Evidence of hybrid speciation in the North American primroses Primula suffrutescensP. parryiP. rusbyi and P. angustifolia (Primulaceae)

The genetic structure of tetraploid (4x = 44) North American species of Primula subgenus Auriculastrum: P. suffrutescens, P. parryi, P. rusbyi, and P. angustifolia was analyzed at seven enzyme loci and compared with that of the related diploid P. cuneifolia and P. nipponica. The studied tetraploid species showed fixed or almost fixed heterozygosity at various loci, indicating a hybrid origin. About half of their alleles were shared with Cuneifolia taxa sampled, suggesting that they arose from crosses involving a maternal Cuneifolia-like ancestor. A preliminary survey of their possible paternal species, as inferred from their genotypes, was carried out among different Primula groups. Several paternal alleles expected were observed in subgenus Aleuritia, particularly among taxa of sect. Crystallophlomis (e.g., P. chionantha, P. minor, and P. nivalis xanthobasis). However, none of these taxa proved to be a suitable paternal species. Hybridization events that originated P. suffrutescens, P. parryi, P. rusbyi, and P. angustifolia presumably occurred during Pleistocene secondary contacts in Beringia and involved a maternal Cuneifolia-like ancestor and at least two paternal species, for sect. Suffrutescens and Parryi, respectively. Further studies, involving a genetic survey of Aleuritia taxa from Siberia will be needed to detect such paternal species, if not extinct.

[1]  L. Peruzzi,et al.  Homoploid hybrid speciation in Doronicum L. (Asteraceae)? Morphological, karyological and molecular evidences , 2012 .

[2]  D. Hojsgaard,et al.  The evolution of apomixis in angiosperms: A reappraisal , 2012 .

[3]  M. Arnold,et al.  Natural hybridization as a catalyst of rapid evolutionary change , 2012 .

[4]  G. Feliner,et al.  Concerted Evolution of Multigene Families and Homoeologous Recombination , 2012 .

[5]  G. Hewitt.  Quaternary phylogeography: the roots of hybrid zones , 2011, Genetica.

[6]  J. Kadereit,et al.  The stability of Quaternary speciation: a case study in Primula sect. Auricula , 2011, Alpine Botany.

[7]  M. Chase,et al.  Chalcone synthase variation and phylogenetic relationships in Dactylorhiza (Orchidaceae) , 2010 .

[8]  E. DeChaine,et al.  Contrasting Patterns of Plant Distribution in Beringia , 2010 .

[9]  A. Goncharov,et al.  Phylogenetic relationships in the genus Primula L. (Primulaceae) inferred from the ITS region sequences of nuclear rDNA , 2009, Russian Journal of Genetics.

[10]  Pamela S Soltis,et al.  The role of hybridization in plant speciation. , 2009, Annual review of plant biology.

[11]  Steven Maere,et al.  Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event , 2009, Proceedings of the National Academy of Sciences.

[12]  E. Conti,et al.  Disentangling reticulate evolution in an arctic-alpine polyploid complex. , 2009, Systematic biology.

[13]  Kevin A. Weitemier,et al.  Phylogeny and Biogeography of Primula sect. Parryi (Primulaceae) , 2009, International Journal of Plant Sciences.

[14]  C. Brochmann,et al.  The Arctic – an evolutionary freezer? , 2008 .

[15]  E. DeChaine.  A bridge or a barrier? Beringia's influence on the distribution and diversity of tundra plants , 2008 .

[16]  U. Grossniklaus,et al.  Genomic origin and organization of the allopolyploid Primula egaliksensis investigated by in situ hybridization. , 2008, Annals of botany.

[17]  M. Chase,et al.  Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. , 2008, Annals of botany.

[18]  J. L. Reveal,et al.  Transfer of Dodecatheon to Primula (Primulaceae) , 2008, Brittonia.

[19]  J. Mallet.  Hybrid speciation , 2007, Nature.

[20]  E. Conti,et al.  The primrose path to heterostyly. , 2006, The New phytologist.

[21]  E. Conti,et al.  Are any primroses (Primula) primitively monomorphic? , 2006, The New phytologist.

[22]  D. Soltis,et al.  Rapid Concerted Evolution of Nuclear Ribosomal DNA in Two Tragopogon Allopolyploids of Recent and Recurrent Origin Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY458586, AY458588, AY458589, and AY458587 , 2005, Genetics.

[23]  Inger Greve Alsos,et al.  Polyploidy in arctic plants , 2004 .

[24]  E. Conti,et al.  Buzz-pollinated Dodecatheon originated from within the heterostylous Primula subgenus Auriculastrum (Primulaceae): a seven-region cpDNA phylogeny and its implications for floral evolution. , 2004, American journal of botany.

[25]  G. Hewitt.  Genetic consequences of climatic oscillations in the Quaternary. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  H. Comes,et al.  The Temporal Course of Quaternary Diversification in the European High Mountain Endemic Primula sect. Auricula (Primulaceae) , 2004, International Journal of Plant Sciences.

[27]  M. Hedrén.  Genetic differentiation, polyploidization and hybridization in northern EuropeanDactylorhiza (Orchidaceae): Evidence from allozyme markers , 1996, Plant Systematics and Evolution.

[28]  J. Wendel,et al.  Ribosomal ITS sequences and plant phylogenetic inference. , 2003, Molecular phylogenetics and evolution.

[29]  C. Oberprieler,et al.  A phylogenetic analysis of Primulaceae s.l. based on internal transcribed spacer (ITS) DNA sequence data , 2003, Plant Systematics and Evolution.

[30]  Christian Brochmann,et al.  History and evolution of the arctic flora: in the footsteps of Eric Hultén , 2003, Molecular ecology.

[31]  H. C. Prentice,et al.  Genetic variation in Scandinavian Anthericum liliago (Anthericaceae): allopolyploidy, hybridization and immigration history , 2002, Plant Systematics and Evolution.

[32]  D. Lang,et al.  Phylogenetic Relationships in Primula L. and Related Genera (Primulaceae) Based on Noncoding Chloroplast DNA , 2001, International Journal of Plant Sciences.

[33]  W. Rossi,et al.  Molecular evidence for allopolyploid speciation and a single origin of the western Mediterranean orchid Dactylorhiza insularis (Orchidaceae) , 2001 .

[34]  M. Källersjö,et al.  Generic realignment in primuloid families of the Ericales s.l.: a phylogenetic analysis based on DNA sequences from three chloroplast genes and morphology. , 2000, American journal of botany.

[35]  A. Young,et al.  AUTOTET: a program for analysis of autotetraploid genotypic data. , 2000, The Journal of heredity.

[36]  E. Conti,et al.  Phylogenetic relationships and character evolution in Primula L.: The usefulness of ITS sequence data , 2000 .

[37]  M. Purugganan,et al.  Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications. , 1999, Molecular biology and evolution.

[38]  J. Aguilar,et al.  Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae) , 1999, Molecular ecology.

[39]  K. Ueda,et al.  Further Analysis of Intraspecific Sequence Variation of Chloroplast DNA in Primula cuneifolia Ledeb. (Primulaceae): Implications for Biogeography of the Japanese Alpine Flora , 1999, Journal of Plant Research.

[40]  T. Ranker,et al.  Allopolyploid origin and population genetics of the rare orchid Spiranthes diluvialis. , 1998, American journal of botany.

[41]  B. Glover,et al.  Low genetic diversity in the Scottish endemic Primula scotica Hook. , 1995, The New phytologist.

[42]  D. Crawford.  Enzyme Electrophoresis and Plant Systematics , 1989 .

[43]  G. Stebbins.  The origin and success of polyploids in the boreal circumpolar Flora: A new analysis , 2006 .

[44]  G. Stebbins.  Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach , 1984 .

[45]  L. Gottlieb,et al.  GENETIC AND BIOCHEMICAL CONSEQUENCES OF POLYPLOIDY IN TRAGOPOGON , 1976, Evolution; international journal of organic evolution.

[46]  H. R. Fletcher,et al.  XXII.—The Genus Primula: Sections Cuneifolia, Floribundae, Parryi, and Auricula , 1949, Transactions of the Royal Society of Edinburgh.

[47]  H. R. Fletcher,et al.  XVII.—The Genus Primula: Section Nivales , 1942, Transactions of the Royal Society of Edinburgh.

[48]  H. G. Bruun.  Cytological studies in Primula with special reference to the relation between the karyology and taxonomy of the genus , 1932 .