The mystery of marsupials
Since I was introduced to marsupials by mAtA-shrI when I was a year or so old I was mystified by them because I never got to see them. After all, most of the forms in the book were from faraway and Down under. I spent a while reading about their morphology in the 9th year of my life from the texts books of Colbert and Young. But they remained alien and confusing. The Australian forms were fascinating because they mirrored the placental morphospace occupancy elsewhere in the world – my first lesson in convergent evolution. But their prehistory lay elsewhere and this was what allured me in those long past days and urged me to look deeper into these mammals. But there was no way of doing that while I was in bhArata. During my last year in bhAratavarSha, R was visiting from abroad, and gave me a fascinating account of her great journey down under and her study of marsupial anatomy. I was green with envy and wondered if my chance might ever come. In my second year in mlechCha desha, I was walking home from work one blustery autumn night when I had my first encounter with the opossum, Didelphis on a shrub. This gave me the signal to study the history of marsupials deeper. I spent some time examining the dental anatomy of Herpetotherium – this gave me a clear idea of the distinctiveness of the metatherian teeth in their primitive state.
The upper molar as shown here has a paracone and metacone placed right in the middle of the tooth with the protocone placed well apart below and the prominent stylar shelf with several cusps. These distinctive features immediately help one to spot the metatherian nature of basal forms like Kokopellia and the primitive Asiatherium.
The lower molar as shown here (divided into two elements the trigonid and the talonid) have a paraconid on lingual side in the trigonid and most characteristically a “twinning” of the entoconid and hypconulid cusps on the side opposite to the hypoconid.
Until recently the affinities and the biogeographical patterns of marsupials remained pretty poorly understood. The 1990s and 2000s saw major developments that appear to clarify many previously confounding issues. For example, the great Australian radiation of diprotodonts (including he most recognizable kangaroo, koala and the wombat) shared with the South American caenolestids (paucituberculata; the Andean shrew opossums) the diprotodont condition, where the first pair of incisors are greatly expanded to form a shovel-like surface for food-processing. Some thought that the diprotodont condition was a synapomorphy uniting these groups. However, within the Australian forms, the diprotodonts shared with marsupial bandicoots (peramelemorphia) the condition of syndactyly – the bundling of the skeleton of the 2nd and 3rd foot digits into a single connective tissue sheath, which is absent in any American form. Further, the great mammal anatomist Szalay showed a striking similarity in the articular surface in the calcaneum of the ankle – the “continuous lower ankle joint pattern” – between the Australian forms and a single South American form, the mysterious mouse-like Dromiciops. These conflicting links resulted in multiple phylogenetic models and biogeographic schemes, though most workers eventually accepted the monophyly of all Australian forms and Dromiciops to form the clade australodelphia. The first support for this came from the primitive molecular phylogeny using serological techniques. However, a recent comprehensive molecular and combined molecular and morphological studied by Meredith et al and Beck et al appears to provided several interesting clues regarding the emergence and affinities of extant marsupials. The tree emerging from the efforts of these workers is shown below.
Based on the tree it is amply clear that the extant American forms are paraphyletic with respect to the australodelphian radiation. The simplest explanation from this tree would be that the Australian forms were derived from a single introduction of a basal Dromiciops-like form to Australia from South America via the Antarctica. There are potential barriers to migration from South American to Australia via Antarctica in the Cenozoic: 1) The Trans-Antarctic mountain range was in place and 2) Between 64-52 Mya the connection between Australia and East Antarctica was getting increasingly tenuous with the Southern Ocean opening up. All indications from molecular clocks are that the marsupial radiation of Australia was a post-Mesozoic one, probably beginning earliest in the Early Eocene (~54.5 Mya). Hence, the introduction of the Australian forms occurred earlier than that, probably in the middle-late Paleocene (59-55 Mya). Given the above barriers to migration in this age, the tree is consistent with a single rare invasion of a South American founder form to Australia.
Now does this match the fossil record? Well perhaps it is in the eye of the beholder :-). We have a great radiation of South American marsupials already in place between the KT-boundary to around 58.7 Mya in Bolivian and Brazilian Paleocene deposits – more than 15 different taxa are recognized from these sites. There is no evidence that any of these early Cenozoic marsupials have any Australian counterparts. This is consistent the above phylogenetic picture of the original Cenozoic marsupial radiation occurring in South America, which was mostly independent of the Australian radiation. While many of these Paleocene S. American forms resemble generalized opossums and shrew opossums they are too fragmentary to be certain of a specific affinity of didelphomorphia or paucituberculata. In terms of the Dromiciops-like forms the situation is extremely tentative: Two Paleocene forms from these deposits, namely Khasia and Mirandatherium, are considered early representatives of the microbiotherian radiation to which Dromiciops belongs. However, they are too fragmentary to be certain of their affinities. Likewise there are supposed microbiotheres from Antarctica which are from around ~44 Mya, but these too are too fragmentary to be certain. The first confirmed Dromiciops-like form is Microbiotherium from around 16.5 Mya. Thus, objectively speaking, there is indeed a huge lacuna in the fossil record of the australodelphians of South America, even thought there is reasonable evidence for a major early radiation of marsupials there. The first bona fide australodelphian from Australia is Djarthia from the famous Tingamarra formation from 54-55 Mya. The recent report of the ankle bones of Djarthia confirm beyond doubt its primitive australodelphian nature, and make it the oldest confirmed member of this clade. But it is already in Australia and in the company of some really enigmatic mammals like Tingamarra and Thylacotinga, and a primitive fragmentary bat. There have been doubts about Tingamarra being even a marsupial. Based on these results Godthelp and Beck have tried to claim that the australodelpians actually emerged in Australia and were back-transferred to South America. While not implausible, we find this an utterly unnecessary proposal, especially given their reliance on absence of evidence (dangerous given the fragmentary nature of the small mammalian fossils!). It is possible that the mysterious forms accompanying Djarthia were other mammalian (marsupial) immigrants via Antarctica that flourished only briefly before going extinct. Thus, Australia was entirely left open for the great radiation of australodelphians from a Djarthia-like lineage. From elephantine diprotodonts, to extraordinary carnivores emerging from within the herbivorous diprotodontia such as the marsupial lion Thylacoleo and the carnivorous kangaroo Ekaltadeta the australodelphians diversified to occupy every possible terrestrial niche.
But the major part of the marsupial story is the part that unfolded outside of Australia beginning in the Mesozoic. Till the end of the Mesozoic there are no genuine South American, Antarctic or Australian marsupials. Relatively recent exciting fossil evidence has shown that the most primitive stem marsupial appears in Asia in the famous Chinese Yixian formation along side one of the most primitive stem placentals Eomaia. This primitive 125 Mya form is in many ways rather like the Didelphis opossum of today – a small tree-climbing form. From such a precursor an initial seeding of North America appears to have occurred. In the North American Cretaceous a major stem marsupial radiation appears to have taken place; they appear to have been the dominant mammalian fauna in this period largely exceeding the placentals in number of taxa. These included opossum-like forms such Alphadon, the pediomyids, the larger carnivorous forms like deltatheroidans (Atokatherium) and stagodontids like Didelphodon, and mysterious herbivores like Galsbius. In the latest phase of the Cretaceous before the K/T extinction they appear to have crossed over from North America to Europe as a low diversity lineage. In Asia, on the contrary they appear to have been largely dominated in numbers by the placentals, and mainly lingered on as low diversity primitive clades like Sulestes, Marsasia and Asiatherium. One stem marsupial radiation, the carnivorous deltatheroidans, also appears to have been fairly prevalent in the late Cretaceous of Asia. The reason for this complementary distribution of marsupials and placentals is largely mysterious. Then K/T extinction appears to have battered the stem marsupials severely – they were nearly wiped out in North America, the deltatheroidans and other sporadic Asiatic lineages also appear to have largely vanished. Thus the end of the age of the dinosaurs was in a sense the end of the age of the first great marsupial radiation.
Nearly immediately after the extinction event the new radiation began in South America, where till then no marsupials were apparently present.The very first marsupials from S. Am. are from the Peruvian Laguna Umayo deposits just a little after the K/T boundary and are extremely fragmentary. Though people have temptingly tried to connect the dental remains in these deposits with the latest North American Cretaceous forms like Peradectes and Pediomys we cannot be sure of their phylogenetic affinities. But in the least they suggest that marsupials probably reached S. Am. just before the K/T extinction and probably exploded immediately after it, perhaps due to the ecological opening created by the extinction. In the next 5 million years a great diversity of marsupials emerge in these regions; many of them appear to resemble the modern didelphids, but given that the opossums retain so much of the primitive marsupial condition it is hard to be certain if these forms are specifically sister-groups to the modern didelphids. Some of these forms like Szalinia are really primitive in dental morphology, whereas others like Andinodelphys and Pucadelphys resemble the modern forms more closely in dental features, but have other cranial features that are more primitive than any modern opossum. Thus, Szalinia may be close the ancestral founder of the S. Am. radiation, whereas the forms like Andinodelphys and Pucadelphys are the stem members of a great radiation of South American carnivorous marsupials, the Borhyaenoids (sparassodontia) as suggested by the great French anatomist Muizon. In my own opinion genuine didelphids appear only later and a Miocene Argentine form, Sparassocynus, with an extraordinary ear structure is actually much closer to the modern didelphid opossums. It appears to represent an interesting branch of the otherwise generalist didelphid lineage that was the second hyper-carnivorous marsupial lineage in S. Am. The first hyper-carnivorous lineage was that of the borhyaenoids, which was extremely successful. It began in the Paleocene in the form of the tree-climbing carnivore Mayulestes from Bolivia and the related Allqokirus. Towards the middle-late Paleocene more advanced forms like Patene emerge in Brazilian deposits. From the Eocene the borhyaenoids started growing enormously in size in the form of the proborhyaenid radiation – large bear-like forms such as Callistoe, Arminiheringia and Proborhyaena which was larger than a grizzly bear are seen. By the Miocene they reached their highpoint occupying a range of carnivore niches: otter-like Cladosictis, a marten-like Prothylacinus, a peculiar long-snouted ambush predator Lycopsis, mongoose-like hathlyacynids, leopard-like Borhyaena, saber-toothed Thylacosmilus resembling the saber-toothed cats and the probably bear-like Pharsophorus. By the Pliocene the Borhyaenoids decline precipitously and became extinct for unknown reasons.
In addition to these carnivores, the S. American marsupials also radiated into other niches and also widely populated western Antarctica before it was frozen over by the circum-polar currents. These included the sister groups of the extant shrew opossums, like Epidolops and the later Abderites which evolved unusual shearing dentition to deal with a range of hard plant-derived foods. Another radiation of this clade spawned the rodent- and lagomorph- like Argyrolagus, which probably also hopped on its long hindlegs and Groeberia and Klohnia with enormous incisors. After occupying South America for almost 60 Mya the marsupials largely collapsed around the end of the Pliocene and only a few small, mainly generalized (excluding the specialized aquatic opossums of S. Am.) lineages remain alive. The reasons for this, at least to me, are not clear. Through the Cenozoic marsupials also appear in North America, Europe, Africa and Asia in low densities but eventually became extinct. These forms resemble the generalist opossums but are only known from fragmentary remains and we know little of most of them. Their origins are also bit murky. The North American early Cenozoic forms are the typified by the well-known Herpetotherium that appears to be a primitive generalized opossum-like form. They appear to be survivors of the K/T extinction that later became extinct rather than being related to modern North American opossums which were later immigrants from South America. The African forms from the Oligocene of Egypt are clearly close to those from Europe and both have been placed in the same genus, Peratherium. In the latest Cretaceous of we have Herpetotherium-like forms reaching Europe from N. Am. It is possible that these European and African forms are descendents of those survivors of the K/T event. In contrast the Asian forms like Sinoperadectes are apparently not very close to these Euro-African forms. So they might be survivors of a Cretaceous fauna of Asian marsupials also related to North American forms like Peradectes. Of course most of these forms being too fragmentary are a mystery to most of us.