Dealing with discordant genetic signal caused by hybridisation, incomplete lineage sorting and paucity of primary nucleotide homologies: a case study of closely related members of the genus Picris subsection Hieracioides (Compositae)

. 2014 ; 9 (9) : e104929. [epub] 20140905

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25192431

We investigated genetic variation and evolutionary history of closely related taxa of Picris subsect. Hieracioides with major focus on the widely distributed P. hieracioides and its closely related congeners, P. hispidissima, P. japonica, P. olympica, and P. nuristanica. Accessions from 140 sample sites of the investigated Picris taxa were analyzed on the infra- and the inter-specific level using nuclear (ITS1-5.8S-ITS2 region) and chloroplast (rpl32-trnL(UAG) region) DNA sequences. Genetic patterns of P. hieracioides, P. hispidissima, and P. olympica were shown to be incongruent and, in several cases, both plastid and nuclear alleles transcended borders of the taxa and genetic lineages. The widespread P. hieracioides was genetically highly variable and non-monophyletic across both markers, with allele groups having particular geographic distributions. Generally, all gene trees and networks displayed only a limited and statistically rather unsupported resolution among ingroup taxa causing their phylogenetic relationships to remain rather unresolved. More light on these intricate evolutionary relationships was cast by the Bayesian coalescent-based analysis, although some relationships were still left unresolved. A combination of suite of phylogenetic analyses revealed the ingroup taxa to represent a complex of genetically closely related and morphologically similar entities that have undergone a highly dynamic and recent evolution. This has been especially affected by the extensive and recurrent gene flow among and within the studied taxa and/or by the maintenance of ancestral variation. Paucity of phylogenetically informative signal further hampers the reconstruction of relationships on the infra- as well as on the inter-specific level. In the present study, we have demonstrated that a combination of various phylogenetic analyses of datasets with extremely complex and incongruent phylogenetic signal may shed more light on the interrelationships and evolutionary history of analysed species groups.

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Comes HP, Abbott RJ (2001) Molecular phylogeny, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution 55: 1943–1962. PubMed

Nieto Feliner G, Gutiérrez Larena B, Fuertes Aguilar J (2004) Fine-scale geographical structure, intra-individual polymorphism and recombination in nuclear ribosomal internal transcribed spacers in Armeria (Plumbaginaceae). Ann Bot (Oxford) 93: 189–200. PubMed PMC

Willyard A, Cronn R, Liston A (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Molec Phylogen Evol 52: 498–511. PubMed

Schmidt-Lebuhn AN, de Vos JM, Keller B, Conti E (2012) Phylogenetic analysis of Primula section Primula reveals rampant non-monophyly among morphologically distinct species. Molec Phylogen Evol 65: 23–34. PubMed

Yu WB, Huang PH, Li DZ, Wang H (2013) Incongruence between nuclear and chloroplast DNA phylogenies in Pedicularis section Cyathophora (Orobanchaceae). PLoS ONE, doi: 10.1371/journal.pone.0074828 PubMed PMC

Rieseberg LH (1997) Hybrid origins of plant species. Ann Rev Ecol Syst 28: 359–389.

Wendel JF, Doyle J (1998) Phylogenetic incongruence: Window into genome history and molecular evolution. In: Soltis D, Soltis P, Doyle J, editors.Molecular systematics of plants II: DNA sequencing. Kluwer, Boston, USA. pp. 265–296.

Linder CR, Rieseberg LH (2004) Reconstructing patterns of reticulate evolution in plants. Amer J Bot 91: 1700–1708. PubMed PMC

Joly S, McLenachan PA, Lockhart PJ (2009) A statistical approach for distinguishing hybridisation and incomplete lineage sorting. Amer Nat 174: 54–70. PubMed

Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Rev Ecol Evol Syst 34: 397–423.

Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction in plants. Austral Syst Bot 17: 145–170.

Holland BR, Benthin S, Lockhart PJ, Moulton V, Huber KT (2008) Using supernetworks to distinguish hybridisation from lineage-sorting. BMC Evol Biol 8: 202. PubMed PMC

Yu Y, Than C, Degnan JH, Nakhleh L (2011) Coalescent histories on phylogenetic networks and detection of hybridisation despite incomplete lineage sorting. Syst Biol 60: 138–149. PubMed PMC

Wiens JJ, Hollingsworth BD (2000) War of the iguanas: Conflicting molecular and morphological phylogenies and long-branch attraction in iguanid lizards. Syst Biol 49: 143–159. PubMed

Duvall MR, Ervin AB (2004) 18S gene trees are positively misleading for monocot/dicot phylogenetics. Molec Phylogen Evol 30: 97–106. PubMed

van der Niet T, Linder HP (2008) Dealing with incongruence in the quest for the species tree: a case study from the orchid genus Satyrium . Molec Phyl Evol 47: 154–174. PubMed

Frajman B, Eggens F, Oxelman B (2009) Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae) - A multigene phylogenetic approach with relative dating. Syst Biol 58: 328–345. PubMed

Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Molec Biol Evol 27: 570–580. PubMed PMC

Kubatko L, Carstens B, Knowles L (2009) STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics 25: 971–973. PubMed

Joly S (2012) JML: testing hybridization from species trees. Molec Ecol Res 12: 179–184. PubMed

Lack HW (1974)Die Gattung Picris L. sensu lato im ostmediterran–westasiatischen Raum. PhD thesis, University of Vienna, Austria. 184 p.

Slovák M, Marhold K (2007) Morphological evaluation of Picris hieracioides L. (Compositae) in Slovakia. Phyton (Horn) 47: 73–102.

Slovák M, Urfus T, Vít P, Marhold K (2009) Balkan endemic Picris hispidissima (Compositae): Morphology, DNA content and relationship to polymorphic P. hieracioides . Pl Syst Evol 278: 178–201.

Slovák M, Kučera J, Marhold K, Zozomová-Lihová J (2012) The morphological and genetic variation in the polymorphic species Picris hieracioides (Compositae, Lactuceae) in Europe strongly contrasts with traditional taxonomical concepts. Syst Bot 21: 258–278.

Lack HW (1979) The genus Picris (Asteraceae, Lactuceae) in Tropical Africa. Pl Syst Evol 131: 35–52.

Samuel R, Gutermann W, Stuessy TF, Ruas CF, Lack HW, et al. (2006) Molecular phylogenetics reveals Leontodon (Asteraceae, Lactuceae) to be diphyletic. Amer J Bot 93: 1193–1205. PubMed

Slovák M, Šingliarová B, Mráz P (2008) Chromosome numbers and mode of reproduction in Picris hieracioides s.l. (Asteraceae) with notes on some other Picris taxa. Nordic J Bot 28: 238–244.

Slovák M, Vít P, Urfus T, Suda J (2009) Complex pattern of genome size variation in a polymorphic member of the Asteraceae. J Biogeogr 36: 372–384.

Lack HW (1975) Picris. In: Davis PH, editor.Flora of Turkey and the East Aegean Islands 5.Edinburgh, UK: University Press. pp. 678–684.

Frajman B, Oxelman B (2007) Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Molec Phylogen Evol 43: 140–155. PubMed

Prentice HC, Malm JU, Hathaway L (2008) Chloroplast DNA variation in the European herb Silene dioica (red campion): postglacial migration and interspecific introgression. Pl Syst Evol 272: 23–37.

Bardy KE, Albach DC, Schneeweiss GM, Fischer MA, Schönswetter P (2010) Disentangling phylogeography, polyploid evolution and taxonomy of a woodland herb (Veronica chamaedrys group, Plantaginaceae s.l.) in southeastern Europe. Molec Phylogen Evol 57: 771–786. PubMed PMC

Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Amer J Bot 94: 275–288. PubMed

Chapman MA, Chang JC, Weisman D, Kesseli RV, Burke JM (2007) Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae). Theor Appl Genet 115: 747–755. PubMed

Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, et al. (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer J Bot 92: 142–166. PubMed

Francisco-Ortega J, Fuertes Aguilar J, Gómez Campo C, Santos-Guerra A, Jansen RK (1999) Internal transcribed spacer sequence phylogeny of Crambe L. (Brassicaceae): Molecular data reveal two old world disjunctions. Molec Phylogen Evol 11: 361–380. PubMed

White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors.PCR Protocols: A Guide to Methods and Applications.New York, USA: Academic Press. pp. 315–322.

Timme R, Kuehl EJ, Boore JK, Jansen RK (2007) A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. Amer J Bot 94: 302–313. PubMed

Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser (Oxford) 41: 95–98.

Fuertes Aguilar J, Nieto Feliner G (2003) Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae). Molec Phylogen Evol 28: 430–447. PubMed

Záveská E, Fér T, Šída O, Krak K, Marhold K, et al. (2012) Phylogeny of Curcuma (Zingiberaceae) based on plastid and nuclear sequences: Proposal of the new subgenus Ecomata . Taxon 61: 747–763.

Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of congruence. Cladistics 10: 315–319.

Swofford DL (2001) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), v. 4.0 beta 10. Sunderland: Sinauer Associates.

Maddison DR, Maddison WP (2000)MacClade4: analysis of phylogeny and character evolution, version 4.0. Sinauer, Sunderland, Massachusetts, USA. 398 p.

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. PubMed

Miller MA, Pfeiffer W, Schwartz T (2010) “Creating the CIPRES Science Gateway for inference of large phylogenetic trees” in Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA : 1–8 pp.

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704. PubMed

Posada D (2008) ModelTest: Phylogenetic Model Averaging. Molec Biol Evol 25: 1253–1256. PubMed

Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molec Biol Evol 23: 254–267. PubMed

Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of the phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619–633. PubMed PMC

Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657–1660. PubMed

Wägelle JW, Rödding F (1998) A priori estimation of phylogenetic information conserved in aligned sequences. Molec Phylogen Evol 9: 358–365. PubMed

Rambaut A, Drummond AJ (2007) Tracer v1.4. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 2014 Jan 21.

Silvestro D, Michalak I (2011) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12: 335–337.

Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51: 492–508. PubMed

Shimodaira H (2008) Testing regions with non-smooth boundaries via multiscale bootstrap. J Stat Plan Inference 138: 1227–1241.

Shimodaira H, Hasegawa M (2001) Consel: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246–1247. PubMed

Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Cambell CS, et al. (1995) The ITS region of nuclear ribosomal DNA: A valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82: 247–277.

Hudson RR (1990) Gene genealogies and the coalescent process. Oxford Surv Evol Biol 7: 1–44.

Jang CG, Müllner AN, Greimler J (2005) Conflicting patterns of genetic and morphological variation in European Gentianella section Gentianella . Bot J Linn Soc 148: 175–187.

Flagel LE, Rapp RA, Grover CE, Widrlechner MP, Hawkins J, et al. (2008) Phylogenetic, morphological, and chemotaxonomic incongruence in the North American endemic genus Echinacea . Amer J Bot 95: 756–765. PubMed

Ramsey J, Robertson A, Husband B (2008) Rapid adaptive divergence in new world Achillea, an autopolyploid complex of ecological races. Evolution 62: 639–653. PubMed

Fuertes Aguilar J, Rosselló JA, Nieto Feliner G (1999) nrDNA concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Mol Ecol 8: 1341–1346. PubMed

Fuertes Aguilar J, Rosselló JA, Nieto Feliner G (1999b) Molecular evidence for the compilospecies model of reticulate evolution in Armeria (Plumbaginaceae). Syst Biol 48: 735–754. PubMed

Baack EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17: 513–518. PubMed PMC

Moody ML, Rieseberg LH (2012) Sorting through the chaff, nDNA gene trees for phylogenetic inference and hybrid identification of annual sunflowers (Helianthus sect. Helianthus). Molec Phylogen Evol 64: 145–155. PubMed

Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogen Evol 29: 417–434. PubMed

Kučera J, Marhold K, Lihová J (2009) Cardamine maritima group (Brassicaceae) in the amphi-Adriatic area: A hotspot of species diversity revealed by DNA sequences and morphological variation. Taxon 59: 148–164.

Koopman WJM (2005) Phylogenetic signal in AFLP data sets. Syst Biol 54: 197–217. PubMed

Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72: 250–259.

Malm JU, Prentice HC (2002) Immigration history and gene dispersal: allozyme variation in Nordic populations of the red campion, Silene dioica (Caryophyllaceae). Biol J Linn Soc 77: 23–34.

Tyler T (2002) Geographical distribution of allozyme variation in relation to post-glacial history in Carex digitata, a widespread European woodland sedge. J Biogeogr 29: 919–930.

Tyler T, Prentice HC, Widén B (2002) Geographic variation and dispersal history in Fennoscandian populations of two forest herbs. Pl Syst Evol 233: 47–64.

Rauscher JT, Doyle JJ, Brown AHD (2002) Internal transcribed spacer repeat-specific primers and the analysis of hybridisation in the Glycine tomentella (Leguminosae) polyploid complex. Mol Ecol 11: 2691–2702. PubMed

Rebernig CA, Schneeweiss GM, Bardy KE, Schönswetter P, Villaseñor JL, et al. (2010) Multiple Pleistocene refugia and Holocene range expansion of an abundant southwestern American desert plant species (Melampodium leucanthum, Asteraceae). Mol Ecol 19: 3421–3443. PubMed

Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B 359: 183–195. PubMed PMC

Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36: 1333–1345.

Kramp K, Huck S, Niketić M, Tomović G, Schmitt T (2009) Multiple glacial refugia and complex postglacial range shifts of the obligatory woodland plant species Polygonatum verticillatum (Convallariaceae). Pl Biol 11: 392–404. PubMed

Huck S, Büdel B, Kadereit JW, Printzen C (2009) Rangewide phylogeography of the European temperate-montane herbaceous plant Meum athamanticum Jacq.: Evidence for periglacial persistence. J Biogeogr 36: 1588–1599.

Rešetnik I, Frajman B, Bogdanović S, Ehrendorfer F, Schönswetter P (2014) Disentangling relationships among the diploid members of the intricate genus Knautia (Caprifoliaceae, Dipsacoideae). Molec Phylogen Evol 74: 97ec P PubMed

Schönswetter P, Solstad H, Garcìa PE, Elven R (2009) A combined molecular and morphological approach to the taxonomically intricate European mountain plant Papaver alpinum s.l. (Papaveraceae) – Taxa or informal phylogeographical groups? Taxon 17: 1326–1343.

Wójcicky JJ (1991) Variability of Prunus fruticosa Pall. and the problem of an anthropohybridisaton. Veröff. Geobot. Inst. ETH, Stiftung Rübel, Zürich 106: 266–272.

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