More Mysterious Palaeogene Eutherians

A few weeks ago, I wrote a post about some of the distinct groups of eutherian mammals that waddled through the world during the Palaeocene, the time period that followed directly after the end of the Cretaceous. At the time, many of the modern groups of mammals were either still fairly marginalised or yet to put in an appearance, and the relationships of most of those primordial eutherians such as pantodonts and taeniodonts remains a remarkable mystery. In this post, I thought I'd focus on one of those early groups that seems to get given an even shorter shrift than most (in fact, this post will be unillustrated because my attempts to find suitable free images online drew a complete blank) - the Tillodontia.

Tillodonts are known only from the Palaeocene and Eocene of North America and Eurasia. Most authors have recognised a single family, the Esthonychidae, though Lucas & Schoch (1998) positioned the genera Lofochaius and Basalina as a paraphyletic series outside that family*. They were medium to large herbivores (one of the later genera, Trogosus, may have weighed around 150 kg - Lucas & Schoch, 1998). Like most mammals of the time, these would not have been the most graceful of beasts - they would have probably been built more like a barrel on legs, perfect for the moist, densely-forested conditions of the time. One of the most distinct features of the tillodonts was the development of large, rodent-like incisors, which in one later clade became open-rooted and permanently-growing like those of rodents. The powerful dentition this gave tillodonts, together with the sturdy legs and claws found in those few species for which post-cranial material is known, would have allowed them to tackle some pretty resilient food-sources, and it is easy to imagine them gnawing bark off trees or digging up roots. A similar lifestyle appears to have also characterised another group of Palaeogene herbivores, the taeniodonts, which also developed rodent-like gnawing teeth. It was once suggested on this basis that taeniodonts and tillodonts were closely related to each other, but the gnawing teeth in taeniodonts were the canines, not the incisors, so the two groups could not have possibly shared a common gnawing ancestor.

*The authors of the late Palaeocene Chinese genus Yuesthonyx (Tong et al., 2003) established a new family for it, Yuesthonychidae. Not only would this family be redundant with its single genus, but Rose (2006) implies that Yuesthonyx is a more derived form not far from the origin of the Trogosinae (see below), making the recognition of a separate family for it all the more pointless.

The very earliest tillodonts such as Lofochaius and Meiostylinodon come from the Lower Palaeocene of China, and this would appear to represent the place of origin for the clade (Rose, 2006). The early Chinese genera were much smaller than the later trogosines, and had less exaggerated dentition. The first North American tillodonts make their appearance in the very end of the Palaeocene with the similarly generalised Azygonyx which survived into the beginning of the Eocene alongside Esthonyx, the most common genus of tillodonts. These forms all lacked permanently-growing incisors, the appearance of which marks the appearance of the clade Trogosinae in the Eocene. Trogosines are known from both North America (Tillodon and Trogosus) and China (Higotherium and Chungchienia), so their geographic origins are unclear. The Chinese Chungchienia had the most advanced dentition of any tillodont - not only were the second incisors a whopping 26 cm long(!), but the ever-growing rootless condition of the incisors was extended to the cheek-teeth (Chow et al., 1996), implying that it must have had an exceedingly tough diet.

While it is fairly well-established that tillodonts were not related to taeniodonts, it has been a decidedly more difficult prospect to establish exactly what they are related to. Van Valen (1963) suggested a close relationship to Arctocyonidae, a family of "condylarths", but this was based on comparisons with the relatively derived North American Esthonyx rather than the mostly then-undiscovered Asian genera. More recent authors have suggested a relationship with the pantodonts, with which tillodonts share dilambdodont cheek teeth. Basal tillodonts may also be difficult to distinguish from basal pantodonts (Rose, 2006). The Palaeocene North American Deltatherium may also be relevant to the origin of tillodonts. However, none of these groups has yet been subject to a proper cladistic analysis to determine whether their shared features indicate actual relationship or convergence. And even if these taxa do form a monophyletic clade, this still just takes a number of small problematic clades of unknown relationships to modern taxa and turns them into one big clade of unknown relationships to modern taxa!

REFERENCES

Chow, M., J. Wang & J. Meng. 1996. A new species of Chungchienia (Tillodontia, Mammalia) from the Eocene of Lushi, China. American Museum Novitates 3171: 1-10.

Lucas, S. G., & R. M. Schoch. 1998. Tillodontia. In Evolution of Tertiary Mammals of North America (C. M. Janis, K. M. Scott & L. L. Jacobs, eds.) pp. 268-273. Cambridge University Press.

Rose, K. D. 2006. The Beginning of the Age of Mammals. JHU Press.

Tong Y.-S., Wang J.-W. & Fu J.-J. 2003. Yuesthonyx, a new tillodont (Mammalia) from the Paleocene of Henan. Vertebrata PalAsiatica 41: 55-65.

Van Valen, L. 1963. The origin and status of the mammalian order Tillodontia. Journal of Mammalogy 44 (3): 364-373.

Turkey-lion-butterfly-scorpion-zebra

Today marks another first for Catalogue of Organisms - for the first time, the Taxon of the Week post is focusing on a single species. Specifically, the tropical fish Dendrochirus zebra (Cuvier, 1829)*, commonly known as dwarf lionfish, zebra turkeyfish, zebra butterfly-cod and doubtless a whole host of others of which I'm not even aware. And a very attractive animal it is too, as you can see in the photo above by K. Uchino. Dendrochirus zebra is a widespread species on reefs in the tropical Indian and Pacific Oceans. A map, as well as a whole heap of other information, can be found on FishBase.

*Things are a little confusing regarding the authority of this species - some sources (including FishBase) cite Cuvier (1829), while others such as Munro (1958) point to Quoy and Gaimard (1824). I have no idea which is correct.

The lionfishes or firefishes are two genera (Pterois and Dendrochirus) forming the subfamily Pteroinae of the family Scorpaenidae, the scorpionfishes (though Smith & Wheeler, 2006, found the pteroines to be more closely related to the Sebastidae rather than the Scorpaeninae). The differences between the two genera are fairly minimal, and a molecular phylogenetic analysis of seven (of thirteen) species of pteroines by Kochzius et al. (2003) failed to resolve their relative monophyly. Dendrochirus zebra was actually originally described as a species of Pterois (Munro, 1958), and it seems a return might be in order - proving once again that vertebrate workers tend to oversplit their genera. The name Dendrochirus ("tree-hand") refers to one of its supposed distinguishing characters, that some of the upper rays in the pectoral fin are branched. The other distinguishing character is that, unlike Pterois, Dendrochirus never has the upper pectoral rays free from the membrane.



The spectacular coloration of the pteroines makes them instantly recognisable, though the above photo of Dendrochirus zebra by Richard Ling shows quite well how the fish are not quite so obvious against a colorful reef background as one might expect. Like other scorpaenids, lionfish are slow-moving ambush predators. Their somewhat glum expression is the result of their relatively gigantic maws, which open up to inhale just about anything that can fit. Lionfish also resemble other scorpaenids in the presence of painfully venomous spines in the dorsal, ventral and anal fins. This toxicity has not prevented D. zebra from becoming popular in the marine aquarium industry. While D. zebra has spawned in captivity (FishBase), the majority of captive specimens would appear to be wild-caught. Unfortunately, FishBase suggests that this species is a relatively slow breeder and moderately vulnerable to overfishing.

One last thing which, though it relates not to Dendrochirus zebra but to another pteroine, is something I stumbled across while researching this post that is just too cool not to share. Take a look at the two photos below:



The above photos come from Fishelson (2006). The upper photo shows a typical individual of Pterois volitans, the red firefish. The lower photo shows a variant with the supraoral tentacles flattened into feather-like ornaments. Such a variant was first sighted near the southern end of the Sinai peninsula in the early 1980s. Since then, records of variant individuals have slowly spread southwards, and have since been recorded as far south as Kenya and the Comoros. While variant individuals remain extremely rare, they do seem to be slowly increasing in abundance...

REFERENCES

Fishelson, L. 2006. Evolution in action-peacock-feather like supraocular tentacles of the lionfish,
Pterois volitans – the distribution of a new signal. Environmental Biology of Fishes 75: 343-348.

Kochzius, M., R. Söller, M. A. Khalaf & D. Blohm. 2003. Molecular phylogeny of the lionfish genera Dendrochirus and Pterois (Scorpaenidae, Pteroinae) based on mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 28 (3): 396-403.

Munro, I. S. R. 1958. The fishes of the New Guinea region: A check-list of the fishes of New Guinea incorporating records of species collected by the Fisheries Survey Vessel “Fairwind” during the years 1948 to 1950. Papua and New Guinea Agricultural Journal 10 (4): 97-369 (reprinted 1958. Territory of Papua and New Guinea Fisheries Bulletin no. 1).

Smith, W. L., & W. C. Wheeler. 2006. Polyphyly of the mail-cheeked fishes (Teleostei: Scorpaeniformes): evidence from mitochondrial and nuclear sequence data. Molecular Phylogenetics and Evolution 32 (2): 627-646.

Chain, Chain, Chain

Hou, X.-G., D. J. Siveter, R. J. Aldridge & D. J. Siveter. 2008. Collective behavior in an early Cambrian arthropod. Science 322: 224.

Fossils can offer fascinating insights into the lives of long-extinct organisms. Sometimes, the lifestyles suggested are so different from anything found in living taxa that we may be at something of a loss to understand their function and significance. The new publication linked to above reports on the fascinating discovery of a collection of early arthropods from the famed Chengjiang fauna of China. (For those unfamiliar with it, the Chengjiang is similar to the Burgess Shale of North America, but even more impressive - it is only the fact that the latter was discovered earlier that gets it more press).

The fossils are of an animal very similar to Waptia, a previously-known, superficially shrimp-like animal of uncertain affinities. Waptia is not uncommon as a Cambrian fossil - according to Taylor (2002), it is the third-most common animal in the Burgess Shale, with over 1000 specimens held by the American National Museum of Natural History. Despite this abundance, Waptia has not been described in detail since Walcott's original preliminary description in 1912 (Taylor, 2002, says that he is working on a revision, but this doesn't seem to have appeared in print yet). Hou et al. (2008) refer to it as a stem-crustacean, but do not specify on what grounds. It could just as easily be a stem-chelicerate, as are the majority of known Cambrian arthropods (Cotton & Brady, 2004).

What makes this new finding so remarkable can be seen in the figure below from Hou et al. (2008). A group of 22 individuals is preserved together, each arranged head to tail in a long chain. As shown in the close-up in fig. 1C, each individual has the tail-end of the individual ahead of it cavered by its carapace. There is no evidence that the animals were lined up in a burrow, so they were most likely living above the sediment surface. The fact that the chain has not broken apart as the animals were buried indicates that they must have had an extremely firm hold on each other in life. Hou et al. interpret the chain as having been pelagic, but that seems unlikely to me - the sheer abundance of Waptia in the Burgess shale seems more consistent with a life close to the sediment surface, which would offer more opportunities for burial. Cambrian animals more likely to be pelagic, such as Amiskwia and Nectocaris, are very rare as fossils.



What on earth were these animals doing lined up like that? Hou et al. claim that such behaviour is unique, but I'm not sure just how unique. Hou et al. claim that lines formed by modern arthropods such as crayfish (for migration) and some caterpillars (feeding) are "more trains than chains", but don't explain exactly what is the difference (the curse of the super-compressed Science format strikes again?) Certainly, I've seen fireblight caterpillars here in Perth form very closely-linked chains, and one of the most horrifying sights I've ever seen was a mass of about twenty fireblights, so closely coiled that it was hard to tell where one finished and another began, moving as one. The waptiid assemblage is unlikely to be connected to feeding, as the close proximity of the mouth of one and the anus of another makes such an arrangement rather too horrible to consider. Hou et al. favour a connection to migration, probably for defense, which is a distinct possibility. I would suggest that the chain could have also been related to mating behaviour. Some animals, such as some marine gastropods, can form chains of multiple intermating individuals. Hou et al. (2008) dismiss this possibility on the grounds that "there is no precedent of arthropods of comparable aggregation for fertilisation". However, living arthropods show an absolutely enormous diversity of mating behaviours. Is it that much of a stretch to entertain the possibility that extinct forms may have shown even more?

REFERENCES

Cotton, T. J., & S. J. Braddy. 2004. The phylogeny of arachnomorph arthropods and the origin of the Chelicerata. Transactions of the Royal Society of Edinburgh: Earth Sciences 94: 169-193.

Taylor, R. S. 2002. A new bivalved arthropod from the Early Cambrian Sirius Passet Fauna, north Greenland. Palaeontology 45 (1): 97-123.

Tortoise Resurrection

In a subsequent portion of this narrative I shall have frequent occasion to mention this species of tortoise. It is found principally, as most of my readers may know, in the group of islands known as the Gallipagos... They are frequently found of an enormous size... They can exist without food for an almost incredible length of time, instances having been known wher they have been thrown into the hold of a vessel and lain two years without nourishment of any kind - being as fat, and, in every respect, in as good order at the expiration of that time as when they were first put in... They are excellent and highly nutritious food, and have, no doubt, been the means of preserving the lives of thousands of seamen employed in the whale-fishery and other pursuits in the Pacific.

--Edgar Allen Poe, The Narrative of Arthur Gordon Pym of Nantucket

For sailors in tropical oceans before the invention of refrigeration, keeping supplies of food was a serious issue. It was a permanent challenge to keep supplies fresh and edible, and indeed, much of the time stores failed at both. Under such conditions, the giant tortoises of the Galapagos islands and the Mascarenes and other islands in the Indian Ocean would have been seen as nothing short of miraculous. Tortoises could be captured easily and kept in the hold of a boat for extended periods without feeding, only slaughtered when they were actually required for eating. As a result, ships that were in a position to do so often took on tortoises in large number, and Charles Darwin apparently recorded single vessels taking up to 700 individuals at a time. By modern standards the idea of seven hundred starving tortoises crammed into a single hull seems unthinkably cruel, but doubtless the sailors who otherwise faced another six months of decomposing ship's biscuit saw things differently.


Geochelone becki, the Volcano Wolf tortoise. Photo by Joe Flanagan.

Unfortunately, such intense harvesting took an inevitable toll. Tortoise numbers declined rapidly, and many went extinct. Honneger (1981) lists three extinct species of tortoise from the Galapagos (including Geochelone abingdoni from Pinta island, which is technically not yet extinct but which only survives in the form of a single captive male) and at least six extinctions from the Seychelles and Mascarenes. Extinct populations on the Galapagos islands of Rabida and Santa Fe may have represented further undescribed species.

However, a paper published yesterday in the Proceedings of the National Academy of Sciences adds a remarkable coda to the history of one of the "extinct" species, the Floreana tortoise Geochelone elephantopus. Using DNA extracted from museum specimens collected on Floreana before the population disappeared, Poulakakis et al. (2008) have demonstrated that G. elephantopus may not be quite as extinct as previously thought. Instead, anomalous genetic haplotypes previously identified in some living individuals of Geochelone becki, a species found on the Volcano Wolf at the northern end of Isabela, the largest island in the Galapagos, indicate descent from G. elephantopus. These individuals would appear to be descendants of past hybridisations between native Volcano Wolf tortoises and introduced Floreana tortoises.

Such a situation is quite believable. As a result of the widespread transport of tortoises for food, many tortoises ended up on islands to which they were not native*. Tortoises were regularly imported to Réunion in the Mascarenes after the native population became extinct. Living populations of giant tortoises on the Granitic Islands of the Seychelles probably descend from imports from Aldabra rather than representing the species originally found there (Honegger, 1981). According to Poulakakis et al. (2008), some 40% of the Volcano Wolf tortoises tested showed evidence of Floreana ancestry, so the genetic legacy of Geochelone elephantopus is alive and well, at least in hybrid form.

*Potentially a serious issue for taxonomy, as researchers cannot assume that species names based on inadequate type material necessarily represent the species native to the island the type was collected on. Honegger (1981), for instance, cast doubt on whether Geochelone gouffei, known from a single specimen found on Farquhar Island in the Seychelles, actually originated there.

This still leaves a significant problem - most conservation policies do not cope well with hybrids. A number of species worldwide, such as the black stilt (Himantopus novaezelandiae) in New Zealand, are regarded as endangered because of the risk of hybridisation with related species. The red wolf (Canis rufus) and the Florida panther (Puma concolor coryi) represent two 'endangered' taxa in the United States for which the suggestion that their histories could have been compromised by hybridisation led to the suggestion that they should be abandoned as worthwhile conservation targets. However, the disappearance or decline of a species in its pure form due to hybridisation with another species is a different proposition from its decline due to replacement by that species. The genetic legacy of the declining species may still persist. Overemphasis on species "purity" may actually hinder the conservation of endangered taxa, especially if natural hybrid zones with related taxa exist in the first place (Allendorf et al., 2001). If there are no purebred Florida panthers, should that mean that there is no place for panthers in Florida?

REFERENCES

Allendorf, F. W., R. F. Leary, P. Spruell & J. K. Wenburg. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution 16 (11): 613-622.

Honegger, R. E. 1981. List of amphibians and reptiles either known or thought to have become extinct since 1600. Biological Conservation 19: 141-158.

Poulakakis, N., S. Glaberman, M. Russello, L. B. Beheregaray, C. Ciofi, J. R. Powell & A. Caccone. 2008. Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise. Proceedings of the National Academy of Sciences of the USA 105 (40): 15464-15469.

Linnaeus' Legacy #12 - The Legacy gets crossed by a Black Cat

The newest edition of Linnaeus' Legacy has been put up by Podblack Cat. This month's keywords: Dante's Inferno, sex, mysteries, bet your ass, ants, ants, ants, ants and more ants, stand back and let rip, expensive varieties, tragic tale, goose almost the size of a small plane, Komodo dragons. Enjoy!

Of Macros and Micros

Vorticella, a sessile ciliate of the intramacronucleate class Oligohymenophora. Photo from here.

Today's Taxon of the Week is the ciliate subphylum Intramacronucleata. Ciliates, one of the most famous groups of protozoa, have been touched on previously at the Catalogue of Organisms. They are certainly one of those groups of organisms that get progressively cooler the further one looks. Admittedly, there are few groups of organisms to which that wouldn't apply.

Intramacronucleata is the largest of the two primary subdivisions within the ciliates recognised in the recent years, and includes most well-known ciliates such as George (Paramecium) and George (Tetrahymena), as well as the Georges (Spirotricha) discussed at the post linked to above (names due to an ex-partner of mine who decided that Paramecium was far too unwieldy a word, and henceforth all microbes should be known as George). The other subphylum goes by the even more unwieldy moniker of Postciliodesmatophora (Lynn, 2003). The name refers to one of the more intriguing features of ciliates, the macronucleus. Ciliate cells always contain at least two nuclei, the reproductive micronucleus and the transcriptional macronucleus. Depending on species and life-cycle stage, a ciliate may have between one and twenty micronuclei, and from one to several hundred macronuclei (McGrath et al., 2006). The vast majority of transcription happens from chromosomes contained in the macronuclei. However, when conjugation (sexual reproduction) occurs, the macronuclei break down and only the micronucleus is propagated. Two conjugating ciliates each generate a pair of haploid micronuclei, one of which they donate to the other. The donor and recipient micronuclei then fuse to form the new diploid micronucleus, which gives rise to the daughter cells' macronuclei. (In the post linked to above, I originally said that the macronuclei break down during cell division, but I was wrong. It only happens in conjugation).


Reproductive cycles in ciliates. Diagram from here.

Despite being derived from the micronucleus, the macronucleus is genetically very different from its progenitor. As well as being replicated, the original genome is subjected to an intense processing programme (described in detail by McGrath et al., 2006). The fewer standard chromosomes contained in the micronucleus are fragmented into a larger number of much smaller chromosomes, each of which is usually present in a large number of chromosomes. The most extreme examples are found among the spirotrichs, some of which start with 120 micronuclear chromosomes which they divide up into as many as 24,000 macronuclear chromosomes. Each of these macronuclear chromosomes may comprise only a single gene, and there may be up to 15,000 copies of each one. New telomeres are generated and tacked onto each of the newly-produced chromosomes. Non-functional sections of DNA in the original micronuclear genome such as repetitive elements, introns and transposons (up to 95% of the original sequence) are brutally excised from the daughter chromosomes, which are stitched back together to form unbroken transcriptional templates.

Intramacronucleata get their name because the microtubules involved in macronuclear division form within the nuclear envelope, while the Postciliodesmatophora include one class (the Heterotrichea) in which the microtubules form outside the macronucleus, and one (the Karyorelictea) in which the macronuclei do not undergo division. While micronuclei divide like respectable nuclei by a process of mitosis, macronuclei are anarchists to the core and divide by a poorly-understood process called amitosis. Amitosis differs from mitosis in that there is no mitotic spindle. As a result, the division of chromosomes between amitotically-produced nuclei is not necessarily even, and in some species of ciliate one daughter nucleus will regularly contain more than twice as many chromosomes as the other. This may explain why ciliate macronuclei may contain such a ridiculous number of copies of each chromosome. When one also factors in that macronuclei are not necessarily evenly distributed during cell division, individual ciliates can vary significantly in their functional genetic makeup even if they descend asexually from the same ancestral cell.


Trichodina, another member of the Oligohymenophora, and a parasite of fish. Image from here.

There is an intriguing paradox at work as a result of all this. Because of their unique disconnect between the products of reproduction and the functional template, one can't help wondering if ciliates are, to some extent, able to dodge the consequences of natural selection. Does the ruthless excision of non-functional sequences prior to transcription mean that the ciliate genome may accumulate more such sequences than it could normally? The uneven assortment of chromosomes during amitosis means that not every macronucleus will necessarily contain all alleles present in the micronucleus. Does this mean that deleterious mutations can persist in the micronucleus even if they would impair function in the macronucleus? Zufall et al. (2006) demonstrated that ciliates showed significantly higher rates of genetic evolution than other eukaryotes, and suggested that such potential persistance of deleterious alleles increased the chance of compensatory mutations appearing in the genome before selection took its toll. As Zufall et al. put it, ciliates were therefore free to "explore protein space" to a higher degree than was possible for other eukaryote groups.

REFERENCES

Lynn, D. H. 2003. Morphology or molecules: How do we identify the major lineages of ciliates (phylum Ciliophora)? European Journal of Protistology 39 (4): 356-364.

McGrath, C. L., R. A. Zufall & L. A. Katz. 2006. Ciliate genome evolution. In Genomics and Evolution of Microbial Eukaryotes (L. A. Katz & D. Bhattacharya, eds.) pp. 64-77. Oxford University Press.

Zufall, R. A., C. L. McGrath, S. V. Muse & L. A. Katz. 2006. Genome architecture drives protein evolution in ciliates. Molecular Biology and Evolution 23 (9): 1681-1687.

Let's Have Less of Les

Tom Holtz of the University of Maryland has confirmed via the Dinosaur Mailing List that the fossil animal introduced in the last post as Les is a snafu. The authors of Les intended for their manuscript to be submitted online to Nature, and its arrival on Nature Precedings was a mistake. There is every possibility that the name given to Les in the manuscript will change before publication (pity, I rather liked the name they'd given), and the reviewers may actually recommend that the authors do just that. It is not uncommon practice for reviewers to recommend that authors not use names that are leaked to the public in some way before publication - I suppose to distance the finished product from the rumour mill, though personally I think it probably confuses things even more.

Still, the very fact that such slips can happen so easily just reinforces everything I said in the last post about the need to discuss how the internet affects our concepts of publication, and whether or not we need to adjust our concepts of how to determine priority accordingly.