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Tetrapod Zoology

Tetrapod Zoology

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Nasalis among the odd-nosed colobines or The Nasalis Paradox (proboscis monkeys part II)

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Yay, more primates. Right?

Yet another well adorned male Proboscis monkey. Photo by Bjørn Christian Tørrissen, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

Before moving on to other things (the list of subjects that need to be covered at Tet Zoo ASAP is now worryingly and impractically long), I must finish with the Proboscis monkey Nasalis larvatus [adjacent photo by Bjørn Christian Tørrissen].

In the previous article I discussed various aspects of this fascinating monkey’s distribution, ecology and behaviour. We also looked at the fact that – like so many Bornean endemics – it's endangered by habitat loss and fragmentation. In this second article on the species we look at what I’ll call the “Nasalis Paradox”, and at the position of the species with respect to its relatives.

Despite frequent references in popular texts on primates to limb proportions and hand and toe form, surprisingly little technical information is available on the anatomy of the Proboscis monkey. Well, I shouldn’t really refer to this absence of information as ‘surprising’ given that anatomical data on any given animal is typically hard or impossible to find. Like so many animals, the Proboscis monkey is definitely full of surprises. Matsuda et al. (2011) recently showed that it practices merycism: that is, it regurgitates partially digested plant food, chews it, and swallows it again. That’s right – the Proboscis monkey is a ‘cud-chewing’ ruminant, convergent with artiodactyls (and those other mammals that chew the cud). So far as we know at the moment, the Proboscis monkey is unique among primates in this respect.

Many monkeys are highly flamboyant. This is one of the pig-tailed macaques (either Macaca leonina or M. nemestrina). Macaques like this are somewhat similar in coat colour, body proportions and so on to the Proboscis monkey.

Another thing that makes the Proboscis monkey especially interesting is the contention that it seems to be one of those animals that leads a lifestyle that it’s seemingly not well adapted for (regular readers will recall my recent mention of the “Anatomy is not destiny” maxim, one of my favourite concepts in historical biology). Its limb proportions, tooth anatomy (it exhibits strong alveolar prognathism*) and skin and coat colour are all of a sort normal for strongly terrestrial monkeys, like macaques, not arboreal ones. The strong sexual dimorphism present in the species is also more typical of terrestrial monkeys than arboreal ones. To quote Brandon-Jones (2006), “These adaptations indicate that the genus evolved in woodland characterized by an openness demanding considerably more terrestrial locomotion than the mangrove and lowland rainforest it currently inhabits” (p. 341). This is the “Nasalis Paradox”.

* That is, the sockets of its teeth are directed so that the teeth themselves project outwards from the jaws.

As I hope to explain here, we get a better perspective on this issue by thinking about things in a tree-based (that is, phylogenetic) context: how does the Proboscis monkey compare in morphology and habitat choice to its close relatives? Is it really such a paradox, or have we been duped by misleading anatomical similarities? In order to investigate this further, we need to visualise the Proboscis monkey within phylogeny [photo below by Frank Wouters].

Male and female Proboscis monkey engaging in allogrooming. Nice view of the pelage details. Photo by Frank Wouters, licensed under Creative Commons Attribution 2.0 Generic license.

Whereabouts do Proboscis monkeys belong within the Old World monkey radiation? They’re certainly colobines* but, beyond that, there has been a reasonable amount of disagreement; in fact, the phylogeny of Asian colobines has become a fairly hot topic within Old World monkey research since about 2003.

* There have been several efforts to get Colobinae – the sister-group of Cercopithecinae – ‘upped’ in rank to become Colobidae. Most texts, however, still list Colobinae and Cercopithecinae as ‘subfamilies’ of Cercopithecidae.

Many odd-nosed colobines are elaborately ornamented, colourful monkeys. This is a Red-shanked douc (Pygathrix nemaeus). Photo by Bjørn Christian Tørrissen, licensed under Creative Commons Attribution-Share Alike 3.0 Unported license.

The Proboscis monkey has frequently been considered a very close relative of the Simakobu, Pig-tailed langur or Pig-tailed snub-nosed langur Simias concolor of the Mentawai Islands off western Sumatra. Both are similar in limb proportions, pelage characters and in having narrow, long-faced skulls with long, narrow nasal bones. In fact some authors have included the Simakobu within Nasalis, the genus that is otherwise uniquely reserved for the Proboscis monkey. A sister-group relationship between the two is seemingly supported by molecular data (Whittaker et al. 2006); whether Simias and Nasalis are regarded as congeneric or as sister ‘genera’ is therefore down to preference. The Simakobu is a poorly known, strongly arboreal monkey and is reported to spend time in pairs rather than large groups.

The general idea that Asian colobines - grouped together as the clade Presbytina - can be divided into an ‘odd-nosed colobine’ and a langur and leaf monkey clade has been around since the 1970s (Groves 1970). An alternative hypothesis regarded the Proboscis monkey as an unusual colobine with an ‘isolated’ phylogenetic position: unlike the others, it has 48 chromosomes (the others have 44), so was regarded as ‘primitive’. Bigoni et al. (2003) argued that the high chromosome number is not a primitive character but the result of unusual splitting events that upped the ancestral number. These authors argued that the Proboscis monkey is deeply nested within the colobine radiation.

This has been given additional supported by more recent molecular work (Sterner et al. 2006, Whittaker et al. 2006, Osterholz et al. 2008, Perelman et al. 2011, Wang et al. 2012), all of which has shown that the Proboscis monkey is indeed part of that 'odd-nosed colobine' clade hypothesised by Groves (1970). However, several different topologies have been recovered for the different odd-nosed colobine taxa. Osterholz et al. (2008) found Nasalis to be in an unresolved polytomy with Rhinopithecus (snub-nosed monkeys) and Pygathrix (doucs), with Presbytis (surilis) and Trachypithecus (lutongs) belonging to a sister-group [douc photo above by Bjørn Christian Tørrissen]. Meyer et al. (2011) found Nasalis to be the sister-taxon to a douc + snub-nosed monkey clade while Perelman et al. (2011) and Wang et al. (2012) supported a closer relationship between the Proboscis monkey and the doucs rather than with the snub-nosed monkeys. As mentioned above, Simias is probably closer to Nasalis than to any other odd-nosed colobine (Whittaker et al. 2006).

Old World monkey phylogeny (with some hominoids too), from Wang et al. (2012). We're interested in the topology among Asian colobines.

As always, the recovery of a robust phylogeny does more than just allow us to hang species on branches; we can now formulate, and perhaps test, hypotheses about patterns of evolution. Living odd-nosed colobines are unlike other Asian colobines in being exclusive to Southeast Asia and Borneo, so the phylogeny strongly suggests that they’re always been limited to this region and are hence tied to its ecology and biogeography.

One of the prettiest monkeys (according to some): Golden snub-nosed monkey (Rhinopithecus roxellana). Photo by Jack Hynes, licensed under Creative Commons Attribution-Share Alike 2.0 Generic license.

You’ll recall from earlier that the Proboscis monkey is (supposedly) seemingly more ‘terrestrial’ in its anatomy than ‘arboreal’. What might the phylogeny tell us about the expected ancestral mode of life for this species, and about that “Nasalis Paradox”? Doucs and snub-nosed monkeys are both forest-dwellers, with populations inhabiting a diversity of coniferous, broadleaved temperate, and evergreen tropical habitats. The Pig-tailed langur is also very much a forest animal, and indeed is described as strongly arboreal [adjacent illustrations of Golden snub-nosed monkey pair by Jack Hynes].

So far as I can see, this could all means one of two things. The first possibility is that the Proboscis monkey comes from a long line of forest-dwelling, mostly arboreal, odd-nosed colobines. Its mostly arboreal, forest-dwelling lifestyle is thus normal for its clade, and those so-called terrestrial features have been misinterpreted: they aren’t indications of a former terrestrial life at all.

The second possibility is that, while it today occurs in forests and is mostly arboreal, the Proboscis monkey (or, at least, populations along its stem-lineage) really did go through a phase of being strongly terrestrial and hence very different from the other odd-nosed colobines – it’s just that this didn’t work out, and the species had to revert to the ancestral, forest-dwelling, mostly arboreal way of life.

Interested in primate diversity, phylogeny and evolutionary history? Then be sure to obtain Ian Redmond's excellent The Primate Family Tree, republished as Primates of the World.

Scientific hypotheses are meant to be led by parsimony (the concept that the simplest solution to a problem is the likely correct one). Viewed within the context of parsimony, the first hypothesis is the favourable one. But that doesn’t mean it’s the best hypothesis. One of the main points of Douglas Brandon-Jones’s article on Asian colobine evolution and history was that climatic fluctuations in Asia’s recent geological past may have had significant impacts on the distribution of the species concerned (Brandon-Jones 1996). He argued that palaeoclimatic data from the Bornean record indicates the existence of an arid phase coinciding with the last glacial maximum of the Late Pleistocene. Supposedly, the reduced forest cover and drier regime that resulted led to species like the Proboscis monkey, seemingly adapted for these more arid, drier woodland habitats. However, biogeographic data from gibbons, orangutans, forest-dwelling langurs and other animals directly contradicts this scenario: it seems instead that Borneo was consistently forested across this time (Earl of Cranbrook 2000, Meijaard & Groves 2004).

It seems appealing to me that there is indeed something in the “Nasalis Paradox” idea, and that members of the Nasalis lineage did go through a ‘dry forest’, semi-terrestrial phase at some stage in their evolution. But I now think that we’ve been duped: that the supposed terrestrial, ‘dry forest’ adaptations of the Proboscis monkey do not represent the vestiges of history, but convergent features with monkeys that evolved in wholly different environments.

For previous Tet Zoo articles on primates, do check out...

And if you are interested in obtaining Ian Redmond's The Primate Family Tree, republished as Primates of the World, please help vital work on primate conservation by purchasing it from the Shop 4 Apes store. And... you don't want to buy anything from amazon anyway, do you? Exactly.

Refs - -

Bigoni, F., Stanyon, R., Wimmer, R. & Schempp, W. 2003. Chromosome painting shows that the proboscis monkey (Nasalis larvatus) has a derived karyotype and is phylogenetically nested within Asian colobines. American Journal of Primatology 60, 85-93.

Earl of Cranbrook 2000. Northern Borneo environments of the past 40,000 years: archaeozoological evidence. The Sarawak Museum Journal 55, 61-109.

Groves, C., 1970. The forgotten leaf-eaters, and the phylogeny of the Colobinae. In Napier, J. R. & Napier, P. H. (eds) Old World Monkeys: Evolution, Systematics and Behavior. Academic Press, New York, pp. 555-587.

Matsuda, I., Murai, T, Clauss, M., Yamada, T., Tuuga, A., Bernard, H. & Higashi, S. 2011. Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus). Biology Letters 7, 786-789.

Meijaard, E. & Groves, C. P. 2004. The biogeographical evolution and phylogeny of the genus Presbytis. Primate Report 68, 71-90.

Meyer, D., Rinaldi, I. D., Ramlee, H., Perwitasari-Farajallah, D., Hodges, J. K. & Roos, C. 2011. Mitochondrial phylogeny of leaf monkeys (genus Presbytis, Eschscholtz, 1821) with implications for taxonomy and conservation. Molecular Phylogenetics and Evolution 59, 311-319.

Osterholz, M., Walter, L. & Roos, C. 2008. Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups. BMC Evolutionary Biology 2008, 8:58 doi:10.1186/1471-2148-8-58.

Perelman, P., Johnson, W. E., Roos, C., Seuanez, H. N., Horvath, J. E., Moreira, M. A. M., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M. P. C., Silva, A., O’Brien, S. J. & Pecon-Slattery, J. 2011. A molecular phylogeny of living primates. PLoS Genetics 7: e1001342.

Sterner, K. N., Raaum, R. L., Zhang, Y. P., Stewart, C. B., Disotell, T. R. 2006. Mitochondrial data support an odd-nosed colobine clade. Molecular Phylogenetics and Evolution 40, 1-7.

Wang, X. P., Yu, L., Roos, C., Ting, N., Chen, C. P., Wang, J. & Zhang, Y. P. 2012. Phylogenetic relationships among the colobine monkeys revisited: new insights from analyses of complete mt genomes and 44 nuclear non-coding markers. PLoS ONE 7(4): e36274. doi:10.1371/journal.pone.0036274

Whittaker, D. J., Ting, N. & Melnick, D. J. 2006. Molecular phylogenetic affinities of the Simakobu monkey (Simias concolor). Molecular Phylogenetics and Evolution 39, 887-892.

The views expressed are those of the author and are not necessarily those of Scientific American.

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