People tend to think of deer as pretty uninteresting since we’re often used to seeing them traipsing around at the edges of agricultural fields or backyards. Yet even the common deer of our daily experience – in my neck of the woods, it’s Odocoileus virginiacus – are extremely strange in their own right. After all, how many animals out there grow gigantic, naked bones out of their head, only to have them fall off after a few months, at which point the animal can chew on them to get a head start on the next pair? Deer also spend a lot of time walking around on their hindlimbs, precariously balanced on those tiny rear hooves. They’re almost endlessly strange, but the general rules of evolutionary history still apply to them, because early-diverging deer are even stranger.
Muntjacs, genus Muntiacus are small, omnivorous, generally solitary deer with greatly enlarged canine tusks or fangs. They’re commonly known as “barking deer” due to their dog-like alarm vocalizations, and have racked up a plethora of local names across their distribution in Southeast Asia. While usually kept hidden under the upper lip during day-to-day activity, the muntjac’s ~2 cm long fangs are very obvious when you take a look at the skull of the animal, and in combination with the robust antler pedicel and small antlers of males, they make for quite a formidable-looking cranium. But apart from the cranium, muntjacs harbor a suite of other oddities from the cytological to the behavioral, but since I have to start somewhere, we’ll begin anteriorly.
Unlike Odocoileus and many other more recent deer genera, Muntiacus retains the large canines thought to be ancestral to Cervidae as a whole. Musk deer (Moschidae, consisting solely of Moschus) are considered to be sister to Cervidae, and have even larger canines. Going further down the tree, Tragulidae (mouse deer) have small but also well-developed canines, which probably means that these tusks are in fact synapomorphic for ruminants as a whole. Other non-muntjac deer have retained (probably not re-evolved) tusk-like canines as well; other than the tufted deer Elaphodus cephalophus, which together with Muntiacus makes up the Muntiacini, Chinese water deer Hydropotes also sport much larger (~6 cm) fangs. However, very clear molecular and morphological signals put Munticacini and Hydropotes on separate branches of the deer tree entirely, with Hydropotes belonging to the Capreolinae, a group which apparently diversified in Asia, though is now best represented in Europe and the Americas (Gilbert et al 2006).
This means that overall, seeing large fangs on small deer isn’t really as strange as one might think. And in order to accommodate these fangs, both Muntiacus and Hydropotes – and probably Moschus – are capable of moving the teeth around within their sockets via their lip muscles (Aitchison 1946). In Muntiacus the motion is primarily posterior and distal, in order to accommodate chewing, but Hydropotes can actually pull their canines forward slightly by way of their lip musculature. So yes, there are mammals with huge (when compared to body size) mobile fangs, but stunningly, those animals are small and not primarily carnivorous, and their mobile fangs have almost nothing at all in common with mobile fangs in Viperids.
The differences in tusk size and mobility are implicated in larger questions about the evolution of Cervidae as a whole, and the selective regime of cranial ornamentation. Given that the evolutionary trend in deer has been a reduction of the tusks and increase in antler size and complexity, it’s assumed that antlers have slowly assumed the role that tusks once played; namely, that of male competition. In deer with tusks but no antlers, male-male combat is quite dangerous, and involves repeatedly attempting to strike the opponent with tusks in order to inflict a wound severe enough that the opponent retreats (Aitchison 1946, Barrette 1976). In muntjacs, males participate in both sparring – nonagressive competition using the antlers exclusively – and fighting, whereby the males use their antlers in an attempt to throw their opponent off balance in order to score a blow with their tusks. Sparring is by far the predominant form of competition between males in Muntiacus, with very little fighting observed (Barrette 1976). Barrette’s explanation for the evolution of antlers centers around he fact that antler-only combat is far less dangerous than combat with tusks; antlers first evolved as a guard against tusks, a way to block blows.
This is a pretty satisfying explanation for the purpose of antlers overall, as it explains a lot of their extremely weird features. First, the antlers of the muntjac point backwards, as do its long antler pedicles, and this position is ideal for blocking tusk blows delivered to the neck and shoulder region, where males attempt to strike one another. Second, the lack of a skin coating on antlers means that any blocked tusk blows will not result in bleeding, torn skin, and a risk of infection. And third, it explains why antler size and tusk size are inversely matched among cervids; with large enough antlers, scoring a blow on your opponent becomes nearly impossible, and thus large tusks are rendered useless. As far as just-so-stories in evolution go, this one seems satisfying to me.
Moving anteriorly to the tusks, another striking feature of the skull can be seen. The muntjac’s preorbital gland is proportionally quite large, occupying an almost orbital-sized area of the snout. Muntjacs, especially the large-glanded males, seem to rely especially heavily on scent markings produced by these glands, and therefore have a specialized facial musculature designed to evert them as far as possible for marking. Unlike in North American cervids, which have relatively little actual muscle associated with their preorbital glands, muntjacs, especially the large-glanded M. reevesi, actually involve five facial muscles in the opening of these glands (Barrette 1976).
A Dwindling Karyotype
It’s well-known that the Indian muntjac, Muntiacus muntjak, has the lowest recorded diploid chromosome number of any mammal, with a diploid count of just 6 chromosomes in females and 7 in males. What’s less appreciated is that out of a baker’s dozen extant species, only M. muntjak has this low chromosome count – though others are close. M. reevesi has a diploid count of 46 in both sexes (Wurster & Benirschke 1970) while M. feae has 13 (female) to 14 chromosomes (male), and M. gongshanensis have 8 (female) to 9 (male) (Tsipouri et al. 2008). Even stranger, M. muntjak and M. reevesi can breed successfully, though the offspring are infertile. In order to reach this karyotype, M. muntjak is estimated to have undergone at least 29 tandem head-to-tail chromosome fusion events since the cervid common ancestor, which had an estimated 70 chromosomes (Tsipouri et al. 2008). Keep in mind that though 70 chromosomes seems like a lot (humans have 46), it’s a reasonable number for mammals.
Even stranger, perhaps due to this extreme chromosomal conglomeration, M. crinifrons, the black muntjac has evolved a bizarre five-chromosome sex determining system. Males (2n=9) have sex chromosomes X1, X2, Y1, Y2, and Y3. X1 is derived from the original X chromosome plus an autosome, Y1 consists of the “real” Y chromosome only, and the other three consist of autosomal material (Huang et al. 2006). The reasons for this extreme (and rapid – occurring over the space of just a few million years (Wang & Lan 2000)) regime of chromosomal fusion throughout Muntiacus are tremendously unclear, but it does seem to be due to some inherent genetic quirk of the animals, especially since the tandem fusions in M. crinifrons are all telomere-centromere events (Huang et al. 2006). I’d think this would point towards some sort of metaphase control mechanism gone awry, but experts suspect instead that homologous repetitions in telomeres and centromeres are to blame.
Also of interest, and probably related to the chromosomal fusions, is the reduction in genome size in low-chromosome number muntjacs. Compared to M. reevesi, M. muntjak‘s genome is about 20% (!) smaller, a reduction primarily driven by a rapid drop in intron size (Zhou et al. 2006), which is associated with a likely recent increase in mutation rate in the muntjac lineage. What does all of this mean? Well, it seems that intron reduction and increased mutation go hand in hand. Work on Drosophila has also shown a negative correlation between intron size and mutation, although this is suggested to be an effect of cis-regulatory elements in introns; if an intron contains many cis-regulatory elements, it’s going to evolve much more slowly because mutations are much more likely to become deleterious (Marais et al. 2005). While this is useful information, it doesn’t explain why such a rapid decrease in intron size would cause a higher mutation rate, or vice versa, since presumably cis-regulatory elements are necessary components of any intron they’re in. This, at least, makes sense in light of the muntjac data, as longer introns in muntjacs were much more likely to be truncated than already short introns, which suggests that you can only cut the intron so much before you get down to a minimum size, conserving regulatory elements. Does chromosome fusion drive intron size reduction in Muntiacus? It looks like we just don’t know for sure yet.
Muntjacs Past and Present
The muntjac fossil record reaches back at least 7-9 million years into the Upper Miocene of the Yunnan province of China (Dong et al 2004), though a large dropped antler likely referable to the genus from Quinghai province would extend the occurrence back to 11 Mya at the earliest (Dong 2007). Though both of these species (M. leileilaoensis from Yunnan and M. noringenensis from Quinghai) are based on very little material – the most complete, M. leileilaoensis is based on two specimens of antler pedicles with an antler and pieces of frontal – their assignment to Muntiacus is pretty obvious. This relatively old age matches rather nicely with the idea that muntjacs represent something like an ancestral cervine, bearing both antlers and tusks. Another eight fossil muntjacs have been named apart from leileilaoensis and noringenensis, although nonoverlapping material means there may not be a real morphological distinction between some taxa (Dong et al 2004). But what’s a species anyway?
Well, a species of muntjac can often be defined by its karyotype, and karyotypes don’t fossilize well. Recent (as in, the past thirty years) discoveries of new species such as M. puhoatensis, M. vuquangensis, and M. atherodes and elevation of old subspecies to species status mean that the IUCN now recognize thirteen species of Muntiacus. The most recent taxonomic revision resulted in two species of Indian muntjac or “red muntjac,” M. muntjak (Southern) and M. vaginalis (Northern). While several muntjacs are listed as being of least concern, at least M. vuquangensis is endangered, and all populations for which sufficient population data has been collected are decreasing in size primarily because of habitat destruction and hunting.
There is one place that muntjac populations are on the rise, though. Southeast Asia isn’t the only place in the world where muntjacs roam free, and a growing number of the M. reevesi can be found in England, Wales and Ireland. First introduced in 1900 by the Duke of Bedford, the deer have been deliberately released in many areas across Britain and their populations are increasing. As a result, they are exerting a negative impact on understory plants in areas where they browse, and often compete for resources with native deer (Carden et al 2011). The world is becoming a biogeographical trainwreck.
That’s all I have to say about muntjacs at the moment. Writing and researching this was quite fun, and these little deer proved to be stranger than I knew them to be. Expect more illustrations in future posts.