A Pleistocene inter-tribal allopolyploidization event precedes the species radiation of Pachycladon (Brassicaceae) in New Zealand.

The Southern Alps in New Zealand contain many herbaceous plant groups that have radiated during the Plicoene-Pleistocene. The species in these genera tend to be polyploid relative to their overseas close relatives, an observation of much interest given that hybridization and allopolyploidy have recently been suggested as a possible stimulus for adaptive radiation. We were interested to determine whether or not allopollyploidy was a feature of Pachycladon, a genus which is hypothesised to have adaptively diversified onto different geological substrates in the mountains of the South Island of New Zealand. Phylogenetic analyses of five single-copy nuclear genes show that Pachycladon species have two copies of each gene representing two highly diverged evolutionary lineages from the Brassicaceae. Molecular clock analyses of all loci suggest that the two genome copies in Pachycladon diverged 8 million years ago, and that the allopolyploid origin of the genus occurred during the Pleistocene between 1.6 and 0.8 million years ago. This hybridization event at the origin of the Pachycladon radiation is perhaps the most extreme example yet reported of successful hybridization between distantly related parents.

[1]  Charles James Nice Bailey,et al.  Toward a global phylogeny of the Brassicaceae. , 2006, Molecular biology and evolution.

[2]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[3]  Pamela S Soltis,et al.  Rate heterogeneity among lineages of tracheophytes: Integration of molecular and fossil data and evidence for molecular living fossils , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  T. Sang,et al.  Speciation through homoploid hybridization between allotetraploids in peonies (Paeonia) , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. Wendel,et al.  Evolutionary dynamics of Waxy and the origin of hexaploid Spartina species (Poaceae). , 2007, Molecular phylogenetics and evolution.

[6]  P. Lockhart,et al.  Transcriptional and biochemical signatures of divergence in natural populations of two species of New Zealand alpine Pachycladon , 2008, Molecular ecology.

[7]  B. Grant,et al.  High Survival of Darwin's Finch Hybrids: Effects of Beak Morphology and Diets , 1996 .

[8]  Phylogenetic relationships of Pachycladon (Brassicaceae) species based on three nuclear and two chloroplast DNA markers , 2006 .

[9]  F. Delsuc,et al.  Relaxed Molecular Clock Provides Evidence for Long-Distance Dispersal of Nothofagus (Southern Beech) , 2005, PLoS biology.

[10]  E. Kellogg,et al.  Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview , 2006, Plant Systematics and Evolution.

[11]  Patrick J Biggs,et al.  An approach to transcriptome analysis of non-model organisms using short-read sequences. , 2008, Genome informatics. International Conference on Genome Informatics.

[12]  T. Mitchell-Olds,et al.  Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. , 2001, American journal of botany.

[13]  R. Lewontin,et al.  HYBRIDIZATION AS A SOURCE OF VARIATION FOR ADAPTATION TO NEW ENVIRONMENTS , 1966, Evolution; international journal of organic evolution.

[14]  J. Felsenstein Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[15]  A. Mitchell,et al.  Molecular systematics of the New Zealand Pachycladon (Brassicaceae) complex: Generic circumscription and relationships to Arabidopsis sens. lat. and Arabis sens. lat. , 2002 .

[16]  J. Doyle,et al.  A phylogenetic analysis of tribe Areceae (Arecaceae) using two low-copy nuclear genes , 2002, Plant Systematics and Evolution.

[17]  J. Doyle,et al.  Testing the polyploid past of soybean using a low-copy nuclear gene--is Glycine (Fabaceae: Papilionoideae) an auto- or allopolyploid? , 2006, Molecular phylogenetics and evolution.

[18]  K. Hokamp,et al.  A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. , 2003, Genome research.

[19]  C. Damgaard,et al.  Maternal Inheritance of Chloroplasts between Brassica rapa and F1-hybrids Demonstrated by cpDNA Markers Specific to Oilseed Rape and B. rapa , 2005, Molecular Breeding.

[20]  N. Barton The role of hybridization in evolution , 2001, Molecular ecology.

[21]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[22]  R. Bicknell,et al.  An artificial intergeneric hybrid derived from sexual hybridization between the distantly related Arabidopsis thaliana and Pachycladon cheesemanii (Brassicaceae) , 2008 .

[23]  K. Schierenbeck,et al.  Hybridization as a stimulus for the evolution of invasiveness in plants? , 2006, Euphytica.

[24]  M. Pérez‐Losada,et al.  Unraveling the evolutionary radiation of the thoracican barnacles using molecular and morphological evidence: a comparison of several divergence time estimation approaches. , 2004, Systematic biology.

[25]  S. Otto,et al.  Polyploid incidence and evolution. , 2000, Annual review of genetics.

[26]  A. Ferguson,et al.  Nuclear DNA variation, chromosome numbers and polyploidy in the endemic and indigenous grass flora of New Zealand. , 2005, Annals of botany.

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

[28]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[29]  J. B. Hair Biosystematics of the New Zealand Flora, 1945–1964 , 1966 .

[30]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[31]  T. Mitchell-Olds,et al.  The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. , 2006, Trends in plant science.

[32]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[33]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[34]  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.

[35]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[36]  M. Chapman,et al.  GENETIC DIVERGENCE AND HYBRID SPECIATION , 2007, Evolution; international journal of organic evolution.

[37]  L. Rieseberg,et al.  Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization , 2003, Science.

[38]  Loren H. Rieseberg,et al.  Hybrid Origins of Plant Species , 1997 .

[39]  O. Seehausen Hybridization and adaptive radiation. , 2004, Trends in ecology & evolution.

[40]  P. Heenan,et al.  Systematic Relationships of New Zealand Endemic Brassicaceae Inferred from nrDNA ITS Sequence Data , 2000 .

[41]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[42]  I. Al‐Shehbaz,et al.  Beringia (Brassicaceae), a new genus of arabidopsoid affinities from Russia and North America , 2001 .

[43]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[44]  W. Hollander,et al.  Introgressive Hybridization , 1949, The Yale Journal of Biology and Medicine.

[45]  Wen-Hsiung Li,et al.  Rates of Nucleotide Substitution in Angiosperm Mitochondrial DNA Sequences and Dates of Divergence Between Brassica and Other Angiosperm Lineages , 1999, Journal of Molecular Evolution.

[46]  D. Soltis,et al.  The role of genetic and genomic attributes in the success of polyploids. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[48]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[49]  E. Finnegan Epialleles - a source of random variation in times of stress. , 2002, Current opinion in plant biology.

[50]  S. Joly,et al.  Polyploid and hybrid evolution in roses east of the Rocky Mountains. , 2006, American journal of botany.

[51]  S. Wagstaff,et al.  Evolution of the New Zealand mountain flora: Origins, diversification and dispersal , 2005 .

[52]  J. Doyle,et al.  Phylogenetic utility of the nuclear gene malate synthase in the palm family (Arecaceae). , 2001, Molecular phylogenetics and evolution.

[53]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[54]  P. Heenan,et al.  Phylogeny, biogeography and adaptive radiation of Pachycladon (Brassicaceae) in the mountains of South Island, New Zealand , 2003 .

[55]  Ziheng Yang,et al.  Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene Loci and calibration points, with application to a radiation of cute-looking mouse lemur species. , 2003, Systematic biology.

[56]  M. Arnold Natural Hybridization and Evolution , 1997 .

[57]  I. Al‐Shehbaz,et al.  Generic placement of species excluded from Arabidopsis (Brassicaceae) , 1999 .

[58]  A. Paterson,et al.  Rate variation among nuclear genes and the age of polyploidy in Gossypium. , 2003, Molecular biology and evolution.

[59]  C. Kiefer,et al.  Supernetwork identifies multiple events of plastid trnF(GAA) pseudogene evolution in the Brassicaceae. , 2007, Molecular biology and evolution.

[60]  Steven Maere,et al.  Genome duplication and the origin of angiosperms. , 2005, Trends in ecology & evolution.

[61]  D. Bryant,et al.  A Simple and Robust Statistical Test for Detecting the Presence of Recombination , 2006, Genetics.