Invasion of the marsupial weasels, dogs, cats and bears... or is it?

By now I hope it's clear, even to novices with no special interest in the extinct wildlife of the Cenozoic, that ancient South America had what we might technically call a Really Awesome Faunal Assemblage. Astrapotheres, sebecosuchians, phorusrhacids, teratorns, gigantic caimans, madtsoiid snakes, sloths, glyptodonts... and this is only half of it, there's so much more. It occurred to me a while back that it would be only fair and proper to cover yet another of South America's extinct Cenozoic groups, and yet again it's a bunch of animals on which comparatively little information is freely available: the borhyaenoids, a long-lived and diverse group of carnivorous marsupials (or are they?). And it's a particularly good time to bring this group to wider attention because, in a series of excellent recent papers, one worker has, almost single-handedly, done the most amazing job of bringing these animals to life...

Borhyaenoids were first recognised during the 1880s when Florentino Ameghino (1854-1911) described a number of Miocene fossils from Patagonia that he grouped together as the Acyonidae Ameghino, 1889. Ameghino thought that these animals descended from opossums and gave rise to canids: as is well known, Ameghino proposed that the similarities present between South American mammals and their Northern Hemisphere counterparts indicated actual evolutionary relationships, rather than convergence (Simpson 1980). Another name that Ameghino coined later on (in 1894) - Borhyaenidae - later came to supersede Acyonidae, and the name we're using for the group here (Borhyaenoidea) is based on that one (Marshall et al. (1978) petitioned the ICZN to suppress Acyonidae, and they also asked that the spelling Borhyaena Ameghino, 1889 be formally recognised over Boryhaena [sic], the name that Ameghino originally used - apparently accidentally - in 1887). Borhyaenoids have also been called sparassodonts (for Sparassodonta Ameghino, 1894), and while this name is used by some recent authors it hasn't been used as much. They've also been called Borhyaeniformes Szalay, 1962 and Borhyaenomorphia Archer, 1984 [image at top, from Argot (2004), shows the diversity of borhyaenoids as represented in skull and neck morphology].

Most borhyaenoids have been characterised as 'dog-like marsupials', and if any common name is used for the group it's this one. As we'll see, at least some borhyaenoids were superficially dog-like, but others certainly weren't, and if you want to find a more zoologically accurate way of describing these animals it might be to think of them as giant predatory opossums [opossum Didelphis shown here, from wikipedia]. It used to be thought that the dog-like marsupials of Australasia, the thylacines, were close kin of borhyaenoids but anatomical and molecular data shows that this is not the case and that thylacines are part of the exclusively Australasian marsupial clade that includes the dasyures. Borhyaenoids have also been considered allied to the stagodontids, a Cretaceous group of mostly North American omnivores or carnivores (some of which had bulbous teeth that look suited for crushing or breaking hard objects), to the deltatheroidans of Cretaceous Asia, and to the pediomyids of Cretaceous North America.

An extensive literature discusses these various proposals, most of it focusing on detailed characters of the braincase and ear region. Muizon et al. (1997) and Muizon (1999) showed that the stagodontid, deltatheroidan and pediomyid proposals were not supported by good character evidence and argued that borhyaenoids should be united with the opossums (didelphids) and their relatives in the clade Didelphimorphia. It's mostly the way in which the back of the skull is put together that unites these groups.

If borhyaenoids are part of Didelphimorphia, then they're part of the marsupial crown-group and can properly be considered part of Marsupialia. If they're not, then they're outside of the crown-group and would be stem-marsupials, or non-marsupialian metatherians. Note that Metatheria is more inclusive, and that Marsupialia is restricted to the crown-group (e.g., Rougier et al. 1998, Asher et al. 2004). In a large and inclusive analysis of metatherians and other mammals, Rougier et al. (1998) found borhyaenoids and other alleged stem-didelphimorphians to be outside of Marsupialia, and Asher et al. (2004) found a similar result for the supposed basal borhyaenoid Mayulestes.

Let's suppose, however, that borhyaenoids are didelphimorphians for a moment. While it might be difficult to imagine that a group of small, superficially rat-like predators are close kin of one of the most spectacular dynasties of big-bodied mammalian macropredators, note that Palaeocene proto-opossums, like Pucadelphys, are really very similar to taxa regarded by some as the most basal of borhyaenoids, like Mayulestes [Pucadelphys shown in adjacent image, from Paleocene Mammals of the World, but original is © MNHN]. The characters that distinguish borhyaenoids from other didelphimorphians are mostly pretty minor little cranial details like absence of prootic canal, the form of the tympanic sinus, and the presence of nasal bones that don't overhang the narial opening, but they are also characterised by specialised shearing teeth (Muizon 1999).

Were borhyaenoids pouched? That's not a dumb question, as pouches have been repeatedly lost within marsupial evolution, and particularly within opossums actually. Articulated borhyaenoid skeletons lack the epipubic bones used in other metatherians to support the pouch, so pouches might have been absent. However, some marsupials (like Thylacinus) that lack ossified epipubic bones have cartilaginous ones, so we can't be that sure.

While people have often made proposals about how certain borhyaenoids lived and hunted, detailed comparative work that analyses the anatomical details of these animals and compares them with those of living carnivorous mammals has generally been lacking. Indeed, harking back to comments I made about the CEE Functional Anatomy meeting, the widely held view that this sort of work is old-fashioned, outdated and redundant ignores the massively under-appreciated fact that, in an absurdly high number of cases, it's never been done at all. Thanks almost entirely to one worker - Christine Argot of the Muséum National d'Histoire Naturelle (Paris) - we now have a very robust, incredibly detailed literature on borhyaenoid functional anatomy. Argot's papers contain so much information that I'm only going to be reviewing but a fraction of the areas she covers. Given that lengthy papers on functional anatomy of any type are pretty rare, it cannot be over-emphasised how important studies like this are. What's also of special interest as goes borhyaenoids is that Argot's work has shown how various taxa, repeatedly depicted in the popular and semi-technical literature, seem to have been quite different from their 'conventional' image.

The most basal reported borhyaenoid is Mayulestes ferox from the Santa Lucía Formation of Tiupampa, Bolivia (Muizon 1994). However, Rougier et al. (1998) didn't find Mayulestes to be part of Borhyaenoidea, and this was followed by Forasiepi et al. (2006). Anyway... Tiupampa has given its name to the Tiupampan Land Mammal Age, a time span dated to the early Palaeocene. A second Tiupampan borhyaenoid, Allqokirus australis, has been regarded as close to Mayulestes and both have been regarded as part of the 'family' Mayulestidae Muizon, 1994, but the fact that Allqokirus is known only from teeth makes this difficult to verify. Mayulestes was weasel-sized and weighed less than 1 kg, and probably less than 500 g. By comparing its pelvis and hindlimb with those of extant marsupials, Argot (2002) showed that this animal had a mobile lumbar region and was agile and well able to climb and move with agility across uneven surfaces. However, the forelimb has features more suggestive of a climbing lifestyle (Argot 2001). It wasn't a cursorial animal, running around in open habitats, nor was it good at leaping, and should probably be imagined as scansorial: as a predominantly terrestrial denizen of cluttered, three-dimensional habitats (like tangled forest floors), but well able to climb [Mayulestes reconstruction from Argot (2004), modified after Muizon. Scale bar = 50 mm].

The Tiupampan fauna includes an assortment of opossums and mioclaenids, and there are also some real oddballs in the fauna, like the pantodont Alcidedorbignya and the opossum-like Szalinia and Jaskhadelphys. It's been hypothesised that Mayulestes preyed on frogs, small marsupials, and the eggs of various crocodilians, turtles and birds (Argot 2004). As the most basal member of Borhyaenoidea, Mayulestes might show us what the ancestral lifestyle and morphology of the group was. However, as we've just seen, there is now doubt as to whether Mayulestes is definitely a borhyaenoid.

The remaining borhyaenoids have been recognised as a clade (which, so far as I know, goes unnamed) united on the basis of braincase details, palatal morphology and an incisor compliment reduced to four uppers and three lowers* (Muizon 1994, 1999). Conventionally, these 'higher borhyaenoids' have been grouped into five 'families': Hathlyacynidae, Prothylacynidae, Proborhyaenidae, Borhyaenidae and Thylacosmilidae. These have also been regarded as 'subfamilies' in those classification schemes where the group here termed Borhyaenoidea has been regarded as a 'family'. Of these groups, hathlyacynids (which differ from other borhyaenoids in possessing a pneumatised squamosal) appear to form the sister-taxon to a clade that includes the remaining taxa (Muizon 1994, 1999).

* The primitive condition for marsupials is five upper incisors and four lowers.

More soon: long-snouted marsupial martens and climbing thylacine-hyaena-binturong hybrids. Regular readers will have noted from the dearth of long articles last week that I was very busy. Shame, given that I missed out on the new Ventastega and bird phylogeny papers. I do what I can, but sometimes there really isn't enough time.

Refs - -

Argot, C. 2001. Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. Journal of Morphology 247, 51-79.

- . 2002. Functional-adaptive analysis of the hindlimb anatomy of extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. Journal of Morphology 253, 76-108.

- . 2004. Evolution of South American mammalian predators (Borhyaenoidea): anatomical and palaeobiological implications. Zoological Journal of the Linnean Society 140, 487-521.

Asher, R. J., Horovitz, I. & Sánchez-Villagra, M. R. 2004. First combined cladistic analysis of marsupial mammal interrelationships. Molecular Phylogenetics and Evolution 33, 240-250.

Forasiepi, A. M., Sánchez-Villagra, M. R., Goin, F. J., Takai, M., Shigehara, N. & Kay, R. F. 2006. A new species of Hathliacynidae (Metatheria, Sparassodonta) from the middle Miocene of Quebrada Honda, Bolivia. Journal of Vertebrate Paleontology 26, 670-684.

Marshall, L. G., Clemens, A., Hoffstetter, R. J., Pascual, R., Patterson, B., Tedford, R. H. & Turnbull, W. D. 1978. Acyonidae Ameghino, 1889 (Mammalia): supplement to proposal to suppress this name. Bulletin of Zoological Nomenclature 35, 12-14.

Muizon, C. 1994. A new carnivorous marsupial from the Palaeocene of Bolivia and the problem of marsupial monophyly. Nature 370, 208-211.

- . 1999. Marsupial skulls from the Deseadan (late Oligocene) of Bolivia and phylogenetic analysis of the Borhyaenoidea (Marsupialia, Mammalia). Geobios 32, 483-509.

- ., Cifelli, R. L. & Paz, R. C. 1997. The origin of the dog-like borhyaenoid marsupials of South America. Nature 389, 486-489.

Rougier, G. W., Wible, J. R. & Novacek, M. J. 1998. Implications of Deltatheridium specimens for early marsupial history. Nature 396, 459-463.

Simpson, G.G. 1980. Splendid Isolation: the Curious History of South American Mammals. Yale University Press, New Haven and London.