Diatoms are the dominant group of phytoplankton in the modern ocean. They account for approximately 40% of oceanic primary productivity and over 50% of organic carbon burial in marine sediments. Owing to their role as a biological carbon pump and effects on atmospheric CO(2) levels, there is great interest in elucidating factors that influenced the rapid rise in diatom diversity during the past 40 million years. Two biotic controls on diversification have been proposed to explain this diversity increase: (1) geochemical coupling between terrestrial grasslands and marine ecosystems through the global silicon cycle; and (2) competitive displacement of other phytoplankton lineages. However, these hypotheses have not been tested using sampling-standardized fossil data. Here we show that reconstructions of species diversity in marine phytoplankton reject these proposed controls and suggest a new pattern for oceanic diatom diversity across the Cenozoic. Peak species diversity in marine planktonic diatoms occurred at the Eocene-Oligocene boundary and was followed by a pronounced decline, from which diversity has not recovered. Although the roles of abiotic and biotic drivers of diversification remain unclear, major features of oceanic diatom evolution are decoupled from both grassland expansion and competition among phytoplankton groups.
BackgroundStramenopiles 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 FindingsPhylogenetic 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/SignificanceThe 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.
Diatoms, unicellular eukaryotic algae with a siliceous skeleton, offer the rare advantage of displaying both an extensive fossil record and numerous extant species, thus providing the opportunity of confronting molecular and paleontological data in a protist group. A portion of the 28s ribosomal RNA was sequenced from 5 diatoms, the divergence times of which are well known. The nucleotide substitution rate was estimated in these unicellular eukaryotes and compared with the rate of multicellular eukaryotes, using a broad data base comprising metazoans and metaphytes. When using fossil record derived divergence times, our results show that the nucleotide substitution rate is about 5 times faster in diatoms than in chordates. But, when using the relative rate test, it is observed that, over a long time period, the nucleotide substitution rate may in fact have been slightly slower in diatoms than in chordates. For this contradiction, two possible explanations are proposed: (i) a failure of the relative rate test, (ii) a gap in the preJurassic diatom fossil record. We have checked that our results concerning the relative rate test were valid. Thus, the second hypothesis, which implies preJurassic diatom evolution, in fact already suggested by some non-molecular evidences, is favoured. Decoupling of morphological differentiation from genetic speciation also appears to have occurred and may account in part for the underestimation of the dates of recent cladogenesis events.
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