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Discordant mtDNA and cpDNA phylogenies indicate geographic speciation and reticulation as driving factors for the diversification of the genus Picea

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Abstract

The phylogeny of the genus Picea was investigated by sequencing three loci from the paternally inherited chloroplast genome (trnK, rbcL and trnTLF) and the intron 2 of the maternally transmitted mitochondrial gene nad1 for 35 species. Significant topological differences were found between the trnK tree and the rbcL and trnTLF phylogenetic trees, and between cpDNA and mtDNA phylogenies. None of the phylogenies matched morphological classifications. The mtDNA phylogeny was geographically more structured than cpDNA phylogenies, reflecting the different inheritance of the two cytoplasmic genomes in the Pinaceae and their differential dispersion by seed only and seed and pollen, respectively. Most North American taxa formed a monophyletic group on the mtDNA tree, with topological patterns suggesting geographic speciation by range fragmentation or by dispersal and isolation. Similar patterns were also found among Asian taxa. Such a trend towards geographic speciation is anticipated in other Pinaceae genera with similar life history, autecology and reproductive system. Incongruences between organelle phylogenies suggested the occurrence of mtDNA capture by invading cpDNA. Incongruences between cpDNA partitions further suggested heterologous recombination presumably also linked to ancient reticulate evolution. Whilst cpDNA appears potentially valuable for molecular taxonomy and systematics purposes, these results emphasize the reduced value of cpDNA to infer vertical descent and the speciation history for plants with paternal transmission and high dispersal of their chloroplast genome.

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Acknowledgements

The authors thank T. Ward and J. Li (Arnold Arboretum, Boston, Massachusetts), E. Johnson (Holden Arboretum, Kirtland, Ohio), M. Chase and L. Csiba (Royal Botanic Garden, Kew, UK), F.T. Ledig (Univ. of California at Davis, Institute of Forest Genetics, USDA), J. Beaulieu and M. Deslauriers (Canadian Forest Service, Québec City), E. Morin (Botanical Garden of Montréal, Québec), D. Simpson and B. Daigle (National Tree Seed Centre, Fredericton, New Brunswick), P. Brownless (Royal Botanic Gardens, Edinburgh, UK), and S. Toomer (Westonbirt National Arboretum, Tetbury, UK) for providing plant materials; M. Lamothe and N. Tremblay (Canada Research Chair in Forest Genomics, Univ. Laval) for support in the laboratory; F. Larochelle, S. Larose and J. Laroche (Center for Bioinformatics and Computational Biology, Univ. Laval) for help with software and their analytical advices; S. González-Martínez and several reviewers for their constructive comments; and the Natural Sciences and Engineering Research Council of Canada for financial support.

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  1. Canada Research Chair in Forest and Environmental Genomics, Centre for Forest Research and Institute for Integrative and Systems Biology, Université Laval, Québec, Québec, Canada, G1V 0A6

    Marie Bouillé, Sauphie Senneville & Jean Bousquet

  2. Pavillon Charles-Eugène-Marchand, Université Laval, Québec, Québec, Canada, G1V 0A6

    Jean Bousquet

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  1. Marie Bouillé
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Communicated by S. González-Martínez

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Figure S1

Position of PCR primers designed in this study to amplify the mitochondrial nad1 intron 2 (JPEG 1 873 kb)

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Bouillé, M., Senneville, S. & Bousquet, J. Discordant mtDNA and cpDNA phylogenies indicate geographic speciation and reticulation as driving factors for the diversification of the genus Picea . Tree Genetics & Genomes 7, 469–484 (2011). https://doi.org/10.1007/s11295-010-0349-z

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