A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages

Abstract

Background: Stramenopiles constitute a large and diverse eukaryotic clade that is currently poorly characterized from both phylogenetic and temporal perspectives at deeper taxonomic levels. To better understand this group, and in particular the photosynthetic stramenopiles (Ochrophyta), we analyzed sequence data from 135 taxa representing most major lineages. Our analytical approach utilized several recently developed methods that more realistically model the temporal evolutionary process.

Methodology/principal findings: Phylogenetic reconstruction employed a Bayesian joint rate- and pattern-heterogeneity model to reconstruct the evolutionary history of these taxa. Inferred phylogenetic resolution was generally high at all taxonomic levels, sister-class relationships in particular receiving good statistical support. A signal for heterotachy was detected in clustered portions of the tree, although this does not seem to have had a major influence on topological inference. Divergence time estimates, assuming a lognormally-distributed relaxed molecular clock while accommodating topological uncertainty, were broadly congruent over alternative temporal prior distributions. These data suggest that Ochrophyta originated near the Proterozoic-Phanerozoic boundary, diverging from their sister-taxon Oomycota. The evolution of the major ochrophyte lineages appears to have proceeded gradually thereafter, with most lineages coming into existence by ∼200 million years ago.

Conclusions/significance: The evolutionary timescale of the autotrophic stramenopiles reconstructed here is generally older than previously inferred from molecular clocks. However, this more ancient timescale nevertheless casts serious doubt on the taxonomic validity of putative xanthophyte/phaeophyte fossils from the Proterozoic, which predate by as much as a half billion years or more the age suggested by our molecular genetic data. If these fossils truly represent crown stramenopile lineages, then this would imply that molecular rate evolution in this group proceeds in a fashion that is fundamentally incompatible with the relaxed molecular clock model employed here. A more likely scenario is that there is considerable convergent morphological evolution within Heterokonta, and that these fossils have been taxonomically misdiagnosed.

Figure 1. Consensus tree inferred from the Bayesian joint rate- and pattern-heterogeneity model.

Consensus tree inferred from the Bayesian joint rate- and pattern-heterogeneity model , . Numbers next to each node indicate inferred posterior clade probabilities. Red branches indicate those lineages inferred to having a greater than a 50% probability of having two distinct lengths in the posterior sample. The scale bar shows the expected number of substitutions per site. Blue circles indicate nodes with explicit temporal constraints (see Table 1).

Figure 2. Maximum clade credibility chronogram.

Maximum clade credibility chronogram derived from the summary of post-burnin samples from six independent BEAST analyses utilizing an uncorrelated lognormal relaxed clock model and lognormal temporal constraint priors (see text for explanation). Nodes are plotted as mean divergence time estimates (Ma), and blue horizontal bars represent 95% posterior credible intervals. Numbers in the tree diagram indicate posterior clade probabilities, with red circles representing nodes with posterior probability equal to 1.0. Green letters indentify major nodes whose age estimates across analyses are provided in Table 2. For legibility, major classes are collapsed and subsequent outgroups are not shown.