspectives. Koeltz Scientific Books; Königstein, Germany: 2007. Regnum Vegetabile 147.

Thórsson Ć.T., Pálsson S., Lascoux M., Anamthawat-Jónsson K. Introgression and phylogeography of Betula nana (diploid), B. pubescens (tetraploid) and their triploid hybrids in Iceland inferred from cpDNA haplotype variation. J. Biogeogr. 2010;37:2098–2110. PubMed

Krahulec F., Krahulcová A., Hlaváček R. Rare hybrid swarm of Pilosella polymastix × P. officinarum: Cytotype structure and modes of reproduction. Preslia. 2014;86:179–192.

Rieseberg L.H., Soltis D.E. Phylogenetic consequences of cytoplasmic gene flow in plants. Evol. Trends Plants. 1991;5:65–84.

Soltis D.E., Kuzoff R.K. Discordance between nuclear and chloroplast phylogenies in the Heuchera group (Saxifragaceae) Evolution. 1995;49:727–742. doi: 10.1111/j.1558-5646.1995.tb02309.x. PubMed DOI

Fehrer J., Gemeinholzer B., Chrtek J., Jr., Bräutigam S. Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae) Mol. Phylogenet. Evol. 2007;42:347–361. doi: 10.1016/j.ympev.2006.07.004. PubMed DOI

Aleza P., Juárez J., Cuenca J., Ollitrault P., Navarro L. Recovery of citrus triploid hybrids by embryo rescue and flow cytometry from 2x × 2x sexual hybridisation and its application to extensive breeding programs. Plant Cell Rep. 2010;29:1023–1034. doi: 10.1007/s00299-010-0888-7. PubMed DOI

Roe A.D., MacQuarrie C.J., Gros-Louis M.C., Simpson J.D., Lamarche J., Beardmore T., Thompson S.L., Tanguay P., Isabel N. Fitness dynamics within a poplar hybrid zone: I. Prezygotic and postzygotic barriers impacting a native poplar hybrid stand. Ecol. Evol. 2014;4:1629–1647. doi: 10.1002/ece3.1029. PubMed DOI PMC

Arnold M.L., Bennett B.D. Natural hybridization in Louisiana irises: Genetic variation and ecological determinants. In: Harrison R.G., editor. Hybrid Zones and the Evolutionary Process. Oxford University Press; Oxford, UK: 1993. pp. 115–139.

Cruzan M.B. Evolutionary Biology: A Plant Perspective. Oxford University Press; New York, NY, USA: 2018. p. 537.

Brennan A.C., Bridle J.R., Wang A.L., Hiscock S.J., Abbott R.J. Adaptation and selection in the Senecio (Asteraceae) hybrid zone on Mount Etna, Sicily. New Phytol. 2009;183:702–717. doi: 10.1111/j.1469-8137.2009.02944.x. PubMed DOI

Haque M.M., Diez J.J. Susceptibility of common alder (Alnus glutinosa) seeds and seedlings to Phytophthora alni and other Phytophthora species. For. Syst. 2012;21:313–322. doi: 10.5424/fs/2012212-02267. DOI

Štochlová P., Novotná K., Černý K. Factors affecting the development of Phytophthora alni ssp. alni in Alnus glutinosa L. . J. For. Sci. 2012;58:123–130.

McVean D.N. Ecology of Alnus glutinosa (L.) Gaertn.: I. Fruit formation. J. Ecol. 1955;43:46–61. doi: 10.2307/2257118. DOI

Ashcroft M.B., French K.O., Chisholm L.A. An evaluation of environmental factors affecting species distributions. Ecol. Model. 2011;222:524–531. doi: 10.1016/j.ecolmodel.2010.10.003. DOI

Yang X.H., Yang J.H., Luo C.J. Review and prospect of mulberry polyploidy breeding. Agric. Sci. Zhejiang. 2000;6:304–306.

Aleza P., Juárez J., Ollitrault P., Navarro L. Production of tetraploid plants of non-apomictic citrus genotypes. Plant Cell Rep. 2009;28:1837–1846. doi: 10.1007/s00299-009-0783-2. PubMed DOI

Aleza P., Juárez J., Cuenca J., Ollitrault P., Navarro L. Extensive citrus triploid hybrid production by 2x × 4x sexual hybridizations and parent-effect on the length of the juvenile phase. Plant Cell Rep. 2012;31:1723–1735. doi: 10.1007/s00299-012-1286-0. PubMed DOI

Gramlich S., Hörandl E. Fitness of natural willow hybrids in a pioneer mosaic hybrid zone. Ecol. Evol. 2016;6:7645–7655. doi: 10.1002/ece3.2470. PubMed DOI PMC

Henry I.M., Dilkes B.P., Young K., Watson B., Wu H., Comai L. Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics. 2005;170:1979–1988. doi: 10.1534/genetics.104.037788. PubMed DOI PMC

Henry I.M., Dilkes B.P., Tyagi A.P., Lin H.Y., Comai L. Dosage and parent-of-origin effects shaping aneuploid swarms in A. thaliana. Heredity. 2009;103:458–468. doi: 10.1038/hdy.2009.81. PubMed DOI

Duszynska D., Vilhjálmsson B.J., Bravo R.C., Swamidatta S., Juenger T.E., Donoghue M.T.A., Comte A., Nordborg M., Sharbel T.F., Brychkova G., et al. Transgenerational effects of inter-ploidy cross direction on reproduction and F2 seed development of Arabidopsis thaliana F1 hybrid triploids. Plant Reprod. 2019;32:275–289. doi: 10.1007/s00497-019-00369-6. PubMed DOI PMC

Slatkin M. Gene flow and selection in a two-locus system. Genetics. 1975;81:787–802. PubMed PMC

Felber-Girard M., Felber F., Buttler A. Habitat differentiation in a narrow hybrid zone between diploid and tetraploid Anthoxanthum alpinum. New Phytol. 1996;133:531–540. doi: 10.1111/j.1469-8137.1996.tb01921.x. DOI

Hewitt G.M. Hybrid zones—Natural laboratories for evolutionary studies. Trends Ecol. Evol. 1988;3:158–167. doi: 10.1016/0169-5347(88)90033-X. PubMed DOI

Janes J.K., Hamilton J.A. Mixing it up: The role of hybridization in forest management and conservation under climate change. For. Trees Livelihoods. 2017;8:237. doi: 10.3390/f8070237. DOI

Wielstra B., Burke T., Butlin R.K., Avcı A., Üzüm N., Bozkurt E., Olgun K., Arntzen J.W. A genomic footprint of hybrid zone movement in crested newts. Evol. Lett. 2017;1:93–101. doi: 10.1002/evl3.9. PubMed DOI PMC

Sobel J.M., Streisfeld M.A. Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus. Evolution. 2015;69:447–461. doi: 10.1111/evo.12589. PubMed DOI

Stankowski S., Chase M.A., Fuiten A.M., Ralph P.L. The tempo of linked selection: Emergence of a heterogeneous genomic landscape during a recent radiation of monkey flowers. PLoS ONE. 2018:e1002112

Szymura J.M., Barton N.H. Genetic analysis of a hybrid zone between the fire-bellied toads Bombina bombina and B. variegata, near Cracow in Southern Poland. Evolution. 1986;40:1141–1159. PubMed

Arntzen J.W., Abrahams C., Meilink W.R., Iosif R., Zuiderwijk A. Amphibian decline, pond loss and reduced population connectivity under agricultural intensification over a 38 year period. Biodivers. Conserv. 2017;26:1411–1430. doi: 10.1007/s10531-017-1307-y. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace