Data on sponge facies in this basin of western Argentina are scarce in the general geological literature. Legarreta mentioned siliceous sponges and sponge spicules as skeletal components of the sedimentary facies of the La Manga formation. The most recent reports of these fossils may be found in Beresi , , During the Lower and Middle Oxfordian, part of the region was extensively flooded as a result of a relative sea level rise Uliana and Biddle, Shelf carbonate facies dominated in southern Mendoza.
The asterisk indicates the position of the sponge bioherms. The carbonate shelf facies is known as the La Manga formation. In southern Mendoza, the carbonate facies may have been deposited in a ramp that evolved to a carbonate platform environment with a clearly defined shelf edge Legarreta, In the Potimalal section, the La Manga formation consists of 10— 15 m of fossiliferous deep-water deposits.
It is lithologically composed of basinal and slope micritic limestones and black shales with brachiopods. The lower unit is 2. The upper unit is 11 m thick, and the base has a sharp contact. This unit is olive-grey skeletal to intraclastic packstone — wackestone , stratified in thick to medium beds. The fossil content is characterized by bivalves and ammonites.
Sponges were found in small bioherms of the lower unit of the La Manga formation. Sponge facies correspond to siliceous sponge framestones. Almost all the sponges from this Oxfordian section are hexactinellids M. This unit consists of grey and moderately bored buildups, made of sponges hexactinellids and lithistids , and associated serpulid worms and rare bryozoans.
The matrix is a skeletal wackestone consisting of small oysters and pelecypod fragments, gastropods, and spicules, and with a subordinate participation of echinoids, forams and calcispheres. Buildups are massive with variable dimensions and geometry. Shapes are primarily pyramidal and range from small bodies with sizes from 0.
The buildup cores are surrounded and covered by crudely stratified pelecypod floatstones. The presence of siliceous sponges buildups situated in a micrite richlimestone mass indicates relatively deep and quiet water. The palaeo-water-depth estimates derived from the stratigraphic reconstruction suggest that the sponge buildups developed around 50 m below sea level.
According to Legarreta , this facies corresponds to the second sequence This second depositional sequence was laid down during the Middle Oxfordian Plicatilis Stipanicic, ; Riccardi, For more details on the other facies, sequences, and fauna, see Legarreta Association of sponges from the biohermal limestones In the investigated locality Fig. Hexactinosa are the most common among the studied sponges of the Potimalal section. This group became very diversified and common in the Late Jurassic Trammer, , ; Pisera, The dominant growth forms Fig.
Cylinders grow up to mm in size, whereas cups are smaller than mm. Sponges with a rigid skeleton are embedded in a micritic matrix in the bioherms that developed by an abundant accumulation of sponges, more abundant than in the surrounding rocks. The matrix is hard and compact micritic limestone. Texturally, the matrix of the bioherms is composed of a medium-grey fine skeletal wackestone with scattered fragments of small oysters and pelecypods. A fauna with low diversity, but rich in specimens of hexactinellids most of which are dictyds , is the dominant component of the biota.
Most sponges are in a living position inside the bioherms and are preserved as larger fragments. Only a few sponges have encrustation of serpulids and brachiopods. No microbial crusts overgrew the sponges. No isolated root tuffs have been seen in the massive limestones. This is suggested by the absence of sedimentary structures, indicative of wave action, and the sponge fauna typical of deep-shelf habitats.
Citaties per jaar
There are not corals, gastropods, or calcareous sponges in this facies. The lithological and paleontological analyses suggest that the sponge associations grew in a deep-water environment characterized by a firm substrate, low rates of sedimentation, and low to moderate water energy, which represents a slight deepening of the platform. The taxonomic composition, dominance of hexactinellids, and absence of calcareous sponges and corals, as well as the very low proportion of encrusters, also suggests deep-water environments.
Consequently, the environment was optimum for the growth of sponges but not of other faunal elements. The assemblage was situated on the outer shelf with normal marine salinity and a very low sedimentation rate that enabled the growth of these sponge types, which formed small bioherms. The occurrence of the siliceous sponge faunas is associated with high sea level. This is in agreement with the important global rise of sea level that took place during the Early Oxfordian. The resulting transgression induced an unusually low sedimentation rate.
The sea floor was colonized by this M. A Upper view of the narrow osculum and folded wall in a cribospongiid sponge. B Lateral view of Laocoetis clathrata. C Lateral view of Laocoetis sp. D Upper view of the same sponge showing the thick wall and the small circular osculum.
Systematic The siliceous sponges are represented almost exclusively by hexactinellids. Most of the collected sponges is representative of the Order Hexactinosa Schrammen, Only sponges with fused choanosomal skeletons composed of dictyonal strands are included here following Pisera These specimens include sponges that show the skeleton structure and canal-opening arrangement in diplorysis Quincunx Krautter, The most common sponges of to the Family Cribrospongiidae are cup-shaped Cribrospongia reticulata , tubular, and conical.
The dermal side, with large oval to rounded canal openings from M. A Longitudinal section of a tubular cribrospongiid sponge. B Laocoetis procumbens, lateral view. C Lateral view of a cylindrical sponge.
D Lateral view of Cribrospongia cucculata. The dictyonal skeleton has regular meshes measuring 0. Schrammen, These specimens are fragments of cylindrical to tubular sponges with heights varying between — mm and widths up to 85 mm with a wide simple osculum at top. The sponges have walls up to 16 mm thick. The external surface is pierced by canal openings of 0. The dermal surface of the dictyonal skeleton is pierced by rounded and oval canal openings that measure in various specimens from 0. They are separated by very regular longitudinal skeletal bands 0. Dictyonal skeletons with normally rectangular meshes measure 0.
Dictyonal strands diverge toward both surfaces and arch toward the outer margin. Loose disassociated spicules of large hexactines pentactines and rhabdoactines from three specimens have been obtained through processing with an acid solution. The hexactine spicules are smooth and straight with square sections 0.
The occurrence of the earliest freshwater sponge fossil spicule is dated to the Permo-Carboniferous [ 51 ] and constitutes the first and only known fossil record of freshwater sponges from the Paleozoic. The radiation of recent freshwater sponges, however, is dated as much younger in both of our analyses Therefore, our results question Schindler et al's [ 51 ] interpretation as Paleozoic spicules.
Also Schultze [ 80 ] interpreted the findings of Schindler and coworkers [ 51 ] as either marine or marine influenced, which again challenges the interpretation of this oldest described freshwater sponge. In contrast, fossil freshwater sponges with intact gemmules i. Yet, Peterson and Butterfield [ 70 ] suggested a divergence of Ma for Recent freshwater sponges using a node-calibrated relaxed molecular clock approach, whereupon the study of Schuster [ 85 ] indicates a Paleogene divergence.
The Paleogene records of freshwater sponges are known to be more diverse than the Neogene records [ 86 , 87 ]. Our analysis includes three freshwater species Baikalospongia intermedia, Lubomirskia baicalensis and Rezinkovia echinata , all Lubomirskiidae , all of which are known to be endemic to Lake Baikal [ 35 , 36 ].
As gemmules are known from the fossil record since the lower Cretaceous [ 84 ], and are present in the Recent spongillids Ephydatia and Eunapius, but absent from Lubomirskiidae see discussion in [ 88 ] , our data is consistent with the hypothesis that the most recent common ancestor of Spongillida possessed gemmules, which were subsequently lost in several endemic lineages such as the Lake Baikal Lubomirskiidae see discussion in [ 88 ]. Despite these Cambrian fossil discoveries, the molecular clock analyses of Sperling et al. These contradictory results may have different explanations.
First, due to their massive and thicker size, the Cambrian tetractinellid tetraxial-like spicules may not be homologous to post-Paleozoic forms [ 14 , 49 ]. Second, the presence of aster-like and monaxon spicules in several recent demosponge groups other than the Tetractinellida may lead to the erroneous interpretation of the Cambrian fossil spicules.
Third, the high level of secondary losses of various spicule types, in particular microscleres within Astrophorina [ 22 , 67 , 89 ], hamper unambiguous interpretation of their homology. The node age shows a left-skewed distribution to younger ages Additional file 7 , BEAST analysis 2 , which correlates with the current known fossil record from the late Jurassic to Recent [ 14 , 26 ].
The only known fossil representative of the genus Neophrissospongia is described from the Early Campanian of Poland [ 26 ], but our analysis indicates a deeper origin dating back to the Middle Jurassic Fig. This increase in fossil sampling neither influenced our results positively by reducing the error bars for instance nor negatively, which corroborates other findings of Heath et al.
The investigation of the divergence ages of this desma-bearing demosponge family strengthens the Jurassic origin of this clade and provides additional information on possible calibration constraints on further molecular clock approaches. The frequency distribution on the node age indicates a slightly right-shifted normal distribution towards younger ages Additional file 7 , BEAST analysis 2.
A characteristic diagnostic feature for this group is the presence of sigmaspire S- to C-shaped microclere spicules. Mehl-Janussen [ 91 ] suggested the occurrence of Spirophorina in the Early Paleozoic, with a possible Cambrian origin, however, these observations cannot be supported by any of our analyses.
As sigma-like spicules are also present in other demosponge lineages like e. The mitochondrial mt rate of evolution differ considerable within Porifera. Among all 4 classes, demosponges show a comparatively low mt evolutionary rate see e. This low evolutionary rate has here been considered as advantageous for dating deep nodes in the phylogeny.
For instance, such an approach would not be feasible for calcareous or hexactinellid sponges, where the rate of mt evolution is much higher see e.
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Even though differences in the mt rate of evolution are observed between poriferan classes, mutation rates within Demospongiae are similar see e. Except for the order Dictyoceratida, none of the other demosponge groups have been found to possess accelerated rates of mt genome evolution see e. Therefore, mutation rate heterogeneity is unlikely to affect our results. Furthermore, adding more genes, e.
However, more important factors to consider in a dated analyses are the number of fossils as calibration points, possible uncertainties in their date estimations, as well using secondary calibration points, which consequently will shift when changing the estimated divergence times. Here we successfully assembled six complete mitogenomes of different demosponge taxa generated by a size-selected reduced representation genomic library.
Integrating these data into a novel mitogenome alignment in tandem with a newly tested relaxed molecular clock approach based on the FBD model, we provide new insights into the evolution of selected Demospongiae. The Neoproterozoic origin of Demospongiae is confirmed. Nevertheless, our estimated divergence times of different higher tetractinellid taxa such as the Astrophorina or Corallistidae can be further used for inferring finer-scaled divergence time estimates to shed new light on e. These results, and in particular the dated split of freshwater and marine sponges, can be used as a root age for further dated phylogenies on freshwater sponges in order to get a better picture of e.
Bayesian Inference molecular phylogeny of the Demospongiae, based on 14 protein coding genes. Maximum likelihood topology is congruent. Clade support values are posterior left and bootstrap right , above branch lengths. PNG kb. XML kb. Tracer statistics of turnover, diversification and sampling proportion of the two runs and the prior from BEAST analysis 2. Mitochondrial genome structure with genome size, gene annotations, GC-content in blue and AT-content in green.
Error bars on node ages are in dark turquoise. We greatly acknowledge Zac H. We want to thank three anonymous reviewers for their helpful comments, which greatly improved the MS. ISK helped in the lab to generate the libraries. SAP provided samples. AS wrote the manuscript and prepared all figures. All authors read and approved the final manuscript. This study did not include protected or endangered species and requires no ethical approval.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Electronic supplementary material. Astrid Schuster, Email: ed. Sergio Vargas, Email: ed. Ingrid S. Knapp, Email: moc. Shirley A. Pomponi, Email: ude. Robert J. Toonen, Email: moc.
Dirk Erpenbeck, Email: ed. National Center for Biotechnology Information , U. BMC Evol Biol. Published online Jul Knapp , 2 Shirley A. Pomponi , 3 Robert J. Author information Article notes Copyright and License information Disclaimer. Corresponding author. Received Nov 6; Accepted Jul 3. This article has been cited by other articles in PMC.
XLSX 52 kb. Additional file 2: Bayesian Inference molecular phylogeny of the Demospongiae, based on 14 protein coding genes. Additional file 4: Detailed information on the fossils used. DOCX kb. Additional file 5: Tracer statistics of turnover, diversification and sampling proportion of the two runs and the prior from BEAST analysis 2.
LOG kb. Additional file 8: Mitochondrial genome structure with genome size, gene annotations, GC-content in blue and AT-content in green. Results Our study supports a Neoproterozoic origin of Demospongiae. Conclusion This study provides novel insights into the evolution of Demospongiae.
Electronic supplementary material The online version of this article Keywords: Mitochondrial genomes, Molecular clock, next-generation sequencing, Demospongiae, Fossilized birth-death model, Porifera, Molecular dating. Background The sequencing of sponge mitochondrial mt genomes greatly increased in the last decade [ 1 — 5 ]. Table 1 Divergence time estimates Ma of demosponge clades of interest from two different analyses. BEAST 2. Open in a separate window.
Results and Discussion Mitochondrial genome organisation — a general comparison While this approach has proven useful in other taxa such as molluscs and cnidarians [ 63 , 64 ], here we provide the first complete mitochondrial genomes obtained from size-selected reduced representation genomic libraries of sponges. Phylogenetic analyses Our ML and BI trees corroborate the sister group relationship of the marine order Sphaerocladina Vetulina , which is morphologically characterized by the possession of sphaeroclone desmas, to freshwater sponges Spongillida Additional file 2 , therefore supporting previous findings from ribosomal and partial mitochondrial single gene data [ 18 — 22 ].
Implications for divergence time estimates for Heteroscleromorpha The present study provides the first dated phylogeny of Heteroscleromorpha based on mt genomes and the relaxed molecular clock FBD model. Inferred divergence scenarios for the split of marine and freshwater sponges Many previously published molecular dating studies of Porifera are based on mitogenomic datasets, although hampered by incomplete taxon sampling, for example lacking freshwater and desma-bearing sponges.
Inferred timing of extant freshwater sponge diversification The occurrence of the earliest freshwater sponge fossil spicule is dated to the Permo-Carboniferous [ 51 ] and constitutes the first and only known fossil record of freshwater sponges from the Paleozoic. Notes and caveats in estmating divergence times in sponges using mt genomes The mitochondrial mt rate of evolution differ considerable within Porifera.
Conclusion Here we successfully assembled six complete mitogenomes of different demosponge taxa generated by a size-selected reduced representation genomic library. Additional file 2: K, png Bayesian Inference molecular phylogeny of the Demospongiae, based on 14 protein coding genes. Additional file 4: K, docx Detailed information on the fossils used. Additional file 5: K, png Tracer statistics of turnover, diversification and sampling proportion of the two runs and the prior from BEAST analysis 2.
Additional file 8: K, png Mitochondrial genome structure with genome size, gene annotations, GC-content in blue and AT-content in green. Notes Ethics approval and consent to participate This study did not include protected or endangered species and requires no ethical approval. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests.
Footnotes Electronic supplementary material The online version of this article Contributor Information Astrid Schuster, Email: ed. References 1. Mitochondrial diversity of early-branching Metazoa is revealed by the complete mt genome of a haplosclerid demosponge. Mol Biol Evol. Glass sponges and bilaterian animals share derived mitochondrial genomic features: a common ancestry or parallel evolution?
Wang X, Lavrov DV. PLoS One. Lavrov DV. Rapid proliferation of repetitive palindromic elements in mtDNA of the endemic Baikalian sponge Lubomirskia baicalensis. Lavrov DV, Pett W. Genome Biol Evol. The complete mitochondrial genome of the deep-sea sponge Poecillastra laminaris Astrophorida, Vulcanellidae.
Mitochondrial DNA. Mitochondrial genomes of the freshwater sponges Spongilla lacustris and Ephydatia cf. Reconstructing ordinal relationships in the Demospongiae using mitochondrial genomic data. Mol Phylogenet Evol. Mitochondrial genomes of two demosponges provide insights into an early stage of animal evolution.
Middle to Upper Oxfordian sponges of the Polish Jura
Diversity of sponge mitochondrial introns revealed by cox1 sequences of Tetillidae. Evolution of group I introns in Porifera: new evidence for intron mobility and implications for DNA barcoding. Pisera A. Systema Porifera. A guide to the classification of sponges. Non-lithistid fossil Demospongiae - Origins of their Palaeobiodiversity and highlights in history of preservation. Systema Porifera, A guide to the classification of Sponges. Family Corallistidae Sollas, Family Vetulinidae Lendenfeld, Phylogeny and classification of lithistid sponges Porifera: Demospongiae : a preliminary assessment using ribosomal DNA sequence comparisions.
Mol Mar Biol Biotechnol. Phylogenetic resolution potential of 18s and 28s rRNA genes within the lithistid Astrophorida. Memoirs-Queensland Museum ; — Phylogeny and systematics of demospongiae in light of new small-subunit ribosomal DNA 18S sequences. Integr Comp Biol. Addis JS, Peterson K. Zool Scr. Deceptive desmas: molecular phylogenetics suggests a new classification and uncovers convergent evolution of lithistid demosponges. A highly diverse siliceous sponge fauna Porifera: Hexactinellida, Demospongiae from the Eocene of north-eastern Italy: systematics and palaeoecology.
J Syst Palaeontol. Bodily preserved Eocene non-lithistid demosponge fauna from southern Australia: taxonomy and affinities. Contrib to Zool. Cretaceous Research. The fossilized birth—death process for coherent calibration of divergence-time estimates. Using more than the oldest fossils: Dating Osmundaceae with three Bayesian clock approaches.
Syst Biol. An evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform fishes Teleostei: Percomorphaceae. Species relationships and divergence times in beeches: new insights from the inclusion of 53 young and old fossils in a birth-death clock model. Philos Trans R Soc Lond. B Biol Sci. Dating early animal evolution using phylogenomic data. Sci Rep. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Long Continental Records from Lake Baikal. Japan: Springer; Veynberg E. Fossil sponge fauna in Lake Baikal region.
Prog Mol Subcell Biol. Ma J-Y, Yang Q. Early divergence dates of demosponges based on mitogenomics and evaluated fossil calibrations. On the oldest tetraxon megascleres. New perspectives in sponge biology. Washington, D. C: Smithsonian Institution Press; Plant Mol Biol Rep.
Upper Jurassic Sponge Megafacies in Spain: Preliminary Report
Jena: Gustav Fischer; Hawaii Institute of. Marine Biol. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. PhyloBayes MPI. Phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Lartillot N, Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.
ProtTest-HPC: fast selection of best-fit models of protein evolution. What can we learn about siliceous sponges from Palaeontology. Boll Mus Is. Biol Univ Genova.