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

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 4 Pinus species that represent the major lineages using 11 nuclear and 4 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 0.70-1.31x10(-9) and 0.22-0.42x10(-9).site-1.year-1 for the nuclear and chloroplast genomes, respectively. These rates are approximately 4- 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, subsect. Australes, Ponderosae, and Contortae, containing over 50 extant species, radiated within a 5 Myr 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. Because 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.

Species delimitation and biogeography of two fir species (Abies) in central China: cytoplasmic DNA variation

“…This produced a range of values for u and hence also for t. One caveat is that a slight bias of nucleotide substitution rates for ptDNA may exist in Abies. Thus, the substitution rates used here are only approximate estimates, although they are consistent with estimates reported recently for other conifer species (Willyard et al, 2007;Gugger et al, 2010). An average haplotype sequence length of 1111 bp and a minimum estimate of generation time of 25 years in Pinaceae were used in the calculations (Brown et al, 2004).…”

Distribution of living Cupressaceae reflects the breakup of Pangea

“…Previous studies of gymnosperm radiations mostly have inferred Oligocene-age crown groups (14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26), and a recent meta-analysis found a median crown age for gymnosperm genera of 32 Ma, younger than that found for angiosperm genera (25). Our dating of those genera with more than one species in the Cupressaceae similarly suggests relatively recent diversifications (Fig.…”

Multilocus Patterns of Nucleotide Diversity, Linkage Disequilibrium and Demographic History of Norway Spruce [Picea abies (L.) Karst]

“…Second, estimates of molecular divergence between Pinus and Picea based on an extensive EST database lead to an estimate of the mutation rate of $1 3 10 À9 /year if the divergence time between pine and spruce is that of the diversification of the Pinaceae in the early Cretaceous ($120-140 MYA) (Savolainen and Wright 2004). Finally, Willyard et al (2006) used divergence at multiple nuclear and chloroplast loci, exemplar taxa, and two calibration points to show that divergence times among pine lineages have often been overestimated and, consequently, absolute mutation rates have been underestimated. They obtain a nuclear silent mutation rate in Pinus of 0.70-1.31 3 10 À9 sites/year.…”