The Font of the Placentals

The large-scale incorporation of molecular data into phylogenetics over the last few decades has caused a revolution in our understanding of life's evolution. Taxa whose interrelationships were previously regarded as intractable have been opened up to study, and many of our previous views on relationships have been forced to shift. Because conflict always makes for a good story, certain cases of the latter have become causes celebres, receiving extensive attention in both the technical and popular literature. One of these subjects of particular interest, not surprisingly, involves the relationships of the living orders of mammals.

Reconstruction of Arctostylops steini by Brian Regal, from Janis et al. (1998). The arctostylopids are a Palaeocene to Eocene group of mammals of uncertain affinities but probably belonging somewhere in the Boreoeutheria.

A lot of this attention has focused around the revelation of the Afrotheria, a grouping of animals (tenrecs, elephant shrews, hyraxes, aardvarks, elephants and manatees) with likely African origins that was completely unsuspected by studies based on morphological data only but which molecular studies have identified with ever-increasing levels of support. Recent molecular studies of placental phylogeny have agreed on three basal divisions within the placental mammals: the Afrotheria, the Xenarthra (armadillos, anteaters and sloths, a grouping that was recognised even before the advent of molecular data), and the remaining placentals in the largest of the three, the Boreoeutheria.

To the best of my knowledge, the Boreoeutheria is a clade that has also so far been supported by molecular data only with no morphological features yet recognised as defining the group. Nevertheless, its support can be considered as well established. The name Boreoeutheria refers to the clade's likely northern origins in contrast to the more southern distribution of the other two. Within the Boreoeutheria, molecular studies indicate a basal divide between the Euarchontaglires on one side and the Laurasiatheria on the other. The Euarchontaglires include the primates and rodents (as well as a handful of smaller orders). The Laurasiatheria include the Eulipotyphla, a group of insectivorous mammals including shrews, moles and hedgehogs, as sister to a clade containing bats, carnivorans, perissodactyls and artiodactyls.

Molecular phylogeny of mammals, from Springer et al. (2004) (note that not all branches shown in this tree are supported by all studies).

This all has interesting ramifications for the early evolution of placentals. There is an extensive fossil record of mammals from the Palaeocene, the epoch of time immediately following the end of the Cretaceous. However, most of these mammals do not belong to the orders alive today and their exact relationships to living mammals remain open to debate. The molecule-induced shake-up of pacental relationships just increased this uncertainty: for instance, the interpretation of a given group of fossil mammals as close to the common ancestry of perissodactyls and elephants rather goes out the window when perissodactyls and elephants are no longer thought to be closely related. And detailed studies that may resolve these issues remain few and far between. One of the most notable analyses in recent years has been that by Halliday et al. (2017) which covered most of the well-preserved placentals and their close relatives from the Cretaceous and Palaeocene periods. However, it is difficult to say just what to make of their results. The unconstrained analysis of their data presents results that remain deeply inconsistent with the molecular tree. Conversely, constraining the analysis to more closely match the molecular data provides results that are intriguing but difficult to accept at face value; I suspect they may be artefacts of the algorithm forcing taxa into the least unacceptable position for inadequate data. Suggesting that pangolins are the last specialised survivors of a broad clade of condylarths, pantodonts, notoungulates and creodonts is... I suppose not a priori impossible, but definitely a big call. A later analysis based on an expanded version of the same data set by Halliday et al. (2019) irons out some of the kinks but still fails to resolve the base of the Boreoeutheria beyond a massive polytomy of 25 branches (an icosipentatomy?). The Euarchontaglires are recovered as a clade but not the Laurasiatheria or any of its molecular subgroups above the ordinal level. And while some of the newer analysis' placements may seem like an improvement (notoungulates are placed as the sister to litopterns instead of hanging out with pangolins), others may still raise an eyebrow (mesonychids are associated with carnivorans but viverravids and miacids are not).

As always, the best answer to this conundrum is likely to involve more research. While researching this post, I did come across comments from people suggesting issues with the Halliday et al. data. Frankly, for a data set of this size (involving 248 taxa and 748 characters in the 2019 paper), it would be incredible were it otherwise. I know from my own experience that as you add more characters and taxa to a phylogenetic analyses, the challenge of keeping everything in line rises exponentially, and the data sets I've dealt with have been nowhere near the size of this one. Nevertheless, it's a start. And we can but hope that even those who find fault with it ultimately take it as inspiration to themselves do better.

REFERENCES

Halliday, T. J. D., M. dos Reis, A. U. Tamuri, H. Ferguson-Gow, Z. Yang & A. Goswami. 2019. Rapid morphological evolution in placental mammals post-dates the origin of the crown group. Proceedings of the Royal Society of London Series B—Biological Sciences 286: 20182418.

Halliday, T. J. D., P. Upchurch & A. Goswami. 2017. Resolving the relationships of Paleocene placental mammals. Biological Reviews 92 (1): 521–550.

The Shrinking World of Bandicoots

A bandicoot is a very disagreeable animal to clean, therefore it should be done as soon after killing as possible, and then the flesh can be left in strong vinegar and water for a few hours before dressing. Sweet potatoes and onion make a good stuffing for bandicoot, which is good either boiled or baked.--Mrs Lance Rawson, Australian Enquiry Book of Household and General Information.

Golden bandicoots Isoodon auratus barrowensis, copyright Kathie Atkinson.

Back when I used to work on Barrow Island in the north-west of Australia, one of the more noticeable animals to be seen around the place was the golden bandicoot Isoodon auratus. In the evenings, the place seemed to absolutely swarm with them. About the size of a guinea pig, with no tails to speak of (bandicoots are actually born with fairly long tails but tend to lose them in the course of their quite vicious fights with one another; few if any individuals reach maturity with their tails intact), there was no question about their qualifications when it came to cuteness.

Bandicoots are a group of twenty-odd species of marsupial found in Australia and New Guinea (one species, the Seram bandicoot Rhynchomeles prattorum, was described from montane forest on the Indonesian island of Seram to the west of New Guinea). Most are primarily insectivorous, but they also eat varying amounts of small vertebrates and plant matter such as bulbs and fruit. The largest bandicoot, the giant bandicoot Peroryctes broadbenti, has been recorded to reach close to five kilograms in weight. The smallest, the Papuan bandicoot Microperoryctes papuensis, weighs less than 200 grams. I suspect many people in Australia assume that the name 'bandicoot' comes from one of the the Aboriginal languages, but it is in fact Indian (specifically Telugu) in origin. The original bandicoot Bandicota indica is a large rat that is widespread in southern Asia and Australian bandicoots were named for their resemblance to this species. Personally, I have maintained in the past that Australian bandicoots look more like rats than rats do: with their relatively long snouts, bandicoots bear a distinct resemblance to the sort of cartoon figure that comes to most people's minds when they hear the word 'rat'.

New Guinea spiny bandicoot Echymipera kalubu, copyright Michael Pennay.

Bandicoots are highly distinctive from all other marsupials in appearance. Their hind legs are noticeably longer than their forelegs and more or less specialised for cursorial locomotion (especially so in one example that I'll get to shortly). The fourth and fifth toes of the hind foot are much larger than the other three; the first toe in particular is reduced to a non-functional stub. The second and third toes of the hind foot, as in diprotodontian marsupials such as kangaroos and possums, are externally joined together with the two claws at the end forming a comb that is used in grooming more than in locomotion. The fore feet, in contrast, are mostly functionally three-fingered (with the first and fifth fingers reduced) and adapted for digging with the claws large and flat.

Many bandicoots are rapid reproducers with their gestation periods among the shortest of any mammal, less than two weeks between fertilisation and birth. Bandicoots also have the most developed placentas of any marsupial group (yes, most marsupials do have a placenta, albeit a much simpler one than found in placental mammals); it is presumably because of this that, despite their short gestation, bandicoot young are born at a more advanced stage of development than those of some other marsupials. When the young are born, they initially remain attached to their mother via the umbilical cord; this latter does not become detached and the placenta ejected until after the joey is firmly attached to a teat in the rearward-opening pouch. The young remain in the pouch for about two months and grow rapidly; they may reach full sexual maturity at the age of only three months. As a result, bandicoot populations may increase rapidly if conditions permit.

Greater bilby Macrotis lagotis, copyright Bernard Dupont.

In terms of classification, there is a general consensus that Recent bandicoots can be divided between four groups though there has been some disagreement about exactly these groups are interrelated (and hence exactly how they should be ranked). The most diverse, but probably also the least studied, group of modern bandicoots are the rainforest bandicoots of the Peroryctidae or Peroryctinae. These are about a dozen species found mostly in New Guinea with the aforementioned Rhynchomeles prattorum on Seram and the the long-nosed spiny bandicoot Echymipera rufescens extending its range to the northern tip of Queensland. Most of continental Australia is home to the dry-country bandicoots of the Peramelidae sensu stricto or Peramelinae, of which there are six Recent species (one of these, the northern brown bandicoot Isoodon macrourus, is also found in southern New Guinea). Peramelids tend to have shorter snouts and flatter skulls than peroryctids. The other two groups are both very small and also native to arid regions of Australia. Two Recent species are known of the genus Macrotis, the bilbies, though one of these is extinct and the other is endangered. Bilbies are larger than most other bandicoots, with long ears (hence their alternative vernacular name of 'rabbit-bandicoots') and a long, silky-haired tail.

Gerard Krefft's 1857 illustration of the pig-footed bandicoot Chaeropus ecaudatus, from here.

The final representative of the Recent bandicoots is unquestionably the weirdest of them all. Unfortunately, it is also now extinct, last recorded some time about the middle of the 20th Century, a fact that cannot be called anything less than a fucking tragedy. The pig-footed bandicoot Chaeropus ecaudatus was the most cursorial of all bandicoots. Its forelegs, rather than being adapted for digging as in other bandicoots, had only two functional toes on which the claws were modified into hooves. The hind legs went a step further and had only a single functional toe (raising the question of how this animal groomed itself without the aforementioned claw-comb of other bandicoots Edit: That was a bit of a blonde moment; a second look at the Krefft illustration above shows that the comb is definitely there). The most extensive observations of its habits seem to have been made by Gerard Krefft (1866) who kept a pair alive for about six weeks in 1857 on a trip to the Murray-Darling region before killing them to provide specimens because, you know, 19th-Century naturalist. Krefft recorded that his bandicoots subsisted primarily on plant foods such as lettuce, grass and roots, refusing all meat offered to them (Krefft also refers to providing grasshoppers for them but his account is unclear about whether they were ever eaten). A herbivorous diet was also indicated by the animals' droppings, which where dry and similar to a sheep's. The bandicoots constructed a covered nest from grass and leaves in the tin enclosure in which Krefft kept them in which they sheltered during the day, only becoming active after nightfall. Krefft notes that he acquired "about eight" specimens of pig-footed bandicoot during his six-month camp, admitting that some met a stickier end than others: "They are very good eating, and I am sorry to confess that my appetite more than once over-ruled my love for science; but 24 hours upon "pig-face" (mesembryanthemum) will dampen the ardour of any naturalist". Krefft also noted that several of the specimens found were female, and that despite being provided with eight teats the females never carried more than two joeys. A particularly interesting detail was that the fourth toe of the joeys' fore foot, rather than being reduced as in the adults, remained large so that the feet resembled those of other bandicoots. Presumably this was so that the fore-claws could still be used to allow the newborn joeys to climb from the birth canal to the pouch.

Krefft also noted that the pig-footed bandicoot was already declining in abundance, blaming its increased rarity on competition with introduced grazing livestock. Sadly, changing habitats and introduced predators have caused other bandicoot species to also become endangered since Krefft's time. Please, don't let them go the way of the pig-footed bandicoot.

REFERENCES

Gordon, G., & a. J. Hulbert. 1989. Peramelidae. In: Fauna of Australia vol. 1B. Mammalia. Australian Biological Resources Study: Canberra.

Krefft, G. 1866. On the vertebrated animals of the lower Murray and Darling, their habits, economy, and geographical distribution. Transactions of the Philosophical Society of New South Wales 1862–1865: 1–33.

The Diprotodontids: Marsupials Go Large

Reconstruction of Diprotodon optatum by Anne Musser, from Long et al. (2002). Offhand, running a search for Diprotodon through Google Image brings up some true horrors of digital imagery.

Prior to the arrival of humans, the Australian fauna included many strange, and often dramatic, animals that are sadly no longer with us. Enormous python-like snakes, monitors that would have made a Komodo dragon look underwhelming, drop bears, and of course the notorious demon duck of doom. But among the most iconic of Australia's extinct fauna were the Diprotodontidae, heavyset herbivores that included the largest of all marsupials. Diprotodontids are sometimes referred to in the popular press as giant wombats, but this is a bit misleading: though more closely related to wombats than any other living marsupials, they were a quite distinct group of animals (besides, they shared their world with actual giant wombats that reached the size of a cow). A potentially more appropriate descriptor that has been suggested is 'marsupial rhinos', though at least some diprotodontids were decidedly not like rhinos either.

Skull of Zygomaturus trilobus in Museum Victoria, photographed by Nigel Waring.

The most famous of the diprotodontids was also the first to be described, and indeed the first fossil mammal of any kind described from Australia. Diprotodon optatum, named by Richard Owen in 1838, was the largest of the diprotodontids, sometimes standing more than six feet tall at the shoulder, and reaching estimated weights of around two and a half tonnes. At the time of human arrival, Diprotodon would have been one of the dominant herbivores in the arid central region of Australia. A number of species of Diprotodon have been named over the years, but a review of the genus by Price (2008) recognised only a single species, with the two different size classes present probably representing the different sexes. In the less arid coastal regions, Diprotodon was replaced by various species of the slightly smaller (but still formidably sized) genus Zygomaturus (Long et al. 2002). The best known species in this genus, Z. trilobus, bore a distinctive large bony boss on the snout, giving its skull a profile reminiscent of a cartoon bear. Two other diprotodontid species that would have come into contact with humans are known from the Pleistocene of montane New Guinea, Hulitherium tomasettii and Maokopia ronaldi. Both these species were smaller than the mainland Australians, being about the 100 kg mark. Maokopia has been interpreted as a grazer, while Hulitherium has been seen as a browser, and suggested as a direct analogue of the Asian giant panda (Long et al. 2002).

Reconstruction of Hulitherium tomassettii as a panda analogue, by Peter Schouten.

The broader record of diprotodontids goes back to the Oligocene, with two main lineages being recognised, the Diprotodontinae and Zygomaturinae. Of the species referred to above, all but Diprotodon optatum are zygomaturines. The two groups are primarily distinguished by their dentition, with the premolars being generally more complex in zygomaturines than diprotodontines. In both lineages, the earlier members were smaller: Long et al. (2002) describe a number of genera as 'sheep-sized'. The smallest known diprotodontid, the late Oligocene Raemeotherium yatkolai, they describe as 'lamb-sized'. Black et al. (2012) estimated the weight of the middle Miocene Nimbadon lavarackorum as abut 70 kg. They also suggested that it was an adept climber, in a similar manner to the modern koala, making it the largest known arboreal mammal from Australia. It might seem odd to picture an animal of this size up in a tree, even allowing for the higher density of the canopy in Australia's Miocene rainforests. However, there are larger arboreal mammals alive even today: male orangutans, for instance, may weigh over 100 kg.

Reconstruction of a climbing pair of Nimbadon lavarackorum (adult and juvenile) by Peter Schouten, from Black et al. (2012).

Interestingly, Nimbadon is not placed as a particular basal diprotodontid in the phylogeny of zygomaturines presented by Mackness (2010). As other related marsupial families, such as koalas or thylacoleonids (marsupial lions), also include climbers, it would not be unreasonable to consider such habits plesiomorphic for diprotodontids as a whole. The 'rhino-like' appearance of the later giants would then be something of a novelty, an adaptation to the drier conditions and more open woodlands that arose at the end of the Miocene. If we are to regard the diprotodontids as marsupial rhinos, then we must consider the possibility of rhinos in trees.

REFERENCES

Black, K. H., A. B. Camens, M. Archer & S. J. Hand. 2012. Herds overhead: Nimbadon lavarackorum (Diprotodontidae), heavyweight marsupial herbivores in the Miocene forests of Australia. PLoS ONE 7 (11): e48213. doi:10.1371/journal.pone.0048213.

Long, J., M. Archer, T. Flannery & S. Hand. 2002. Prehistoric Mammals of Australia and New Guinea: One hundred million years of evolution. University of New South Wales Press: Sydney.

Mackness, B. S. 2010. On the identity of Euowenia robusta De Vis, 1891 with a description of a new zygomaturine genus. Alcheringa 34 (4): 455–469.

Price, G. J. 2008. Taxonomy and palaeobiology of the largest-ever marsupial, Diprotodon Owen, 1838 (Diprotodontidae, Marsupialia). Zoological Journal of the Linnean Society 153: 389–417.

Barrallier's Monkey

"Gogy told me that they had brought portions of a monkey (in the native language "colo"), but they had cut it in pieces, and the head, which I should have liked to secure, had disappeared. I could only get two feet through an exchange which Gogy made for two spears and one tomahawk. I sent these two feet to the Governor in a bottle of spirits."

In November 1802, Governor Philip King sent an exploratory expedition west of Sydney under the command of Ensign Francis Barrallier, a French ex-pat who had taken service with the British after fleeing France with his parents following the French revolution. As well as finding a passage across the mountains that barred Sydney from the interior, Barrallier was trying to find the seat of a figure that Governor King later referred to in letters as the 'King of the Mountains'. Who exactly this King of the Mountains was supposed to be is unclear. Many have thought he was supposed to be some sort of overlord of the local Aboriginals. David Levell, in his 2008 book Tour to Hell, argues the King of the Mountains to have been the head of a secret inland settlement that many of the convicts imprisoned in Sydney believed would offer sanctuary to any who escaped there. Barrallier returned to Sydney in late December, having failed to locate either passage or king (the one would be discovered later, the other would prove to be mythical under any interpretation). Barralier's journal of his expedition languished in relative obscurity until an English translation was published in 1897.

The main interest for later readers of Barrallier's account has been in his dealings with the indigenous people he encountered and worked with. Barrallier had an interest in developing a rapport with the local people he met that was not shared by most of his British associates and his notes, sparse as they may be, provide one of the few direct records available of pre-colonial life in the Sydney region. I've brought Barrallier into this post, however, because of an incident he describes briefly in his journal where the game procured by some of Barrallier's aboriginal associates included an animal that Barrallier refers to as a 'monkey'. Barrallier did not see the animal's remains before it had already been butchered, but he is still the first European known to have acquired a specimen of one of Australia's most iconic animals: the koala.

Koalas Phascolarctos cinereus, photographed by Dinkum.

Koalas are widespread in the east of Australia, though loss of habitat has rendered their distribution localised in some areas. To most people outside Australia, the koala seems like a plush toy come to life, the essence of cuteness manifest in a single animal. The Australians themselves often have a more ambivalent attitude: while the koala is certainly a high-ranking member of the pantheon of the Australian fauna, together with such luminaries as the kangaroo, the platypus, the kookaburra and the gumnut baby, Australians also tend to look upon it as indolent, bad-tempered, and steeped in the kind of aroma that only an exclusive diet of eucalyptus leaves can give an animal (many Australians look more affectionately on the koala's closest living cousin, the wombat). To zoologists, Phascolarctos cinereus is the only surviving species of a lineage that goes back at least to the late Oligocene. Three subspecies of koala have been recognised, but these probably represent clinal variations rather than geographically discrete units (Houlden et al. 1999).

At just what point koalas became eucalyptus specialists is something we don't know for sure. The late Oligocene Perikoala palankarinnica possesses an ankylosed lower jaw (i.e. one that has the two sides fused together at the front) that may indicate a diet of tough leaves (Long et al 2002). Eucalyptus would be at least one candidate for such a diet. However, Perikoala's rough contemporary, Madakoala, lacked such a fused jaw and may have taken softer browse. Nor is a fused lower jaw present in the Miocene genera Litokoala or Nimiokoala (Louys et al. 2009). It seems likely that specialisation on Euclayptus may only have developed with the modern genus Phascolarctos, corresponding with the rise of eucalypt dominance in the Australian flora in the late Miocene. As well as being potentially less specialised, the fossil genera of koalas were also distinctly smaller than the living species. Koala evolution reached an apogee of sorts in the Pliocene and Pleistocene with the fossil species Phascolarctos yorkensis, which tipped the scales at nearly twice the size of P. cinereus (Long et al. 2002) (somewhat disappointingly, no-one seems to seen fit to present a fossil koala with the name of Katastaxarctos).


Koalas can be very vocal animals, using bellows and grunts as their main method of communicating. This video of a vocalising bull comes from here.

The specialisation of the modern koala is truly a remarkable thing. True exclusivity of diet seems to be a rarity among large terrestrial vertebrates (and as it can reach sizes of 20 kg, there is no denying that the koala is a large vertebrate). Many have their preferred delicacies but remain far from averse to the occasional variation (something that I really wish the ABC had been more aware of with that lorikeet article). Thus we have cattle gnawing on bones, cats eating grass, or deer killing and eating birds. Even the giant panda, perhaps the other specialist mammal most familiar to the general public, has been known to supplement its bamboo diet with roots and small animals. But the koala turns up its nose at almost anything other than Eucalyptus leaves—and usually only a small number of Eucalyptus species at that. The toughness of Eucalyptus leaves mean they require a great deal of digestive processing, and the small nutritive return is responsible for the extended periods of inactivity that koalas are known for. Early British naturalists often compared the koala to the South American sloth, which functions under similar constraints. The low nutrition of their diet is also reflected in the notoriously small brains of koalas, which have one of the smallest brains relative to body size of any mammal. So noxious is the eucalypt diet that koala joeys have to be weaned onto it through stages. When a joey is about six months old, its mother starts producing a faecal pap of half-digested leaves that the joey eats direct from her cloaca before moving to a more direct leaf diet about a month later.

Nevertheless, by specialising on Eucalyptus leaves, koalas have access to an abundant food source that few other mammals can handle. Even after the arrival of Europeans, koalas have handled the incursion of foreign predators better than many other Australian natives. The main threat to their continued existence is clearing of the forests on which they depend for food. The koala deserves its position as an icon, and an icon is worthy of respect.

Video of a koala joey feeding on pap, from Arkive.

REFERENCES

Houlden, B. A., B. H. Costello, D. Sharkey, E. V. Fowler, A. Melzer, W. Ellis, F. Carrick, P. R. Baverstock & M. S. Elphinstone. 1999. Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817). Molecular Ecology 8 (6): 999–1011.

Long, J., M. Archer, T. Flannery & S. Hand. 2002. Prehistoric Mammals of Australia and New Guinea: One Hundred Million Years of Evolution. University of New South Wales Press: Sydney.

Louys, J., K. Aplin, R. M. D. Beck & M. Archer. 2009. Cranial anatomy of Oligo-Miocene koalas (Diprotodontia: Phascolarctidae): stages in the evolution of an extreme leaf-eating specialization. Journal of Vertebrate Paleontology 29 (4): 981–992.

The Mysterious Name of Queen Lestoros

The shrew-opossum Caenolestes fuliginosus. Photo from here.

Those of you who are familiar with the more encyclopaedically-arranged natural history books will almost certainly have encountered the phenomenon of the Mysterious Name. In the introductory section of the book, where the scope of the text is indicated, there'll be some sort of taxonomic listing - the phyla of animals, for instance, or the families of birds - with each of the taxa listing being described in a subsequent part of the book. But often, if you're the sort that will pore over such a listing closely enough, you'll notice that the listing includes at least one name, one taxon (often more) on which the remainder of the book is silent. It's there in the beginning, it has its place firmly indicated in the hierarchy - and then silence.

One taxon that throughout my youth remained to me a mysterious name was the Caenolestidae. Caenolestids are small South American marsupials, commonly known as shrew-opossums*. In most lists of marsupial families, they'll be near the beginning, after the true opossums of the Didelphidae. But all the books I read as a child would skip straight from Didelphidae to Dasyuridae, with nary a hint of anything in between.

*Another sign of their obscurity in the public eye - that they are only given the names of other animals, rather than being thought deserving of a name of their own.

Admittedly, the caenolestids are not a large family. Gardner (2005) lists just six species in three genera, Caenolestes, Lestoros and Rhyncholestes. Four of those species are in Caenolestes, the other two genera are regarded by Gardner as monotypic (though one effect of their understudied status is that no two authors will entirely agree on the caenolestid species list, and some authors may recognise two species in either or both of the smaller genera, while others will recognise only a single genus with as few as three species). Of course, that's still more species than other mammal families such as Rhinocerotidae or Hominidae that have no trouble claiming page space for themselves, and while caenolestids may be few in number now, they were more abundant in the past. Caenolestids were the most abundant small marsupials in South America during the early Miocene (Marshall, 1980).


Lestoros inca. Photo by Phil Myers.

Living caenolestids are widespread, and probably not particularly uncommon, but specimens are few and far between. This has mainly been blamed on their unobliging choice of habitat - they prefer very dense, humid forest, though they may be concentrated close to open meadows (Nowak, 1999). They are shrew-like in appearance (hence the common name), and females lack a pouch (presumably the young just hang directly onto the teats, but females with emerged young seem to have not yet been observed). The front of the lower jaw contains an elongate, procumbent pair of incisors, on which more in a moment.

The most detailed account of their behaviour comes from Kirsch & Waller (1979), who trapped and observed specimens of four caenolestid species. Though stomach contents indicate that the caenolestid diet is mostly invertebrates (Nowak, 1999), Kirsch and Waller found that specimens were most attracted to traps baited with meat, and when offered a choice between insects and meat, they would more readily take the latter. A male caenolestid offered newborn rats proved an efficient predator:

The animal would move toward a rat, sniffing vigorously, seize and lift the rat with its forepaws or pin it to the substrate, and bite it several times quickly with its incisors. The caenolestid would then commence eating the rat by biting off a section of the head with its cheek teeth and take successive bites posteriorly.

In fact, the large incisors were used rarely by caenolestids in feeding - almost all biting and chewing was done with the cheek teeth, and the incisors are primarily for dispatching prey. Caenolestids have a distinct flap on either side of the upper lip, and this probably protects the face and whiskers from getting clogged up with blood and dirt while the animal is busy stuffing prey towards the back of its mouth. When offered larger food items such as earthworms, the caenolestids would sit upright on their tails and use their front paws to manipulate their food, similar to the way a mouse does.


Skull of Caenolestes condorensis, so you can get a better look at those lower incisors which a such bad news if you're a baby mouse. Image from here.

Fossil caenolestids (or near-caenolestids, depending on your preferred classification) were ecologically more diverse than modern species, and a number appear to have been herbivorous. One such genus, the Miocene Abderites, had a large sharp and multi-grooved first molar like the teeth of the multituberculates. Marshall (1980), in the last major review of the fossil caenolestids, suggested that the arrival of the caviomorph rodents in South America was what triggered the demise of the caenolestid herbivores, while the more generalised insectivores/carnivores were able to keep sailing on.

Phylogenetically, caenolestids have been difficult. Perhaps the most honest representation of our current state of knowledge of marsupial phylogeny would be a trichotomy between the caenolestids, didelphids and australidelphians (Australian marsupials), with all possible relationships between these three having been suggested in the past. Some earlier authors suggested a relationship between caenolestids and the Australian diprotodont marsupials on the basis of the procumbent incisors, but this hypothesis was pretty firmly flattened when it was established that a different pair of incisors was involved in each of the two groups. Perhaps the most popular option at present is that caenolestids are the sister to australidelphians, to the exclusion of didelphids, as supported by some molecular data (Springer et al., 1998). However, a relationship between didelphids and caenolestids remains a distinct possibility due to the occurence in both of sperm pairing. After leaving the testes, sperm of members of these two families connect up to each other, forming a single moving pair (perhaps enabling them to swim faster through the uterus). However, the homology of this character is debatable, as the sperm connect in a different place in the different families.

REFERENCES

Gardner, A. L. 2005. Order Paucituberculata. In D. E. Wilson & D. M. Reeder (eds.) Mammal Species of the World: A taxonomic and geographic reference pp. 19-20. JHU Press.

Kirsch, J. A. W., & P. F. Waller. 1979. Notes on the trapping and behavior of the Caenolestidae (Marsupialia). Journal of Mammalogy 60 (2): 390-395.

Marshall, L. G. 1980. Systematics of the South American marsupial family Caenolestidae. Fieldiana: Geology, new series 5: 1-145.

Nowak, R. M. 1999. Walker's Mammals of the World, 6th ed. JHU Press.

Springer, M. S., M. Westerman, J. R. Kavanagh, A. Burk, M. O. Woodburne, D. J. Kao & C. Krajewski. 1998. The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole. Proceedings of the Royal Society of London Series B - Biological Sciences 265 (1413): 2381-2386.

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.

Life in the Palaeocene - We Don't Need No Placentalia?

The pantodont Coryphodon, as reconstructed by Heinrich Harder. At the time of their existence, pantodonts were the largest herbivorous mammals. According to Wikipedia, Coryphodon reached about a metre in height and a weight of half a tonne, and also had the dubious distinction of having the smallest brain/body weight ratio of any mammal living or extinct.

Sixty-five million years ago last Tuesday, the mighty dinosaurs went extinct. Well, they didn't all go extinct, but that's how it's usually expressed because "the mighty dinosaurs went extinct except for a number of volant clades that actually continued to do pretty well for themselves, really" somehow just doesn't have quite the same ring to it. What remains a fact is that something pretty significant happened to the ecosystem at the end of the Cretaceous, leading to a major turnover that's usually represented as out with the dinosaurs, bring in the mammals. It is true that the mammals showed a significant rise in diversity during the Palaeocene, the time period immediately following the Cretaceous. However, few of the prominent mammalian groups of the time would be recognisable today.

Modern mammals are divided between monotreme, marsupials and placentals. It is the Placentalia (the group we ourselves belong to) that have been the most successful of the three groups overall, a success that has generally been attributed to their reproductive system of nourishing developing foetuses for longer periods and giving birth to more developed young*. When the fossil record is actually taken into account, Placentalia are a subset of a larger group called Eutheria. Eutherians are the total group containing placentals and all fossil mammals more closely related to placentals than marsupials, while placentals are the crown group of the eutherian lineages that have survived to the present.

*Whether this is really the secret of the placentals' success is more debatable than generally let on. For instance, it has been suggested that in highly unpredictable environments such as the arid centre of modern Australia, marsupials, with their lower nutrient commitment to developing offspring, may actually have the edge reproductive system-wise.


Skull of the taeniodont Psittacotherium, from Matthew (1937) via Paleocene Mammals. Late Palaeocene taeniodonts developed massively powerful jaws and cutting teeth. Psittacotherium was one of the most extreme forms, and at a weight of about 50 kg would have been comparable in size to a medium dog.

The eutherian and marsupial lineages had separated from each other by the early Cretaceous, but the question of when the modern placentals arose has been a hotly debated topic. While a number of Cretaceous lineages have been suggested to belong to the Cretaceous crown group - Zhelestidae as relatives of the ungulates (hoofed mammals), while Zalambdalestidae were close to rodents and lagomorphs (Archibald et al., 2001) - recent analyses have placed these taxa outside the placental crown, and the fairly comprehensive analysis by Wible et al. (2007) suggested that none of the fossil eutherians known from the Cretaceous are placentals. This stands in fairly stark contrast to molecular dating studies, which are fairly unanimous in suggesting that the modern placental orders diverged from each other during the Cretaceous. Either the molecular dating is all wrong for some reason, or the placentals were around in the Cretaceous and we just haven't found them yet.

Still, whether it was the ancestors of the placentals or a number of lineages that survived the end of the Cretaceous, the fossil evidence indicates at least four eutherian lineages survived into the Palaeocene. The Cimolestidae and Leptictidae, families present in both the Cretaceous and the Palaeocene, were placed by Wible et al. (2007) outside the placentals, while the Taeniodonta, a eutherian lineage of unknown relationships, was represented in the late Cretaceous by the species Schowalteria clemensi (Fox & Naylor, 2003). Whether the various other lineages known from the Palaeocene diverged from these lines after the end of the Cretaceous or also survived from earlier times is a decidedly open question.

As already indicated, few of the Palaeocene eutherians can be related directly to modern placental orders. Instead, the Palaeocene was the time of a number of lineages that are no longer with use - herbivores such as the pantodonts and dinocerates, small insectivores such as apatemyids and leptictids, carnivores such as creodonts and arctocyonids. Martin Jehle's Paleocene Mammals website has detailed coverage of many such groups. Palaeocene mammals were also quite distinct from modern taxa in the overall range of morphologies - for want of a better way to put it, Palaeocene eutherians tend to look - well - lumpier than modern species. The broad grasslands that currently dominate the terrestrial part of the world were not yet in existence, and the Palaeocene was a time of forests. As a result, the grassland-adapted cursorial morphologies like modern horses and antelope were also absent, and the low-slung waddler was king.


The early dinocerate Prodinoceras xinjiangensis, as reconstructed by Stanton Fink.

So how did these Palaeocene waddlers relate to the modern taxa evolutionarily? The only answer we can really give at this point is, who knows? The relationships between the Palaeocene and the modern eutherian orders remain almost completely unknown, and those few connections that have been accepted in the past have been profoundly shaken. For instance, many of the Palaeocene families have been included in the 'condylarths', a heterogeneous assemblage believed to be related to the modern ungulates. However, it has become well established in recent years that the ungulates represent at least three separate lineages, with the artiodactyls (even-toed hoofed mammals), perissodactyls (horses and rhinoceros) and paenungulates (elephants and hyraxes) all arising from separate ancestors in the placental tree. Which condylarths are related to which modern ungulates? For that matter, are they related to any of them? If the ungulate morphology arose at least three times in lineages that survived to the present, why should we assume that it couldn't have also appeared independently in extinct lineages? Similar issues surround Palaeocene 'insectivoran' families, whose association with possibly polyphyletic modern insectivorans should be regarded as doubtful.

In light of the findings of Wible et al. (2007), we might even doubt whether many of the Palaeocene eutherians even represent placentals. The classification of McKenna and Bell (1997) united many early eutherians such as Cimolestidae, Pantodonta and Taeniodonta (as well as the modern pangolins) into a group called Cimolesta, which was then included in the Ferae with creodonts and Carnivora. While pangolins may indeed be related to carnivorans, Cimolestidae, as referred to above, are not even placentals. What then becomes of the rest of the "Cimolesta"? Are they also stem-eutherians like Cimolestidae, or are they true placentals?

Such questions are not mere curiosities - the answer could have significant effects on our understanding of Palaeocene ecology. At least some stem eutherians such as the Zalambdalestidae possessed epipubes, bones that support the pouch in marsupials but are absent from placentals (Kielan-Jaworowska, 1975). Because of the restrictions epipubes place on the expansion of the abdomen, they may be incompatible with a placental reproductive system. As a result, we cannot assume that stem eutherians bore well-developed young like modern placentals do. Did pantodonts walk around with pouches slung from their bellies?

REFERENCES

Archibald, J. D., A. O. Averianov & E. G. Ekdale. 2001. Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals. Nature 414: 62-65.

Fox, R. C., & B. G. Naylor. 2003. A Late Cretaceous taeniodont (Eutheria, Mammalia) from Alberta, Canada. Neues Jahrbuch für Geologie und Paläontologie – Abhandlungen 229 (3): 393-420.

Kielan-Jaworowska, Z. 1975. Possible occurrence of marsupial bones in Cretaceous eutherian mammals. Nature 255: 698-699.

Wible, J. R., G. W. Rougier, M. J. Novacek & R. J. Asher. 2007. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary. Nature 447: 1003-1006.

A little bit mole-ish in the Miocene

After the last two posts on unicellular organisms, I'm going to bravely leap to another end of phylospace and cover a mammal. Necrolestes patagonensis was a small fossorial animal from the Miocene of Patagonia that has always held a certain appeal for me, both because of its somewhat morbid genus name (it translates as "robber of the dead") and because of its enigmatic phylogenetic position (recent review by Asher et al., 2007).

Necrolestes was described by Florentino Ameghino in 1891. Ameghino seems to have left a few conundrums in his wake - he originally described the giant carnivorous bird Phorusrhacos (sometimes spelt Phororhacos - I'll have to explain that sometime) as a toothless mammal, and mistakenly described the "wingless" penguin Palaeoapterodytes (see here for an explanation). Ameghino seems to have favoured an association of Necrolestes with the African golden moles (Chrysochloridae) - a not unreasonable suggestion for the time. Since then, probably the majority of authors have felt that Necrolestes was a marsupial, but it has also been compared with edentates or suggested as a late survivor of an equally enigmatic group of South American fossil mammals called Gondwanatheria (see here). I recall seeing a nice little cartoon in one paper doubting a marsupial affinity for Necrolestes (I think it was Archer, 1984 but I'm not certain) showing a little Necrolestes being drop-kicked by an anthropomorphised borhyaenid out the door of a gathering of marsupial representatives (borhyaenids were a family of dog-like marsupial carnivores).

After a detailed redescription of the available material (which, among other things, introduced me to the glorious-sounding term schmelzmuster, which refers to the spatial arrangement of different enamel types within a tooth), Asher et al. (2007) attempt to shed some light on the position of Necrolestes by trying to match its characters with previously optimised trees for other mammals. This proves to be quite tricky - Necrolestes has a rather oddball combination of primitive and derived characters, and any suggested position requires a certain amount of convergence. Asher divide the possibilities into three main options - a position outside the Theria (the marsupials + placentals clade), a position close to or within marsupials (metatherians), and a position close to or within placentals (eutherians).

In regards to a position outside Theria, Necrolestes has an atlas (the first cervical vertebra after the skull) with the left and right halves not fused to each other, something unlike any adult therian. It also lacks many of the tooth apomorphies associated with Theria, though this may just be due to the simplified teeth of Necrolestes. However, Necrolestes does have a coiled cochlea, an astragalar neck and lacks a septomaxilla, so Asher et al. conclude it is most likely a therian. As Gondwanatheria is often regarded as non-therian, Asher et al. suggest that Necrolestes is probably not a gondwanatherian, but I feel that the non-therian nature of Gondwanatheria has not really been demonstrated.

In regards to whether Necrolestes is a metatherian or eutherian, Asher et al. don't really come to a firm conclusion. Patterson (1958) claimed that Necrolestes possessed epipubic bones, which are a primitive character retained in marsupials but absent from modern placentals (thought they were present in some stem eutherians). Asher et al., however, found no sign of epipubic bones. It also has a non-inflected mandibular angle, which is generally a eutherian character, but is also found in some derived marsupials. Necrolestes does share a number of characters with metatherians, most of them "absence" characters - lack of a stapedial artery sulcus, lack of a labial mandibular foramen, etc. It agrees with metatherians in having three premolars, but seems to have one too few molars (three instead of four), and shares a ball-shaped distal process on the ulna and transverse canal foramina on the basisphenoid with crown marsupials.

Characters shared with eutherians are a posteriorly small zygomatic process on the squamosal and small incisive foramina, as well as the aforementioned non-inflected mandible and lack of epipubic bones.

Overall, Asher et al. feel that a metatherian affinity for Necrolestes is most likely, which is appealing on biogeographical grounds (most South American insectivores and such at the time being marsupials). However, they admit that a eutherian affinity can't be ruled out, and I would certainly like to see this possibility further investigated. In particular, if Gondwanatheria are related to edentates (another South American group) as some authors have apparently suggested, the idea that Necrolestes is a late survivor of them may yet be reborn.

REFERENCES

Ameghino, F. 1891. Nuevos restos de mamiferos fosiles descubiertos por Carlos Ameghino en el Eoceno inferior de la Patagonia austral. Especies nuevas adiciones y correcciones. Revista Argentina de Historia Natural 1: 289–328.

Archer, M. 1984. Origins and early radiations of marsupials. In Vertebrate Zoogeography and Evolution in Australasia (M. Archer & G. Clayton, eds.) pp. 585–626. Carlisle: Hesperian Press.

Asher, R. J., I. Horovitz, T. Martin & M. R. Sanchez-Villagra. 2007. Neither a rodent nor a platypus: a reexamination of Necrolestes patagonensis Ameghino. American Museum Novitates 3546: 1-40.

Patterson, B. 1958. Affinities of the Patagonian fossil mammal, Necrolestes. Breviora Museum of Comparative Zoology 94: 1–14.