•True multicellularity involves specialized cell types, the specialization of reproductive cells, and apoptosis.
•Possible multicellular eukaryotes may extend back to 2.2 Ga
•Multicellularity arose five times among eukaryotes.
•Porifera (sponges) are the most primitive grade of metazoan.
•There are three major poriferan taxa (Hexactinellida, Demospongea, Calcarea) and one oddball (Homoscleromorpha).
•There is no strong consensus on whether poriferans are monophyletic.
•The earliest potential sponge fossils are Ediacaran but geochemical evidence form them goes back to 1.8 Ga
•Several enigmatic Phanerozoic fossil groups are likely to be poriferans.
"Well, it's not secret that the best thing about secrets is telling someone else your secret, thereby adding another secret to your secret collection of secrets, secretly.
(SpongeBob Squarepants, Season 2, Episode 35a.)
Most of the semester remaining will address the fossil record of Metazoa (animals.) Metazoans are one of five groups of multicellular eukaryotes to arise during the Neoproterozoic. Unlike simple cell colonies like Volvox or slime molds (right), each of these groups forms organized bodies in which:
Specialized cells perform specific functions
Body cells forego reproduction, leaving that task to specialized reproductive cells - gametes
Cells even engage in apoptosis - programmed cell death.
Critters of "slime-mold grade" (right) show the starting point of this transition, being independent cells that come together to produce fruiting bodies from which spores (haploid reproductive cells) are dispersed.
The earliest fossil evidence for colonial eukaryotes comes from the Proterozoic:
Grypania spiralis 2.1 Ga. A colony of cells forming coiled ribbons resembling some eukaryotic algal colonies. Despite bold claims, there is no direct evidence that these are eukaryote-grade. (Han and Runnegar, 1992.)
Bangiomorpha pubescens 1.2 Ga. A possible rhodophyte with a frond and holdfast capable of attaching to and elevating itself above the substrate. The big news is that Bangiomorpha shows distinct spores and gametes - the first known multicelular organisms to reproduce sexually! (Butterfield, 2000.)
These were forerunners to the emergence of multicellularity during the Cryogenian among.
For the rest of the course we concentrate on Metazoa and Viridiphytae.
Five major groups form the main branches of its cladogram:
Cnidaria: anemones, jellyfish, and kin (Ediacaran - Quaternary, significant fossil record)
Placozoa: tiny weirdos (possible representatives in Ediacaran)
Bilateria: animals with bilateral symmetry and flow-through guts (Ediacaran - Quaternary, significant fossil record)
The pattern of metazoan phylogeny is controversial. Results of molecular phylogenetic analysis are sensitive to the portion of the genome sampled (see Nosenko et al., 2013) The cladogram at right is a consensus. Ongoing controversy surrounds the positions of:
Ctenophora: Traditionally considered a Eumetazoan, but found by Whelan et al., 2015 to be basal to Porifera and Eumetazoa.
Porifera - the sponges:
(Ediacaran - Quaternary) The sponges represent the most primitive metazoan grade, lacking organs, possessing only the vaguest approximations of tissues, but possessing:
Specialized cell types
Cells that adhere in a regular body plan.
Signaling between cells
Interdependence. Indeed, sponge cells that have been mechanically separated can often coalesce into new sponges, but are unable to survive for long independently.
In their simplest form, sponges are hollow cylinders of living tissue, attached to the substrate at one end and open at the other. Key features:
Spongocoel: The large cavity occupying the sponge's interior.
Osculum: The opening from the spongocoel to the exterior through which filtered water is expelled.
Incurrent canals: lead from the exterior, through the body wall, to the spongocoel. Entrances to these are termed ostia (sing. ostium)
Mesohyl: Cells line the outer and inner surfaces of the sponge, and form the walls of pores. They secrete a gelatinous extracellular matrix of mesohyl that occupies the space in between. Depending on the type of sponge, this may also contain calcareous or silicate spicules or spongin fibers.
Choanocytes: Line the spongocoel, propelling water toward the osculum (hence drawing it into the ostia.) Choanocytes are primarily responsible for capturing food, which they filter from passing water, ingest, then package in golgi bodies and transfer to archeocytes, who transfer it to other cells. They closely resemble choanoflagellates
Pinacocytes: Line and protect the outer surface and may ingest food particles too large to pass through pores. Also secrete massive external skeleton, if there is one.
Porocytes: Line the pores and control the size of the ostia.
Archeocytes (a.k.a. "amoebocytes"): amoeboid cells occupying mesohyl that digest and transport nutrients. Archeocytes are totipotent - capable of transforming into most other cell types when needed (including ova).
Sclerocytes: Inhabit the mesohyl and lay down mineral spicules.
Spongocytes: Inhabit the mesohyl and secrete a form of collagen that polymerizes as spongin fibers.
Myocytes: Cells capable of contraction occur occasionally.
Gray cells: Mediate something like an immune response, immobilizing or killing cells in the vicinity of an infection.
Whether sponges lack tissues depends on one's definition. Indeed, the beginnings of distinct tissues are discernible:
Endoderm: lining the spongocoel
Ectoderm: lining the exterior.
Sponges are capable of only the simplest organized movement, although pinacocytes can often contract in a coordinated manner, and some sponges possess specialized myocytes that can contract to close off vulnerable areas like the osculum.
Sponge organizational grades (choanocytes in red) from AuxBulles.com
Although all sponges conform to this body plan, many increase their complexity by repeating it in a fractal manner. In the schematic at right, choanocyte-endoderm is highlighted in red:
Ascon grade sponges consist of single cylindrical units.
Sycon grade sponges are composites of numerous ascon-type units formed by the pleated infolding of the inner surface. In them, macroscopic incurrent canals bring external water to the pores.
Leucon grade sponges are, in turn, composites of syscon-type units with complex three-dimensional networks of incurrent canals and choanocyte chambers.
By production, in times of stress, of gemmules - hard-walled cysts containing archaeocytes. These survive harsh conditions and germinate to form new sponges, with archaeocytes differentiating into other necessary cell types.
Sexual, with ova developing from archeocytes, and sperm from choanocytes. Fertilization can be external or internal (with sperm from other individuals being captured by choanocytes and transferred internally to ova.)
Zygotes develop into larvae - balls of ciliated cells (either directly as part of the plankton or inside their mother) that swim in the plankton then settle onto the substrate, whereupon their cells transform into archaeocytes and from there into the normal array of adult cells.
Crystalline calcite spicules of diverse morphology.
Calcarea prefer warm shallow waters - coincidentally, the kind of environment where CaCO3 precipitates most readily.
Precipitation of calcite is mediated by carbonic anhydrase. Sclerocytes form spicules inside a proteinaceous sheath that is displaced by the growing crystal. Indeed, metabolic effort seems to be required to limit crystalization (Weiner and Addadi, 1997.)
Some may also secrete massive external skeleton of calcite. When this is present, it consists of amorphous calcite - calcite granules mixed with glycoproteins.
Sphinctozoan forms were significant Permian reef builders, pruned significantly by P-Tr extinction, and "extinguished" in the fossil record at K-P extinction. And yet the living Vaceletia is considered to be a sphinctozoan. A Lazarus taxon or an Elvis taxon?
Never as diverse as other major sponge groups, but calcarean peak diversity is during Cretaceous, matching the pattern from other major groups.
Demospongea: stove-pipe sponge Aplysina archeri and barrel sponge.
Demospongea (AKA Demospongia, Demospongiae (!)): (Cambrian - Quaternary) Roughly 90% of modern sponges. Characteristics:
All leucon grade
Spongin generally present
Spicules, when present, are of amorphous silica and may come in a variety of shapes. In contrast to hexactinellids (see below), their rays are never at right angles.
Internal transport of dissolved silica is mediated by silicase, chemically very similar to carbonic anhydrase. Sclerocytes deposit amorphous silica blobs onto a matrix of silicatein and glyconectin in side a vacuole, then export into mesohyl. Note that in this case, effort is expended to promote silica deposition.
Some with encrusting morphology lack spicules or spongin.
Less limited to shallow waters than Calcarea. (Consistent with their reliance on silica.)
Massive external skeleton, if present, made of aragonite (cf. Calcarea.)
Diversity: Too great to explore here, but likely to include some oddballs such as:
find Porifera to be distinctly paraphyletic, with Homoscleromorpha, Calcarea, and Demospongea to be sequentially remote from Eumetazoa.
Dohrmann et al., 2008 find weak support for poriferan monophyly. Calcarea and Homoscleromorpha are sister taxa, but their big news is the Demospongea is paraphyletic with respect to Hexactinellida.
Nosenko et al., 2013 have the current last word. In their analysis, results differ depending on which part of the genome is sampled, however their combined analysis finds Calcarea and Homoscleromorpha to be sister taxa. They are closer to Eumetazoa than the monophyletic Demospongea and its sister taxon - Hexactinellida.
Given the morphological similarity of Homoscleromorpha to some demosponges, it is odd that molecular phylogenies consistently find Homoscleromorpha close to Calcarea with whom they lack morphological or cytological synapomorphies and pair Demospongea with Hexactinellida.
Botting et al., 2017 report on Conciliospongia anjiensis from the Late Ordovician - a stem demosponge with hexactinellid-style spicules. Strong support for the molecular pairing of Demospongea and Hexactinellida.
Whatever their phylogeny, sponges may be the most ancient metazoans. Claims for precambrian sponge fossils include:
McCaffrey et al., 1994, describe the presence of 24-isopropylcholestane, a steroid associated with Demospongea in 1.8 Ga rocks. Whether these represent actual sponges or the biochemical traces of choanoflagellates is unclear.
Li et al. 1998, describe 580 Ma silicate sponge spicules from Doushantou, Guizhou, China, along with possible soft-tissue fossils of demospongean character.
Brain et al. 2012, describe Otavia antiqua, 760 - 580 Ma putative body fossils of small (0.3 - 5 mm) sponges from the Cryogenian Otavi and Ediacaran NaMa groups of Namibia. Spicules are absent, but the fossils are calcified and show an ascon-grade morphology. Arguably the earliest convincing poriferan-grade organisms.
Clites et al. 2012, describe Coronacollina acula (right), Ediacaran putative body fossils of small (10 mm) thimble-shaped sponges from the Ediacaran Rawnsley Quartzite of Australia with an odd array of up to four long spicules.
Maloof et al. 2010, describe an earliest Ediacaran modular organism without symmetry and with a network of interior canals that lead to circular surface openings. Sponge-like but lacking oscula and unambiguous spicules. (Silica particles present in the fossil may be either precursors of spicules or be diagenetic.)
Before we get too excited, Antcliffe et al. 2014 reject these claims. Their conservative approach identifies the earliest sponges as hexactinellids from the earliest Cambrian of Iran.
Problematic fossil poriferans (?):
Chaetetida: (Ordovician - Quaternary) Encrusting laminar form with skeleton of closely packed upright tubes and, rarely spicules. Enigmatic as fossils, stimulating speculation that they were algae or tabulate corals. Long thought to have died out in Miocene. Discovery of the living representative Acanthochaetetes wellesi, with siliceous spicules, clinched the argument that they belong to Demospongea.
Form binding laminations of their massive external skeleton.
The external skeleton is composed of high-Mg calcite.
Hard parts consists of upright tubes with tabulae.
Binding reef organisms, requiring hard substrate initially.
Restricted to cryptic low-light environments such as reef cavities and overhangs.
Stromatoporoidea: (Ordovician - Quaternary?): Monophyletic group or polyphyletic assemblage of Elvis taxa? Stromatoporoids, massive calcareous encrusting organisms, were important Paleozoic reef-builders that require our attention. Note: Don't confuse with stromatolites, even when they occur together.
Encrusters with calcareous (high-Mg calcite) laminated massive external skeletons characterized by laminations separated by columns.
The living tissue occupied spaces between the upper laminations while lower ones (occupied previously) were back-filled with calcite.
Surface had swellings called mamelons, surrounded by radiating grooves called astrorhizae. Mamelons thought to indicate the sites of excurrent openings.
Cross-section of stromatoporoid encrustation of Late Silurian Keyser Limestone at Cumberland Cave, MD.
Make a comeback during the Mesozoic, but never regain former glory. Are the Mesozoic stromatoporoids members of the same group, or are they ecologically convergent Elvis-taxa?
"Sclerospongea": As long as stromatoporoids were extinct, their true nature (alga? sponge? coral?) was debated. The issue was resolved when living cryptic sclerosponges were discovered. They had:
External massive skeletons
Mamelons and astrorhizae
Thus, stromatoporoids have more recently been regarded as fossil sclerosponges.
Are sclerosponges Elvis taxa? Hard to say, but (contrary to your textbook) it seems clear that living sclerosponges are polyphyletic with members distributed within Demospongea (Chombard et al., 1997). They resemble stromatoporoids so strongly that we are at least secure in viewing living sclerosponges and stromatoporoids as members of Demospongea. Beyond that, they probably represent an ecomorph that has evolved several times.
Before you conclude that all enigmas have been resolved...
Archaeocyatha: (Early - Middle Cambrian). Considered "poriferan grade" based on general body plan, but there is no consensus on their phylogeny. Reitner, 1990 found them to be nested within Porifera. If "Porifera" is paraphyletic, then GORK. At best, we assert that they branch close to, if not within Porifera.
Perforate calcareous hard tissues with double-walled cone-in-cone structure:
Calcareous outer and inner walls separated by septa. (Diagenetic alteration makes it unclear whether this was secreted as calcite or aragonite.)
Intervallum that contained the living tissue enclosed by walls.
All calcareous partitions perforated by pores. As in sponges, these are wider in the inner wall.
In some, tabulae and dissepiments reminiscent of cnidarians are present.
Shallow, warm carbonate shelf environments of normal salinity.
Often occur together with algae, indicating good illumination, and bacterial stromatolites.
Although most individuals were solitary, some were colonial
Considered the first major reef framework building organisms, although it was usually the algae and bacteria that they lived with that did the actual binding.
Common and speciose during Early Cambrian.
Extinguished during Middle Cambrian.
Ecologically replaced by recognizible sponges and cnidarians.
A Final Thought:
I withheld one hypothesis of poriferan phylogeny - the minority view of Maldonaldo, 2004, who regards choanoflagellates as being derived from Demospongea through a process of paedomorphic simplification. Sounds strange, but is based in part on the observation that some choanoflagellates are capable of secreting internal structures of amorphous silica and the quite reasonable argument that in sponges, the ability to secrete silica was probably derived secondarily from the secretion of calcite.
Is it insane? Our aesthetic of evolutionary progress compels us to view choanoflagellates as precursors to poriferans, but nature isn't obliged to cooperate. Maybe Proterospongia is a drastically simplified poriferan, and choanoflagellates are choanocytes that have shaken free of their association with other cells. More data, please.