Spongebob is a child of snowball Earth

Image from commons.wikimedia.org

Although looking a little like plants, sponges (Phylum Porifera) are animals. Admittedly, they area very different kind of animal from the ones we see around us in everyday life. Unlike most others they lack bodies constructed from properly organized tissues, they are instead more like giant colonies of single cells. Indeed a famous experiment demonstrated that sponges that have been completely disaggregated into its constituent cells (by forcing them through a fine-mesh screen*) will begin to reconstitute themselves. Sponges lack any sort of gut, they instead live by sieving fine organic particles out of seawater. The food is absorbed directly by specialized ‘collar cells’ (more formally choanocytes) that line the canals and chambers that run through the sponges body. Sponges are also remarkable for their unique skeletons, which are generally made of tiny to microscopic spicules of silica or calcite or a lacy network of elastic organic material known as spongin (as in the original bath sponges). As you might expect with animals that lack a gut, nervous system or indeed organs of any sort, sponges are a very early branch of the animal tree. Indeed the tiny little disc of cells known as Trichoplax adhaerens may be the only living animal that branched away before sponges and all other animals split. Actually I’m oversimplifying here, because the evidence is looking good for sponge paraphyly. That means some of the different sponge groups are more closely related to tissue-grade animals (a clade called Eumetazoa) than to other sponges, so it wasn’t a single sponge-eumetazoan split. The remarkable conclusion that leads to is that we are directly descended from an animal that we would call a sponge.
Given their early divergence and simple construction, one would expect sponges to have a venerable fossil record. Indeed they do, but not quite as long as one might expect. Sponge spicules seemed to appear in the fossil record at the beginning of the Cambrian Period along with a great number of eumetazoan groups (now dated to 542 million years). Some spicules have been reported from older strata but these are not without controversy. In contrast eumetazoans clearly had an older fossil record (e.g. the 545-565 million year old Ediacaran fauna). The mid 1990’s saw the publication of Palaeophragmodictya, the first probable whole body fossils of sponges from the Ediacaran fauna. Nevertheless without spicular preservation (like other ediacaran macrofossils Palaeophragmodictya are preserved as impressions on the base of sandstone beds) there may always be some doubt as to its identity. What remains unusual is that it took so long for such Ediacaran sponges to be found and that they remain a very rare component of Ediacaran faunas.



Small individuals of the putative Ediacaran sponge Palaeophragmodictya. From Gehling and Rigby (1996)



Close up of a large Palaeophragmodictya showing what might be the impression of a spicular mesh.From Gehling and Rigby (1996)

Furthermore divergence dates calculated using molecular clock methods suggested a sponge- eumetazoan divergence of 650 million years. If the common ancestor was itself a sponge-grade organism we should expect the record of sponges and sponge-grade animals extending back to pre-Ediacaran times. This is well illustrated in the following diagram that teases apart the so-called ‘Cambrian explosion’(image from www.snowball.org). An interesting aspect of this molecular date is that it extends the range of animals back into a Period known as the Cryogenian, or just after it.



What is special about the Cryogenian? It was period in Earth history lasting from 750-620 million years where the Earth went through several severe glaciations events known as ‘snowball earths’. Although the exact severity of the snowball-earth glaciations is a contentious topic, there is convincing evidence that the Earth was cold enough to support sea-level glaciers in the equatorial belt. So an important question is: had animal divergence begun in the Cryogenian as the molecular divergence dates suggest? That question has been conclusively answered this year in a Nature paper by Gordon Love and colleagues.
Love et al. found convincing sponge fossils in sediments securely dated to the age of the Marinoan glaciation, the last snowball earth glaciations event of the Cryogenian. As a small aside the Marinoan is named after the seaside suburb of Marino, on the southern coast of Adelaide, my home town. My first ever geological field trip for my degree was looking at the Marinoan rocks of Marino. Anyway enough reminiscing, onto the Cryogenian sponges fossils. What were they? Spicules? Whole body impressions? No, Love et al. found molecular fossils, in particular 24-isopropylcholestanes. These particular hydrocarbons are, according to the authors, the degraded products of C30 sterols, a class of molecules only produced by members of the sponge class Demospongiae (here I have to accept the author’s word, I know far too little about organic chemistry to have any way of assessing the veracity of this statement). An interesting feature of snowball Earth Glaciations is that they are usually covered by a thin but continuous layer of carbonate rock: the 'cap carbonates'. These are thought to have precipitated out under extraordinarily hot conditions bought on by the retreat of the glaciers leaving behind an atmosphere dense in CO2 (which would accumulate while terrestrial weathering was essentially shut down underneath the ice-cover). Anyway these molecular sponge fossils are found in rocks below the cap carbonates, that is during the glacial period itself.
The implications are pretty huge. It means that multicellar animals arose and first diversified in frigid seas largely covered by ice, and not during the flush of warmth that suffused the planet immediately after the glaciers lost their grip. Where could animals exist in such a sea? There were probably numerous little oases of light where cracks in the relatively thin equatorial sea ice would allow local blooms of bacteria and algae. These little patches may well have been the birthplace of multicellular animal life.


A modern day equivalent of the oases that was the birthplace of animal life? Image from www.snowball.org.

References
Gehling, J.G. and Rigby, J.K. (1996) Long Expected Sponges from the Neoproterozoic Ediacara Fauna of South Australia. Journal of Paleontology 70: 185-195.

Love, G., Grosjean, E., Stalvies, C., Fike, D., Grotzinger, J., Bradley, A., Kelly, A., Bhatia, M., Meredith, W., Snape, C., Bowring, S., Condon, D., & Summons, R. (2009). Fossil steroids record the appearance of Demospongiae during the Cryogenian period Nature, 457 (7230), 718-721 DOI: 10.1038/nature07673

*They were the luckiest of all

Misleading Mitochondria and Ancient Neopterygian Fossils

Last post we looked at the basics of ray-finned fish classification and some of the problems associated with them. Foremost among these are two rather dramatically different topologies. Morphology supports a clade called the Neopterygii which includes ginglymods, halecomorphs and teleosts whereas mitochondrial genetics support an ‘Ancient Fish Clade (AFC)’ that groups chondrosteans, ginglymods and halecomorphs to the exclusion of teleosts. Divergence dates based on the molecular clock are also dramatically older than minimal dates based on the fossil record. Hurley et al. (2007) tackle both problems with a two-pronged approach. Firstly they relook at the early ray-finned fossil record, scrutinizing it for the first appearance of derived characters diagnostic of these major groups and incorporating the data into a new cladistic analysis. Secondly they assembled a new, comprehensive molecular data set of four nuclear genes 29 species covering all the relevant clades (except the cladistians), thus is the first analysis capable of addressing the timing of the whole genome duplication event.
The tree based on the morphological data found strong support for the Neopterygii and virtually no support for the ‘Ancient Fish Clade’ at all. Indeed when the AFC topology was enforced upon an analysis that included only the living taxa the tree length grew by 80 steps (125% of the number of steps in the shortest possible tree) and found just one character that could be interpreted as a synapomorphy of this clade. Clearly the morphology doesn’t just fail to support the molecular ‘AFC’ it is strongly contradicting it. Analysis of the nuclear gene data also strongly supports the neopterygian clade over the AFC. Thus the signal for the AFC is coming from the mitochondrial genes alone. Given that this data set is so at odds with morphology, nuclear genes and the fossil record it seems likely that the source of error is the mitochondrial data. Perhaps more interesting is the morphological analysis that includes the fossils. Neopterygii continues to be strongly supported but the divergence date estimates have changed. Two fossils in particular were found to be significant: Brachydegma and Discoserra. Brachydegma from the Early Permian (285 million years) of Texas was previously regarded as a basal actinopterygian that diverged before the chondrostean-neopterygian split. However Hurley et al. found that it had a number of characteristics of Halecomorpha (that is the bowfin and its fossil relatives), such as an enlarged gular plate, a medial shelf at the front end of the maxilla, and possibly a posteriorly indented maxilla. The latter character is less secure because it depends on the interpretation of a small elliptical patch of differing ornament on the rear edge of the maxilla. If this patch is interpreted as a fused-on scale, then the maxilla does have the classic halecomorph indented maxilla (see figure below).



Brachydegma (from Hurley et al. 2007) on the left and the modern bowfin (Amia) on the right (not to scale; from Grande and Bemis 1998). Two diagnostic features of the Halecomorphi are colourised – the posteriorly indented maxilla (red) and the very large gular plate (green).

Sure enough Brachydegma comes out as the basal most member of the Halecomorphi in their analysis. As an halecomorph, Brachydegma is part of the neopterygian crown-group and pushes the origin of this clade back the Palaeozoic Era, before the big extinction event at the end of the Permian Period. The previous oldest known crown-group neopterygians were the parasemionotids (also halecomorphs) from the Early Triassic of Madagascar and Greenland. Discoserra from the Early Carboniferous (320 million years) of Montana (the famous Bear Gulch Limestone fish deposits) is a far older fish, and is not apparently a member of the neopterygian crown group but it has many of the synapomorphies of the crown-group indicating that by this early stage the neopterygian bodyplan was mostly in place. Previously Discoserra was thought to be an early cladistian.



Discoserra, from Lund 2000.

The new fossil data places the origination of the neopterygian crown group into the Paleozoic Era, long before the big Permo-Triassic mass extinction event of 251 million years, and at least 40 million years earlier than the previous oldest crown-group neopterygian and somewhat closing the gap between the molecular and palaeontological dating of the Neopterygian crown-group origination. Furthermore molecular clock dating using the nuclear gene data, rather than the mitochondrial genes yields a more recent range of dates 271-371 million years that actually ecompasses the age of Brachydegma, thus the discrepancy is more or less resolved. Once again it appears that the mitochondrial genes are giving misleading results, but why this is so is not immediately clear. No particularly ancient crown-group teleosts were recognized in this study so the fossil based minimum age for this clade is unchanged. However the new nuclear genetic data were used to estimate the divergence of the crown group. Like the estimates for the age of the neopterygian crown-group the estimates for the teleost crown-group based on nuclear genes are considerably younger than the estimates based on mitochondrial data. Thus using these new age estimates the discrepancy between molecular and palaeontological dates closes to a minimum of 30 million years.
Lastly Hurley et al. look at the timing of the whole genome duplication and how it relates to the explosive radiation of teleost fishes. The duplication event is indeed shown to be a feature of the teleost stem, as its products appear to be present in all living teleosts but are not found in the other surviving actinopterygian groups. This suggests that the duplication event most likely happened sometime in the Permian or Triassic, with the most recent possible occurrence being the Mid Jurassic, before the first appearance of crown-group teleosts in the fossil record. However the explosion in teleost diversity does not get underway until the Late Cretaceous, demonstrating a considerable lag between the duplication event and the rapid diversification event. This falsifies the hypothesis that the duplication was the direct causative agent of diversification.
In conclusion, this is a case where the morphological signal appears to have given a more reliable estimate of phylogeny than mitochondrial genes, whereas the huge discrepancy in divergence date estimates were a product of both overlooked fossil data and misleading signal based on the same unreliable genetic data.

Grande, L. and Bemis, W.E. (1998) A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. Society of Vertebrate Paleontology Memoir 4: 1-690.

Hurley, I.A., Lockridge Mueller, R, Dunn, K.A.,Schmidt, Friedman, M., Ho1, R.K., Prince, V.E., Yang, Z., Thomas, M.G. and Coates, M.I. (2007)A new timescale for ray finned fish evolution. Proc. R. Soc. B 274, 489–498

Lund, R. (2000) The new actinopterygian order Guildayichthyiformes from the Lower Carboniferous of Montana (USA). Geodiversitas 22, 171-206.

A paper you may have missed

Images courtesy of Fernando Abdala

Today I’m showcasing a little paper on some very intriguing little teeth (shown above) from the Triassic of South Africa that appeared last year (Abdala et al. 2007). It didn’t make much of an impact partly because of its location (the local ‘South African Journal of Science’) and perhaps also because no firm conclusions could be reached. Nevertheless it deserves comment because whatever the teeth turn out to belong to they are significant, indeed they have the potential to be extremely significant.
The teeth in question were recognised when Helke Mocke, then an honours student at the BPI who was being supervised by Fernando Abdala, was attempting to find isolated cheek teeth of Bauria, a therocephalian therapsid with some striking convergences with mammals. Helke was attempting to test the hypothesis that Bauria was an herbivore by looking for dental microwear on the cheek teeth. Most of the Bauria in our collections either have the lower jaws tightly clamped against the upper jaws making it impossible to see the chewing surfaces of the teeth, or had the teeth mechanically prepared out of hard matrix with airscribes and pins, potentially adding a whole new set of scratches and microwear that had nothing to do with the diet of the animal. Bauria comes from the middle part of the Burgersdorp Formation of the Karoo Basin. This part of the formation is thought to be latest Early Triassic in age and is also the source of such well known extinct animals as Erythrosuchus, Cynognathus and Kannemeyeria. It is here that I play a very minor role in the story. I suggested to Helke that she might find good Bauria teeth in the older parts of the Burgersdorp Formation. The older parts (known informally as the ‘A zone’) are generally rich in aquatic or subaquatic taxa such as lungfish, hybodontid sharks and temnospondyl amphibians but a rich channel lag deposit found by palaeontologist/geologist John Hancox is crammed with all sorts of small vertebrate fossils, including some terrestrial creatures. Amongst them were teeth that had been identified as bauriid. These could be isolated by simple surface picking at the site, or screen washing in the lab. So Helke proceeded to look at the A zone bauriid teeth with a microscope. As it turned out this was the first time anyone had given these teeth anything more than a cursory glance. Surprisingly they weren’t bauriid teeth at all. Even more surprisingly the crowns of these teeth resembled nothing more than those of early mammals called haramiyidans. Compare the A zone teeth featured above with those of a haramiyidan below)

Haramiyavia, from Jenkins et al. 1997.

Haramiyidans themselves are an enigmatic group known only from teeth and incomplete jaws (apparently there are some postcranials of Haramiyavia but these are rather uninformative). Their cheek teeth bear double rows of small cusps, similar to those of multituberculates, which they are often grouped together with in the clade Allotheria. Multituberculates have a derived therian-like shoulder girdle, indicating that they share a more recent common ancestor with them than monotremes or other major Mesozoic mammal groups like eutriconodonts, docodonts and morganucodonts. The earliest haramiyidans are from the late Norian Stage of the Late Triassic. If they are truly early relatives of the multis then they would push back the origin of crown group mammals, and even more significantly advanced theriimorph mammals, to a time 45 million years or more before the next oldest appearance of this clade in the fossil record. If the A zone teeth are also regarded as allotherian then we have the appearance of theriimorph mammals before the appearance of probainognathians, at a time when only the earliest eucynodonts had just made their appearance. Clearly this is strongly at odds with the known fossil record. At this point I think there are three main hypotheses that can explain these teeth. I order them here from what is in my opinion the most likely to the least likely. 1) The A zone teeth are convergently similar to haramiyidans and do not belong to a mammal at all. 2) The A zone teeth are early haramiyidans but haramiyidans are themselves an early branch of cynodonts and are not mammals. 3) The A zone teeth are haramiyidans and haramiyidans are allotherian mammals. This last hypothesis implies a huge stratigraphic debt, with ghost lineages for chiniquodonts, probainoganthids, trithelodonts, tritylodonts, morganucodonts, Sinoconodon, docodonts, Hadrocodium, Kuehneotherium, australosphenidians and stem trechnotherians all extending back to the Early Triassic.
Multicusped rasping teeth have evolved multiple times in synapsid evolution with tritylodontids, multituberculates and ektopodontids all being independant examples (I am sure there are more). The A zone teeth are single rooted (like basal cynodonts but unlike almost all advanced cynodonts including mammals and haramiyidans) which supports hypothesis 1.
If they are only convergently mammal-like then what are they? We can't say now but I like the idea that maybe they are derived bauriids afterall. The answer will be forthcoming from the next field trip, I hope.
Oh, we still don't know what Bauria ate.

References

Abdala F, Mocke H, Hancox PJ (2007) Lower Triassic postcanine teeth with allotherian-like crowns. South African Journal of Science 103: 245-247.

Jenkins FA Jr, Gatesy SM, Shubin N, Amaral WW (1997) Haramiyids and Triassic mammalian evolution. Nature 385: 715-718.