Ulf Sorhannus

Diversity dynamics of marine planktonic diatoms across the Cenozoic.

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 CO2 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.

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

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.

HERMIT CRAB PHYLOGENY: A REAPPRAISAL AND ITS “FALL-OUT”

Abstract The hypothesis of monophyly in Paguroidea and the relationship of this superfamily to the other three superfamilies of Anomura have been reassessed using current cladistic methods and computer generated analysis. In the analysis, 79 external morphological characters were examined for an in-group consisting of the seven paguroid families, Pylochelidae, Coenobitidae, Diogenidae, Pylojacquesidae, Paguridae, Parapaguridae, and Lithodidae (divided into the subfamilies Lithodinae and Hapalogastrinae), three hippoid families, Blepharipodidae, Albuneidae, and Hippidae, five galatheoid families, Galatheidae, Chirostylidae, Kiwaidae, Aeglidae, and Porcellanidae, and the Lomisoideas monotypic Lomisidae. The out-group was comprised of Neoglyphea inopinata, representing Fractosternalia, and the families Dromiidae and Dynomenidae representing Brachyura. This analysis has shown that Anomura indeed is a monophyletic infraorder, as is Hippoidea a monophyletic superfamily. However, while six of the paguroid families form a cohesive clade, the two subfamilies of Lithodidae form a distinct clade more closely related to the superfamily Hippoidea than to the other paguroids. Galatheoidea, as presently constituted, is polyphyletic. Aeglidae, like Lithodidae, is more closely related to Hippoidea than to the galatheoid clade formed by the families Galatheidae, Chirostylidae, and Porcellanidae. Kiwaidae is also distinct from Galatheoidea sensu stricto, but its relationship, and that of Lomisoidea, to the remainder of the anomuran taxa are unresolved in the present analysis. As a result of this reappraisal, we propose that Lithodidae be removed from Paguroidea sensu lato and elevated to superfamily rank with families Lithodidae and Hapalogastridae. Similarly, we propose that Galatheoidea be restricted to the families Galatheidae, Chirostylidae, and Porcellanidae, whereas Kiwaidae and Aeglidae are each to be elevated to superfamily rank. Anomura will then consist of seven superfamilies, Hippoidea, Lithodoidea, Aegloidea, Lomisoidea, Kiwaoidea, Galatheoidea sensu stricto, and Paguroidea sensu stricto.

Diatom phylogenetics inferred based on direct optimization of nuclear-encoded SSU rRNA sequences

Direct optimization (DO) of 126 nuclear‐encoded SSU rRNA diatom sequences was conducted. The optimal phylogeny indicated several unique relationships with respect to those recovered from a maximum likelihood (ML) analysis of an alignment based on maximizing primary and secondary structural similarity between 126 nuclear‐encoded SSU rRNA diatom sequences ( Medlin and Kaczmarska, 2004 ). Dividing diatoms into the subdivisions Coscinodiscophytina and Bacillariophytina was not supported by the DO phylogeny, due to the paraphyly of the former. The same pertains to Coscinodiscophyceae, Mediophyceae, Thalassiosira, Fragilaria and Amphora. The ordinal‐level classification of the diatoms proposed by Round et al. (1990 ) was for the most part found to be unsupported. The DO phylogeny represented a more rigorous hypothesis than the ML tree because DO maximized character congruence during the homology testing (i.e., alignment/tree search) process whereas the non‐phylogenetic similarity‐based alignment used in the ML analysis did not. The above statement is supported by “controlled” parsimony analyses of 35 sequences, which strongly suggested that dissimilarities in the DO and ML tree structure were due to the specific homology testing approach used. It could not be precluded that differences in taxon sampling and the use of a dissimilar optimality criteria contributed to discrepancies in the structure of the optimal ML and DO trees.

PECTINATE CLAWS IN DECAPOD CRUSTACEANS: CONVERGENCE IN FOUR LINEAGES

Abstract Decapod crustaceans bearing major claws with long, slender fingers armed with pectinate (comblike) denticles have been described in six genera arrayed within three families (Polychelidae, Nephropidae, and Ctenochelidae) in three infraorders (Palinura, Astacidea, and Anomura, respectively). Only one or a few genera in each infraorder exhibit this claw form. The pectinate claw form is confidently interpreted as having evolved independently in four lineages: once in the Polychelidae, once in the Ctenochelidae, and twice in the Nephropidae. Three of the lineages are known from both the fossil record and modern seas; the polychelid form is known only from Jurassic rocks. Convergence in this claw form developed to the extent that isolated fossil claws (i.e., claws without associated bodies) have commonly been misidentified at high taxonomic levels. The fossil record confirms what seems intuitively reasonable: that claw morphology is prone to convergence and should not, by itself, be given a high degree of taxonomic importance.

Evidence for Positive Selection on a Sexual Reproduction Gene in the Diatom Genus Thalassiosira (Bacillariophyta)

Single likelihood ancestor counting (SLAC), fixed effects likelihood (FEL), and several random effects likelihood (REL) methods were utilized to identify positively and negatively selected sites in sexually induced gene 1 (Sig1) of four different Thalassiosira species. The SLAC analysis did not find any sites affected by positive selection but suggested 13 sites influenced by negative selection. The SLAC approach may be too conservative because of low sequence divergence. The FEL and REL analyses revealed over 60 negatively selected sites and two positively selected sites that were unique to each method. The REL method may not be able to reliably identify individual sites under selection when applied to short sequences with low divergence. Instead, we proposed a new alignment-wide test for adaptive evolution based on codon models with variation in synonymous and nonsynonymous substitution rates among sites and found evidence for diversifying evolution without relying on site-by-site testing. The performance of the FEL and REL approaches was evaluated by subjecting the tests to a type I error rate simulation analysis, using the specific characteristics of the Sig1 data set. Simulation results indicated that the FEL test had reasonable Type I errors, while REL might have been too liberal, suggesting that the two positively selected sites identified by FEL (codons 94 and 174) are not likely to be false positives. The evolution of these codon sites, one of which is located in functional domain II, appears to be associated with divergence among the three major Thalassiosira lineages.

RpoA: A Useful Gene for Phylogenetic Analysis in Diatoms

Abstract The aim of this study was to compare the usefulness of two chloroplast-encoded genes (rpoA and rbcL) and the nuclear-encoded small subunit (SSU) ribosomal RNA for reconstructing phylogenetic relationships among diatoms at lower taxonomic levels. To this end, the rpoA and rbcL genes for selected centric and pennate diatoms were sequenced. The new rpoA and rbcL sequences, and an existing nuclear-encoded SSU rRNA data set, were subjected to weighted/unweighted parsimony, maximum likelihood, minimum evolution, and Bayesian analyses. All of the tree-building methods employed showed, based on the support values, that the rpoA gene was the most useful, relative to the rbcL and SSU rRNA genes, in determining phylogenetic relationships among the sampled diatoms. The support values for the relationships among the pennate lineages were, in many instances, greater in the rpoA trees than in the SSU rRNA trees. These results suggest that rpoA might be of value in determining phylogenetic relationships among pennate lineages.

Synonymous and Nonsynonymous Substitution Rates in Diatoms: A Comparison Between Chloroplast and Nuclear Genes

Abstract. Rates of synonymous and nonsynonymous nucleotide substitutions and codon usage bias (ENC) were estimated for a number of nuclear and chloroplast genes in a sample of centric and pennate diatoms. The results suggest that DNA evolution has taken place, on an average, at a slower rate in the chloroplast genes than in the nuclear genes: a rate variation pattern similar to that observed in land plants. Synonymous substitution rates in the chloroplast genes show a negative association with the degree of codon usage bias, suggesting that genes with a higher degree of codon usage bias have evolved at a slower rate. While this relationship has been shown in both prokaryotes and multicellular eukaryotes, it has not been demonstrated before in diatoms.

Phylogenetic analyses of a combined data set suggest that the Attheya lineage is the closest living relative of the pennate diatoms (Bacillariophyceae).

A Bayesian analysis of a seven gene data set was conducted to reconstruct phylogenetic relationships among a sample of centric and pennate diatoms and to test alternative hypotheses about the closest living relative of Bacillariophyceae. A lineage, composed of two Attheya species, was inferred to share the most recent common ancestor with Bacillariophyceae--a relationship that was also corroborated by the combined parsimony analysis. All competing hypotheses about the closest living relative of Bacillariophyceae were rejected because 100% of the trees in the post-burn-in sample in the Bayesian analysis supported the Attheya-Bacillariophyceae clade. According to a partitioned Bremer support analysis, the majority of the genes in the combined data matrix supported the Attheya--Bacillariophyceae relationship. The global topology of the phylogenetic tree indicated that a monophyletic group consisting of Thalassiosirales and Toxarium undulatum formed the deepest branch followed by a node uniting a clade composed of Bacillariophyceae/Attheya species and a lineage made up of Eucampia zoodiacus, Chaetocerotales, Lithodesmiales, Triceratiales, Biddulphiales and Cymatosirales. Except for the phylogenetic positions of Lithodesmiales, Thalassiosira sp and Skeletonema costatum, the optimal tree obtained from the combined parsimony analysis showed the same branching order of taxa as those seen in the consensus tree inferred from three independent Markov chain Monte Carlo analyses. Noteworthy findings are that Toxarium undulatum shares a strongly supported node with Thalassiosirales and that the genus Attheya is not a member of the Chaetocerotales lineage.

evolution of Antifreeze protein Genes in the Diatom Genus Fragilariopsis: evidence for Horizontal Gene Transfer, Gene Duplication and episodic Diversifying selection

Hypotheses about horizontal transfer of antifreeze protein genes to ice-living diatoms were addressed using two different statistical methods available in the program Prunier. The role of diversifying selection in driving the differentiation of a set of antifreeze protein genes in the diatom genus Fragilariopsis was also investigated. Four horizontal gene transfer events were identified. Two of these took place between two major eukaryote lineages, that is from the diatom Chaetoceros neogracile to the copepod Stephos longipes and from a basidiomycete clade to a monophyletic group, consisting of the diatom species Fragilariopsis curta and Fragilariopsis cylindrus. The remaining two events included transfers from an ascomycete lineage to the proteobacterium Stigmatella aurantiaca and from the proteobacterium Polaribacter irgensii to a group composed of 4 proteobacterium species. After the Fragilariopsis lineage acquired the antifreeze protein gene from the basidiomycetes, it duplicated and went through episodic evolution, characterized by strong positive selection acting on short segments of the branches in the tree. This selection pattern suggests that the paralogs differentiated functionally over relatively short time periods. Taken together, the results obtained here indicate that the group of antifreeze protein genes considered here have a complex evolutionary history.