Among the most intriguing of recently described fossil mammals has to be the Minorcan giant rabbit Nuralagus rex, published recently in Journal of Vertebrate Paleontology (Quintana et al. 2011). It’s a very neat discovery, whether you’re interested in lagomorph diversity or not. As usual, the one thing that everyone has been interested in is the size of this animal: how big was Nuralagus? With an estimated mass of about 12 kg, it was about ten times bigger than an average modern bunny (the examplar is of course the [ancestrally] Euro-African Oryctolagus cuniculus) and about twice as big as both the largest domestic rabbit (the Flemish) and the largest modern lagomorph of them all (the European hare Lepus europaeus). [Image below - by Sa monea, from wikipedia - shows a Nuralagus femur compared to that of Oryctolagus.]

Nuralagus is also morphologically peculiar compared to many other rabbits and hares. Relatively small eyes and small auditory bullae suggest that its senses weren’t as acute as those of continental lagomorphs, and its spreading digits, the nature of its limb bone articulations, and the low degree of flexibility in its spine all indicate that it was a relatively slow-moving walker, not a jumper or sprinter (Quintana et al. 2011).

However, you may well have heard all of this before, and it’s not why I’m here. I see two other things relevant to Nuralagus that are worth commenting on.

Firstly, fossil lagomorph diversity is reviewed all too infrequently in my opinion, so here are a few comments. According to Quintana et al. (2011), the closest relative of Nuralagus seems to be Alilepus, a widespread fossil rabbit, the different species of which are known from the Miocene, Pliocene and Pleistocene of Europe, Asia and North America. Both taxa share various detailed tooth characters, and it seems that Nuralagus is more similar in some respects to Eurasian Alilepus species than to North American ones (does this mean that Alilepus might be paraphyletic with respect to Nuralagus?).

For the record, note that all rabbits and hares are united within the group Leporidae. Leporids are the sister-group to Ochotonidae, the pikas (pikas had their heyday in the Miocene, it seems, when they far outnumbered leporids in number of species). A small number of fossil taxa from the Paleocene and Eocene (eurymylids, Gomphos and the mimotonids) appear to be stem-lagomorphs, and all of these taxa just mentioned have been united in the clade Duplicidentata (Wyss & Meng 1996, Asher et al. 2005).

So – we know that Nuralagus is close to Alilepus…. but what sort of leporid is Alilepus? Quintana et al. (2011) don’t include a phylogenetic analysis in their article, but a few preceding studies allow us to get a rough handle on leporid phylogeny.

In pursuit of a cladogram for fossil rabbits

McKenna (1982) published a hand-cranked phylogeny for lagomorphs [shown below: click to enlarge]. Pentalagus (the very special Ryukyu rabbit), Oryctolagus and Lepus formed a crown-group while Hypolagus (a widespread, long-lived taxon with species from the Miocene, Pliocene and Pleistocene of North America and Eurasia) and Archaeolagus (from the Oligocene and Miocene of North America) were arranged in successively more distant locations along the leporid stem. Chadrolagus, Palaeolagus and Litolagus were placed in a polytomy with this Hypolagus + crown-leporid clade (note that Palaeolagus was recovered as a stem-lagomorph by Asher et al. (2005) and hence removed from Leporidae entirely: P. haydeni - the type species (from the Lower Oligocene of Nebraska) - is shown in the adjacent image).

Dawson (2008) also provided a hand-cranked phylogeny; this time with more taxa included, and with names used for various of the clades and (dare I say it) grades. Dawson certainly wasn’t the first to use these names: in a rabbit classification published in 1929, Lee R. Dice proposed a subdivision of Leporidae into three ‘subfamilies’, and other authors introduced more such subdivisions later on. Anyway, the ‘base’ of Dawson’s tree was occupied by Procaprolagus, the various species of which are from both the Eocene and Oligocene of Asia and North America. A diversity of Eocene, Oligocene and Miocene taxa were then grouped into the paraphyletic ‘Palaeolaginae’, while the two clades Archaeolaginae and Leporinae were shown as sharing an ancestor with a ‘palaeolagine’ clade that included Mytonolagus and Palaeolagus (Dawson 2008). Tooth characters show that Alilepus is a leporine but, beyond that, Dawson didn’t elucidate: Pronotolagus from the Miocene of North America was identified as the most basal leporine, but the affinities within Leporinae weren’t the focus of her interest.

Again, let’s note that both the McKenna and Dawson trees are what we call hand-cranked: this means (it’s a very much informal term) that these workers constructed their trees ‘by hand’, following their assessment of a relatively small number of characters. History has shown us that hand-cranked trees are (generally) approximately right, but because (normal) humans aren’t able to assess the hundreds or even thousands of data points that need to be compared simultaneously whenever organisms are examined in detail, you need computers that run parsimony algorithms to best assess the data you collect. You know all this already: it’s phylogenetics 101.

But one thing that becomes quickly obvious when you try to look at fossil rabbit phylogeny is that hardly any work has been done, which is a bit surprising given the number of specimens that are known and the quality of their preservation. Wible (2007) published a parsimony-based cladogram of leporids [it's shown here]: Pronolagus and Romerolagus were shown as being outside the clade that includes hares, cottontails and so on, but no fossil leporid taxa were included. A few other phylogenetic studies have incorporated data from fossil leporids (Meng & Wyss 2001, Asher et al. 2005, Kraatz et al. 2010), but they also don’t include enough taxa to flesh out the tree at all. So, as yet, there’s no real idea as to how such taxa as Alilepus and Nuralagus relate to other rabbits. For now, the adventure ends here. As I said above, the lack of work on lagomorph phylogeny is surprising given the quality of much of the fossil material and the number of specimens involved, and also given that lagomorphs are just so freakin’ weird compared to other placental mammals. Seriously, they’re insane. If any newbies want elaboration on that, I’ll be happy to oblige.

Incidentally, most of the phylogenetic hypotheses that have been published for leporids rely heavily on data that comes from tooth cusp anatomy. Rabbit teeth are very weird and experts have argued for years over how their tooth cusps should be homologised with those of other mammals – I’d love to discuss this matter in more detail but now is not the time. As it happens, Kraatz et al. (2010) have recently published an open-access paper on this very issue, so you can check it out for yourselves [adjacent image, showing postulated transformation in lagomorph tooth cusp anatomy, from Kraatz's website].

And thanks much to Brian Kraatz for his help and sage advice on leporid phylogeny, by the way. He has big plans for fossil rabbits – hopefully they’ll pan out.

The neck, the neck, oh, the neck

The second thing I wanted to say about Nuralagus is a little more arcane than its phylogenetic position, and there might not be that many people who have the required overlapping fields of interest to even think it worthy of note, but here I go.

Quintana et al. (2011) include a very nice reconstruction of Nuralagus in their paper on the animal: you might already have seen it online. It’s really very good: it shows the animal to scale with a European rabbit, and portrays it in nice, realistic fashion. But... they almost certainly have the neck horribly wrong.

They show the neck skeleton of Nuralagus held just about straight, in a strange, sub-horizontal pose, and with no curve in it whatsoever. I presume they did this because they imagine that’s how extant rabbits hold their necks. In fact – as you’ll know if you followed the neck posture stuff I published with Mike P. Taylor and Mathew Wedel (Taylor et al. 2009) [link to pdf below] – it definitely ain’t so. Like rodents and other ‘short necked’ mammals, rabbits actually have a strongly curved neck skeleton that descends sharply close to the cervico-thoracic transition before ascending to meet the occiput. None of this is at all obvious in the living animal and is only revealed in x-ray (or when other imaging techniques are applied). It’s crazy, but it’s really there: rabbits have a virtually S-shaped neck skeleton: check out the x-rays of a live rabbit below, from Vidal et al. (1986).

Regardless of whatever preconceptions you might have, we really should assume by default that the neck of this weird, giant, island-endemic rabbit was also S-shaped, with a strong curvature just like seen in extant rabbit species. And it’s no use saying that the fossil bones won’t allow this sort of posture, since one of the things that’s obvious from x-rays of living animals is that the postures their necks maintain during life aren’t readily reproducible from dry bones either. The soft tissues present in the living animal make the neck skeleton more flexible that is the case in the dry skeleton, not less.

So, there we have it. My initial plan here was just to make a quick observation on Nuralagus and tie it into work I and colleagues have done on neck posture, but it seems there’s an awful lot to say about fossil lagomorphs. As usual, I’ve barely touched on the many neat things you could say about these animals: I think we’ll definitely be coming back to them in time.

Refs - -

Asher, R. J., Meng, J., Wible, R. R., McKenna, M. C., Rougier, G. W., Dashzeveg, D. & Novacek, M. J. 2005. Stem Lagomorpha and the antiquity of Glires. Science 307, 1091-1094.

Dawson, M. R. 2008. Lagomorpha. In Janis, C. M., Gunnell, G. F. & Uhen, M. D. (eds) Evolution of Tertiary Mammals of North America. Volume 2: Small Mammals, Xenarthrans, and Marine Mammals. Cambridge University Press, 293-310.

Kraatz, B. P., Meng, J., Weksler, M. & Li, C. 2010. Evolutionary patterns in the dentition of Duplicidentata (Mammalia) and a novel trend in the molarization of premolars. PLoS ONE 5(9): e12838. doi:10.1371/journal.pone.0012838

McKenna, M. C. 1982. Lagomorph interrelationships. Geobios, mémoire spécial 6, 213-223.

Quintana, J., Köhler, M. & Moyà-Solà, S. 2011. Nuralagus rex, gen. et sp. nov., an endemic insular giant rabbit from the Neogene of Minorca (Balearic Islands, Spain). Journal of Vertebrate Paleontology 31, 231-240.

Taylor, M. P., Wedel, M. J. & Naish, D. 2009. Head and neck posture in sauropod dinosaurs inferred from extant animals. Acta Palaeontologica Polonica 54, 213-220.

Vidal, P. P., Graf, W. & Berthoz, A. 1986. The orientation of the cervical vertebral column in unrestrained awake animals. Experimental Brain Research 61, 549-559.

Wible, J. R. 2007. On the cranial osteology of the Lagomorpha. Bulletin of Carnegie Museum of Natural History 39, 213-234.

Wyss, A. R. & Meng, J. 1996. Application of phylogenetic taxonomy to poorly resolved crown clades: a stem-modified node-based definition of Rodentia. Systematic Biology 45, 559-568.