Phylogenetic-Signal Dissection of Nuclear Housekeeping Genes Supports the Paraphyly of Sponges and the Monophyly of Eumetazoa

The relationships at the base of the metazoan tree have been difficult to robustly resolve, and there are several different hypotheses regarding the interrelationships among sponges, cnidarians, ctenophores, placozoans, and bilaterians, with each hypothesis having different implications for the body plan of the last common ancestor of animals and the paleoecology of the late Precambrian. We have sequenced seven nuclear housekeeping genes from 17 new sponges, bringing the total to 29 species analyzed, including multiple representatives of the Demospongiae, Calcarea, Hexactinellida, and Homoscleromorpha, and analyzed a data set also including six nonmetazoan outgroups and 36 eumetazoans using a variety of phylogenetic methods and evolutionary models. We used leaf stability to identify rogue taxa and investigate their effect on the support of the nodes in our trees, and we identified clades most likely to represent phylogenetic artifacts through the comparison of trees derived using different methods (and models) and through site-stripping analyses. Further, we investigated compositional heterogeneity and tested whether amino acid composition bias affected our results. Finally, we used Bayes factors to compare our results against previously published phylogenies. All our maximum likelihood (ML) and Bayesian analyses find sponges to be paraphyletic, with all analyses finding three extant paraphyletic sponge lineages, Demospongiae plus Hexactinellida, Calcarea, and Homoscleromorpha. All but one of our ML and Bayesian analyses support the monophyly of Eumetazoa (here Cnidaria þ Bilateria) and a sister group relationship between Placozoa (here Trichoplax adhaerens) and Eumetazoa. Bayes factors invariably provide decisive support in favor of poriferan paraphyly when compared against either a sister group relationship between Porifera and Cnidaria or with a monophyletic Porifera with respect to a monophyletic Eumetazoa. Although we were able to recover sponge monophyly using our data set, this was only possible under unrealistic evolutionary models, if poorly performing phylogenetic methods were used, or in situations where the potential for the generation of tree reconstruction artifacts was artificially exacerbated. Everything considered, our data set does not provide any support for a monophyletic Diploblastica (here Placozoa þ Cnidaria þ Porifera) and suggests that a monophyletic Porifera may be better seen as a phylogenetic artifact

Phylogenetic-Signal Dissection of Nuclear Housekeeping Genes Supports the Paraphyly of Sponges and the Monophyly of Eumetazoa

The relationships at the base of the metazoan tree have been difficult to robustly resolve, and there are several different hypotheses regarding the interrelationships among sponges, cnidarians, ctenophores, placozoans, and bilaterians, with each hypothesis having different implications for the body plan of the last common ancestor of animals and the paleoecology of the late Precambrian. We have sequenced seven nuclear housekeeping genes from 17 new sponges, bringing the total to 29 species analyzed, including multiple representatives of the Demospongiae, Calcarea, Hexactinellida, and Homoscleromorpha, and analyzed a data set also including six nonmetazoan outgroups and 36 eumetazoans using a variety of phylogenetic methods and evolutionary models. We used leaf stability to identify rogue taxa and investigate their effect on the support of the nodes in our trees, and we identified clades most likely to represent phylogenetic artifacts through the comparison of trees derived using different methods (and models) and through site-stripping analyses. Further, we investigated compositional heterogeneity and tested whether amino acid composition bias affected our results. Finally, we used Bayes factors to compare our results against previously published phylogenies. All our maximum likelihood (ML) and Bayesian analyses find sponges to be paraphyletic, with all analyses finding three extant paraphyletic sponge lineages, Demospongiae plus Hexactinellida, Calcarea, and Homoscleromorpha. All but one of our ML and Bayesian analyses support the monophyly of Eumetazoa (here Cnidaria þ Bilateria) and a sister group relationship between Placozoa (here Trichoplax adhaerens) and Eumetazoa. Bayes factors invariably provide decisive support in favor of poriferan paraphyly when compared against either a sister group relationship between Porifera and Cnidaria or with a monophyletic Porifera with respect to a monophyletic Eumetazoa. Although we were able to recover sponge monophyly using our data set, this was only possible under unrealistic evolutionary models, if poorly performing phylogenetic methods were used, or in situations where the potential for the generation of tree reconstruction artifacts was artificially exacerbated. Everything considered, our data set does not provide any support for a monophyletic Diploblastica (here Placozoa þ Cnidaria þ Porifera) and suggests that a monophyletic Porifera may be better seen as a phylogenetic artifact

Oxygen and animals in Earth history

Earth and Planetary Science

The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: Evidence for programmed translational frameshifting

<p>Abstract</p> <p>Background</p> <p>Mitochondrial genomes (mtDNA) of numerous sponges have been sequenced as part of an ongoing effort to resolve the class-level phylogeny of the Porifera, as well as to place the various lower metazoan groups on the animal-kingdom tree. Most recently, the partial mtDNA of two glass sponges, class Hexactinellida, were reported. While previous phylogenetic estimations based on these data remain uncertain due to insufficient taxon sampling and accelerated rates of evolution, the mtDNA molecules themselves reveal interesting traits that may be unique to hexactinellids. Here we determined the first complete mitochondrial genome of a hexactinellid sponge, <it>Aphrocallistes vastus</it>, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.</p> <p>Results</p> <p>The <it>A. vastus </it>mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs. The <it>A. vastus </it>mtDNA showed a typical hexactinellid nucleotide composition and shared a large synteny with the other sequenced glass sponge mtDNAs. It also contained an unidentified open reading frame and large intergenic space region. Two frameshifts, in the <it>cox3 </it>and <it>nad6 </it>genes, were not corrected by RNA editing, but rather possessed identical shift sites marked by the extremely rare tryptophan codon (UGG) followed by the common glycine codon (GGA) in the +1 frame.</p> <p>Conclusion</p> <p>Hexactinellid mtDNAs have shown similar trends in gene content, nucleotide composition, and codon usage, and have retained a large gene syntenty. Analysis of the mtDNA of <it>A. vastus </it>has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.</p

A Basin Redox Transect at the Dawn of Animal Life

Multiple eukaryotic clades make their first appearance in the fossil record between ~810 and 715 Ma. Molecular clock studies suggest that the origin of animal multicellularity may have been part of this broader eukaryotic radiation. Animals require oxygen to fuel their metabolism, and low oxygen levels have been hypothesized to account for the temporal lag between metazoan origins and the Cambrian radiation of large, ecologically diverse animals. Here, paleoredox conditions were investigated in the Fifteenmile Group, Ogilvie Mountains, Yukon, Canada, which hosts an 811 Ma ash horizon and spans the temporal window that captures the inferred origin and early evolution of animals. Iron-based redox proxies, redox-sensitive trace elements, organic carbon percentages and pyrite sulfur isotopes were analyzed in seven stratigraphic sections along two parallel basin transects. These data suggest that for this basin, oxygenated shelf waters overlay generally anoxic deeper waters. The anoxic water column was dominantly ferruginous, but brief periods of euxinia likely occurred. These oscillations coincide with changes in total organic carbon, suggesting euxinia was primarily driven by increased organic carbon loading. Overall, these data are consistent with proposed quantitative constraints on Proterozoic atmospheric oxygen being greater than 1% of modern levels, but less than present levels. Comparing these oxygen levels against the likely oxygen requirements of the earliest animals, both theoretical considerations and the ecology of modern oxygen-deficient settings suggest that the inferred oxygen levels in the mixed layer would not have been prohibitive to the presence of sponges, eumetazoans or bilaterians. Thus the evolution of the earliest animals was probably not limited by the low absolute oxygen levels that may have characterized Neoproterozoic oceans, although these inferred levels would constrain animals to very small sizes and low metabolic rates.Earth and Planetary SciencesOrganismic and Evolutionary Biolog

Oxygen, Ecology, and the Cambrian Radiation of Animals

The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event and the evident increase in diversity and disparity. Ecological triggers focused on escalatory predator–prey “arms races” can explain the evolutionary pattern but not its timing, whereas environmental triggers, particularly ocean/atmosphere oxygenation, do the reverse. Using modern oxygen minimum zones as an analog for Proterozoic oceans, we explore the effect of low oxygen levels on the feeding ecology of polychaetes, the dominant macrofaunal animals in deep-sea sediments. Here we show that low oxygen is clearly linked to low proportions of carnivores in a community and low diversity of carnivorous taxa, whereas higher oxygen levels support more complex food webs. The recognition of a physiological control on carnivory therefore links environmental triggers and ecological drivers, providing an integrated explanation for both the pattern and timing of Cambrian animal radiation.Earth and Planetary SciencesOrganismic and Evolutionary Biolog

Persistent global marine euxinia in the early Silurian

The second pulse of the Late Ordovician mass extinction occurred around the Hirnantian-Rhuddanian boundary (~444 Ma) and has been correlated with expanded marine anoxia lasting into the earliest Silurian. Characterization of the Hirnantian ocean anoxic event has focused on the onset of anoxia, with global reconstructions based on carbonate δ238U modeling. However, there have been limited attempts to quantify uncertainty in metal isotope mass balance approaches. Here, we probabilistically evaluate coupled metal isotopes and sedimentary archives to increase constraint. We present iron speciation, metal concentration, δ98Mo and δ238U measurements of Rhuddanian black shales from the Murzuq Basin, Libya. We evaluate these data (and published carbonate δ238U data) with a coupled stochastic mass balance model. Combined statistical analysis of metal isotopes and sedimentary sinks provides uncertainty-bounded constraints on the intensity of Hirnantian-Rhuddanian euxinia. This work extends the duration of anoxia to &gt;3 Myrs – notably longer than well-studied Mesozoic ocean anoxic events

Early Neoproterozoic Basin Formation in Yukon, Canada: Implications for the make-up and break-up of Rodinia

SUMMARY: Geological mapping and stratigraphic anaylsis of the early Neoproterozoic Fifteenmile Group in the western Ogilvie Mountains of Yukon, Canada, has revealed large lateral facies changes in both carbonate and siliciclastic strata.  Syn-sedimentary NNW-side-down normal faulting during deposition of the lower Fifteenmile Group generated local topographic relief and wedge-shaped stratal geometries. These strata were eventually capped by platformal carbonate after the establishment of a NNW-facing stromatolitic reef complex that formed adjacent to the coeval Little Dal Group of the Mackenzie Mountains, Northwest Territories.  Correlations between specific formations within these groups are tested with carbon isotope chemostratigraphy.  As there are no known 830-780 Ma stratigraphic successions south of 62°N, the basin-forming event that accommodated the Fifteenmile and Little Dal Groups of the Ogilvie and Mackenzie Mountains and equivalent strata in the Shaler Supergroup of Victoria Island was restricted to the northwest margin of Laurentia. Therefore, this event does not represent widespread rifting of the entire western margin of Laurentia and instead we propose that these strata were accommodated in a failed rift generated by localized subsidence associated with the emplacement of the coeval Guibei (China) and Gairdner (Australia) large igneous provinces.  The northern margin of Laurentia was reactivated by renewed extension at ca. 720 Ma associated with the emplacement of the Franklin large igneous province.  Significant crustal thinning and generation of a thermally subsiding passive margin on the western margin of Laurentia may not have occurred until the late Ediacaran.RÉSUMÉLe cartographiage géologique et l’analyse stratigraphique du groupe néoprotézoïque Fifteenmile situé à l’ouest des montagnes Ogilvie du Yukon, Canada, ont révélé de grands changements latéraux de faciès à la fois pour les strates carbonatées et silicoclastiques. La mise en place des failles normales syn-sédimentaires inclinées vers le NNW au cours du dépôt du groupe Fifteenmile inférieur, a entrainé la formation locale d’un relief topographique et une prisme des strates. Ces dernières ont finalement été recouvertes de carbonates de plate-forme issus de la mise en place d’un complexe récifal stromatolitique exposé NNW contigu à la formation de même âge du groupe Little Dal des montagnes Ogilvie, en Territoires du Nord-Ouest. Les corrélations existant entre des formations spécifiques de chacun de ces groupes, sont testées grâce à la chimiostratigraphie des isotopes du carbone. Aucunes successions stratigraphiques agées de 830-780 Ma n’étant connues au sud de 62° N, la formation du bassin où sont accumulés les groupes Fifteenmile et Little Dal des massifs Ogilvie et Mackenzie, ainsi que les strates analogues du supergroupe Shaler de l’île Victoria, était restreinte à la bordure nord-ouest de la Laurentie. De ce fait, cet événement ne correspond pas au large rifting s’étendant sur l’entière bordure ouest de la Laurentie et nous proposons à la place, que ces strates ont été localisées au cours d’un rift avorté généré par la mise en place simultanée des larges provinces ignées Guibei (Chine) et Gairdner (Australie). La bordure nord de la Laurentie a été réactivée par une nouvelle phase d’extension à ca. 720 Ma associée à l’emplacement de la province ignée Franklin. L’amincissement crustal et la formation d’une marge passive thermiquement subsidente le long de la bordure ouest de la Laurentie ne se sont certainement pas produits avant l’Édiacarien supérieur

Demosponge steroid biomarker 26-methylstigmastane provides evidence for Neoproterozoic animals

Sterane biomarkers preserved in ancient sedimentary rocks hold promise for tracking the diversification and ecological expansion of eukaryotes. The earliest proposed animal biomarkers from demosponges (Demospongiae) are recorded in a sequence around 100 Myr long of Neoproterozoic–Cambrian marine sedimentary strata from the Huqf Supergroup, South Oman Salt Basin. This C_(30) sterane biomarker, informally known as 24-isopropylcholestane (24-ipc), possesses the same carbon skeleton as sterols found in some modern-day demosponges. However, this evidence is controversial because 24-ipc is not exclusive to demosponges since 24-ipc sterols are found in trace amounts in some pelagophyte algae. Here, we report a new fossil sterane biomarker that co-occurs with 24-ipc in a suite of late Neoproterozoic–Cambrian sedimentary rocks and oils, which possesses a rare hydrocarbon skeleton that is uniquely found within extant demosponge taxa. This sterane is informally designated as 26-methylstigmastane (26-mes), reflecting the very unusual methylation at the terminus of the steroid side chain. It is the first animal-specific sterane marker detected in the geological record that can be unambiguously linked to precursor sterols only reported from extant demosponges. These new findings strongly suggest that demosponges, and hence multicellular animals, were prominent in some late Neoproterozoic marine environments at least extending back to the Cryogenian period