Evaluating the Impact of Genomic Data and Priors on Bayesian Estimates of the Angiosperm Evolutionary Timescale

Abstract

The evolutionary timescale of angiosperms has long been a key question in biology. Molecular estimates of this timescale have shown considerable variation, being influenced by differences in taxon sampling, gene sampling, fossil calibrations, evolutionary models, and choices of priors. Here, we analyze a data set comprising 76 protein-coding genes from the chloroplast genomes of 195 taxa spanning 86 families, including novel genome sequences for 11 taxa, to evaluate the impact of models, priors, and gene sampling on Bayesian estimates of the angiosperm evolutionary timescale. Using a Bayesian relaxed molecular-clock method, with a core set of 35 minimum and two maximum fossil constraints, we estimated that crown angiosperms arose 221 (251-192) Ma during the Triassic. Based on a range of additional sensitivity and subsampling analyses, we found that our date estimates were generally robust to large changes in the parameters of the birth-death tree prior and of the model of rate variation across branches. We found an exception to this when we implemented fossil calibrations in the form of highly informative gamma priors rather than as uniform priors on node ages. Under all other calibration schemes, including trials of seven maximum age constraints, we consistently found that the earliest divergences of angiosperm clades substantially predate the oldest fossils that can be assigned unequivocally to their crown group. Overall, our results and experiments with genome-scale data suggest that reliable estimates of the angiosperm crown age will require increased taxon sampling, significant methodological changes, and new information from the fossil record. [Angiospermae, chloroplast, genome, molecular dating, Triassic.].

The Emergence of Earliest Angiosperms May be Earlier than Fossil Evidence Indicates

“…Our age estimates, emerging from multiple calibration sets, converge on an age of extant angiosperm origin in the mid Permian (mean ages of individual analyses 294–257 mya). Such a time estimate is controversial, but is consistent with, or only slightly older than, other recent, fossil-only constraint molecular dating results such as 242 mya for a relaxed analysis (Magallón and Castillo 2009), 275–215 mya (Magallón 2010), 240–175 (Clarke et al 2011), 240–225 mya (Zeng et al 2014), or 251–192 (Foster et al 2017). Interestingly, all these ages are significantly older than the angiosperm fossil record (Friis et al 2011).…”

“…represents the sister group to all other extant angiosperms (Amborella Genome Project 2013), no fossils can be placed near this key divergence. Most of the estimates for this date using molecular data fall in the 250–145 mya range (Bell et al 2010; Magallón 2010; Moore et al 2007; Smith et al 2010; Foster et al 2017). Hence, calculated ages are considerably older than the oldest accepted angiosperm fossils of about 130 mya (Friis et al 2011).…”

“…Hence, calculated ages are considerably older than the oldest accepted angiosperm fossils of about 130 mya (Friis et al 2011). The age of the earliest angiosperm lineages remains hotly debated (Buerki et al 2014; Doyle and Endress 2014; Magallón 2014; Beaulieu et al 2015; Magallón et al 2015; Foster et al 2017; Herendeen et al 2017). …”

Was Charles Darwin right in his explanation of the ‘abominable mystery’?

“…The reconstruction of the genome of the most recent common angiosperm ancestor suggests an age of 214 Ma for its appearance (Murat et al 2017). By contrast, reliable angiosperm fossil records older than 130-140 Ma have been not found so far (Doyle 2012;Foster et al 2017, Herendeen et al 2017. Even though the lack of fossil records before the early Cretaceous suggested to several scholars that angiosperms must have undergone extremely fast evolution early in their history, Cascales-Miñana et al (2016) argued that for 100 million years of their evolutionary history angiosperms remained relatively rare, maybe growing in habitats poorly represented in the fossil records.…”

“…The age estimates of the divergence of crown group angiosperms using molecular clock data vary considerably, between 140 and 240 Ma or earlier (Martin et al 1989a,b;Soltis and Soltis 2004;Moore et al 2007;Bell et al 2010;Silvestro et al 2014;Foster et al 2017). The reconstruction of the genome of the most recent common angiosperm ancestor suggests an age of 214 Ma for its appearance (Murat et al 2017).…”