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MBE Advance Access published online on September 22, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl131
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted September 19, 2006

Research Article

Fossil Calibration of Molecular Divergence Infers a Moderate Mutation Rate and Recent Radiations for Pinus

Willyard Ann 1, John Syring 2, David S. Gernandt 3, Aaron Liston 1, and Richard Cronn 4 *

1 Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331 USA
2 Department of Biological and Physical Sciences, Montana State University, 1500 University Drive, Billings, MT 59101
3 Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Apartado Postal 1-69 Plaza Juárez, Pachuca, Hidalgo 42001, Mexico
4 Pacific Northwest Research Station, USDA Forest Service, 3200 SW Jefferson Way, Corvallis, OR 97331 USA

* To whom correspondence should be addressed.
Richard Cronn, E-mail: rcronn{at}fs.fed.us


  Abstract

Silent mutation rate estimates for Pinus vary 50-fold, ranging from angiosperm-like to among the slowest reported for plants. These differences either reflect extraordinary genomic processes or inconsistent fossil calibration, and they have important consequences for population and biogeographical inferences. Here we estimate mutation rates from four Pinus species that represent the major lineages using eleven nuclear and four chloroplast loci. Calibration was tested at the divergence of Pinus subgenera with the oldest leaf fossil from subg. Strobus (Eocene; 45 MYA) or a recently published subg. Strobus wood fossil (Cretaceous; 85 MYA). These calibrations place the origin of Pinus 190-102 MYA, and give absolute silent rate estimates of 0.70-1.31 x 10-9 and 0.22-0.42 x 10-9·site-1·year-1 for the nuclear and chloroplast genomes, respectively. These rates are approximately four- to 20-fold slower than angiosperms, but unlike many previous estimates, they are more consistent with the high per-generation deleterious mutation rates observed in pines. Chronograms from nuclear and chloroplast genomes show that the divergence of subgenera accounts for about half of the time since Pinus diverged from Picea, with subsequent radiations occurring more recently. By extending the sampling to encompass the phylogenetic diversity of Pinus, we predict that most extant subsections diverged during the Miocene. Moreover, subsections Australes, Ponderosae, and Contortae, containing over 50 extant species, radiated within a 5 MY time span starting as recently as 18 MYA. An Eocene divergence of pine subgenera (using leaf fossils) does not conflict with fossil-based estimates of the Pinus-Picea split, but a Cretaceous divergence using wood fossils accommodates Oligocene fossils that may represent modern subsections. Since homoplasy and polarity of character states have not been tested for fossil pine assignments, the choice of fossil and calibration node represents a significant source of uncertainty. Based on several lines of evidence (including agreement with ages inferred using calibrations outside of Pinus), we conclude that the 85 MYA calibration at the divergence of pine subgenera provides a reasonable lower bound and that further refinements in age and mutation rate estimates will require a synthetic examination of pine fossil history.

Keywords: Molecular evolution; Pinus; silent substitution rates; chronogram; fossils.
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