Illustration of an African Giant pangolin Smutsia gigantea, by John Wolf. Image in public domain.

Further to the previous article on placental mammal phylogeny, I now want to start looking at a few specific details of the tree – details that are somewhat surprising in view of traditional ideas about the groups concerned. A disclaimer: those of you up to date and informed as goes placental mammal phylogeny will be familiar with the relationships and discoveries discussed in these articles.

Sometimes when I look at pangolins I can imagine a civet-like mammal beneath those scales. This is a captive Tree pangolin Phataginus tricuspis. Image by Николай Усик, CC BY-SA 3.0.

The incredible pangolins (properly Pholidota) are toothless, scale-covered, long-tailed insectivores, convergent in some respects with insectivorous xenarthrans. Living pangolins resemble xenarthrans in having a strongly reduced dentition, a rectus thoracis muscle, a weirdly modified mastoid and occipital region, a near-absent or absent subarcuate fossa in the skull, and an extensively fused sacrum-pelvis complex. For these reason, the conventional view of pangolins is that they’re close kin of xenarthrans (Novacek 1992, Gaudin et al. 1996).

The view that pangolins and xenarthrans might be allied goes back the late 1700s when Georges Cuvier and his followers grouped these mammals together with aardvarks in an assemblage termed Edentata. By the late 1800s it seemed likely that this assemblage was artificial (Thomas Huxley implied this in 1872); Oldfield Thomas, nevertheless, grouped Xenarthra and Pholidota together in a placental infraclass Paratheria in 1887, intended to be equivalent to Metatheria and Eutheria. Of course, these interpretations were all based on anatomy and on general aspects of biology and behaviour.

Pangolins look more like xenarthrans (like the giant anteater at left) than they do like carnivorans (like the bobcat at right) - but looks are deceiving. Illustrations by Darren Naish.

What do other lines of data have to say about the position of pangolins? Studies that incorporate amino acid sequences as well as DNA have repeatedly found pangolins to be close relatives of carnivorans (e.g., Shoshani 1986, Springer et al. 2004, Beck et al. 2006, Murphy et al. 2007, Meredith et al. 2011) – a surprising result that doesn’t look obvious based on anatomy or behaviour. Having said that, I recall reading that pangolin skull embryology provides some anatomical support for this relationship – can’t track down the supporting literature though! Furthermore, at least a few characters that might link pangolins and carnivorans have since been identified by O'Leary et al. (2013), including the detailed form of the occipital condyle and astragalus (thanks Albert for reminding me about this data, tucked away in the supplementary information...).

The majority of molecular studies now support this sort of topology: pangolins are nested within Laurasiatheria and Scrotifera, and are the sister-group to Carnivora.

Based on the fossil record, pangolins and carnivorans must have diverged more than 50 million years ago. Du Toit et al. (2014) suggested a Late Cretaceous divergence date of c. 87 Ma. Of course, there are supposed stem-carnivorans that date to 55 Ma or more. As yet, however, there are no fossil animals that have been interpreted as potential common ancestors (or close relatives of those common ancestors) of the pangolin-carnivoran clade. Maybe we know of such creatures (there are, after all, a large number of Paleogene fossil mammals that have been suggested to be vaguely related to carnivorans) – maybe ongoing efforts to allocate fossil placentals to precise positions on the new placental tree will identify some of them (several such efforts are due to appear in print very soon). I mean to elaborate on pangolin evolution at some other time -- must discuss the fascinating idea that they originated as herbivores...

Dated image from years past showing Eurotamandua from the Eocene of Germany reconstructed as a xenarthran. Nope: it's actually a stem-pangolin. Illustrations by Darren Naish.

The many stem-pangolins. On that note, a large number of fossil taxa now regarded as stem-pangolins are known. Gaudin et al. (2009) recently reviewed the pangolin fossil record and identified Patriomanis and Cryptomanis, Necromanis, Eomanis and Euromanis as successively more distant members of Pholidota (they used Manidae for the crown-clade). Eurotamandua – the controversial mammal from the Middle Eocene of Messel, Germany, originally proposed to be a European xenarthran (Storch 1981, Storch & Habersetzer 1991) and specifically an anteater (and previously covered here at Tet Zoo ver 2) – was also regarded as a pangolin, closer to the Eomanis + Manidae clade than is Euromanis. This seemingly resolves the controversy about this animal: Szalay & Schrenk (1998) had previously done a good job of showing that it wasn’t a xenarthran at all but they left its broader affinities unresolved.

An additional group of fossil mammals – the palaeanodonts – also now seem to be stem-members of the pangolin lineage. Gaudin et al. (2009) found palaeanodonts to be a clade (rather than a series of plesions along the pangolin stem) and erected the new node-based name Pholidotamorpha for the Palaeanodonta + Pholidota clade. Among the many anatomical features that unite pholidotamorphs are proportionally wide, flat metatarsals, a wide metacarpal IV, a set of characters involving muscle attachment sites and crests on the forelimb bones, a C-shaped dorsal process on the premaxilla, and an epitympanic sinus (a cavity within the middle ear) between the squamosal and petrosal (Gaudin et al. 2009). Incidentally, note that Rose (1999) had previously suggested a close relationship between Eurotamandua and palaeanodonts.

Reconstructed skeleton of the Eocene palaeanodont Metacheiromys. Note the generally pangolin-like form of the skeleton. Image in public domain.

Palaeanodonts are a very cool little group of mammals and I’ve long planned to write about them at Tet Zoo. Classic, familiar members of the group (example: Metacheiromys from the Middle Eocene of the USA) are long-tailed, long-headed mammals with an approximately pangolin-like demeanour. Many palaeanodonts of this sort are included within the group Metacheiromyidae, the species of which are known from the Upper Paleocene and Lower and Middle Eocene. So far they're only known from the USA and France (members of other palaeanodont lineages are, in addition, known from Canada and Asia).

A cartoon that might be remembered by long-time readers (cough). The animal at the far right is an epoicotheriid palaeanodont. Drawing by Darren Naish.

Somewhat more surprising are those taxa included within the longer-lived group Epoicotheriidae (known from the Upper Paleocene to the Lower Oligocene). Ok, some taxa included in Epoicotheriidae – the classic example is Pentapassalus from the Lower Eocene – are highly similar to metacheiromyids, so much so that “had not the skull and jaws been found the material [of Pentapassalus] would have referred unhesitatingly to [Metacheiromys]” (Gazin, in Rose 1978, p. 666). But we now know that the most ‘advanced’ members of this group had short hands, bizarrely modified forelimb bones, and a flaring, upturned snout and strongly reduced eyes. They were among the most specialised of digging mammals that ever evolved, being convergent overall with golden moles and fairy armadillos (Rose & Emry 1983). Check out this brilliant life restoration by Bonnie Dalzell...

Near-blind, scratch-digging Xenocranium in a burrow: a reconstruction by Bonnie Dalzell, from Rose & Emry (1983).

Bully for Smutsia and Phataginus. One more thing to say on pangolins. The classic view of extant pangolins is that they’re all samey enough to belong in the same one genus: Manis. However, the lineages concerned are really very different in terms of anatomy, proportions, behaviour and biology. Furthermore, some molecular clock studies suggest that these lineages have been distinct for over 40 million years (Du Toit et al. 2014). I therefore agree with Gaudin et al. (2009) that it’s most appropriate to recognise Phataginus for African tree pangolins, Smutsia for African ground pangolins, and to keep Manis for Asian pangolins alone.

A pangolin montage. Clockwise from top left: Ground or Temminck's pangolin S. temminckii by Masteraah, in public domain; climbing Tree pangolin P. tricuspis, in public domain; Sunda pangolin M. javanica by Piekfrosch, image CC BY-SA 3.0; Indian pangolin M. crassicaudata by Sandip kumar, image CC BY-SA 3.0.
You might have strong feelings regarding those members of your own species who harvest, kill, and consume pangolins at a rate way beyond anything approaching sustainability. Pangolin flesh is eaten, and unborn babies are thought to have aphrodisiac properties.

Oh, and – one more thing to say on pangolins. Nowadays, you can’t (or, at least, you shouldn’t) mention pangolins without making reference to the appalling and horribly unsustainable exploitation of these animals for the Asian restaurant trade. Thousands upon thousands are being taken from the wild and eaten. And – remember – all eight or so living pangolin species are CITES listed, meaning that any and all trade in them is completely illegal. Pangolins are, in fact, the most illegally traded mammals in the world. The trade is ethically disgusting and needs to stop (or, at least, drop to sustainable levels). Visit for more and do your bit to help raise awareness of pangolin plight.

World Pangolin Day is 21st February every year – I keep missing it but will aim to do my bit in future. And, yes, more on pangolins (and palaeanodonts) in the future.

For previous articles relevant to topics discussed here, see...

Refs - -

Beck, R. M. D., Bininda-Emonds, O. R. P, Cardillo, M., Liu, F.-G. R. & Purvis, A. 2006. A higher level MRP supertree of placental mammals. BMC Evolutionary Biology 6: 93.

Du Toit, Z., Grobler, J. P., Kotzé, A., Jansen, R., Brettschneider, H. & Dalton, D. L. 2014. The complete mitochondrial genome of Temminck's ground pangolin (Smutsia temminckii; Smuts, 1832) and phylogenetic position of the Pholidota (Weber, 1904). Gene 1, 49-54.

Gaudin, T. J., Wible, J. R., Hopson, J. A. & Turnbull, W. D. 1996. Reexamination of the morphological evidence for the cohort Epitheria (Mammalia, Eutheria). Journal of Mammalian Evolution 3, 31-79.

- ., Emry, R. J. & Wible, J. R. 2009. The phylogeny of living and extinct pangolins (Mammalia, Pholidota) and associated taxa: a morphology based analysis. Journal of Mammalian Evolution 16, 235-305.

Meredith, R. W., Janečka, J. E., Gatesy, J., Ryder, O. A., Fisher, C. A., Teeling, E. C., Goodbla, A., Eizirik, E., Simão, T. L. L., Stadler, T., Rabosky, D. L., Honeycutt, R. L., Flynn, J. J., Ingram, C. M., Steiner, C., Williams, T. L., Robinson, T. J., Burk-Herrick, A., Westerman, M., Ayoub, N. A., Springer, M. S. & Murphy, W. J. 2011. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521-524.

Murphy, W. J., Pringle, T. H., Crider, T. A., Springer, M. S. & Miller, W. 2007. Using genomic data to unravel the root of the placental mammal phylogeny. Genome Research 17, 413-421

Novacek, M. J. 1992. Fossils, topologies, missing data, and the higher level phylogeny of eutherian mammals. Systematic Biology 41, 58-73.

O'Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B. P., Luo, Z.-X., Meng, J., Ni, X., Novacek, M. J., Perini, F. A., Randall, Z. S., Rougier, G. W., Sargis, E. J., Silcox, M. T., Simmons, N. B., Spaulding, M., Velazco, P. M., Weksler, M., Wible, J. R. & Cirranello, A. L. 2013. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339, 662-667

Rose, K. D. 1978. A new Paleocene epoicotheriid (Mammalia), with comments on the Palaeanodonta. Journal of Paleontology 52, 658-674.

- . 1999. Eurotamandua and Palaeanodonta: convergent or related? Paläontologische Zeitschrift 73, 395-401.

- . & Emry, R. J. 1983. Extraordinary fossorial adaptations in the Oligocene palaeanodonts Epoicotherium and Xenocranium (Mammalia). Journal of Morphology 175, 33-56.

Shoshani, J. 1986. Mammalian phylogeny: comparison of morphological and molecular results. Molecular Biology and Evolution 3, 222-242.

Springer, M. S., Stanhope, M. J., Madsen, O. & De Jong, W. W. 2004. Molecules consolidate the placental mammal tree. Trends In Ecology & Evolution 19, 430-438.

Storch, G. 1981. Eurotamandua joresi, ein Myrmecophagidae aus dem Eozän der “Grube Messel” bei Darmstadt (Mammalia, Xenarthra). Senckenbergiana lethaea 61, 247-289.

– . & Habersetzer, J. 1991. Rückverlagerte Choanen und akzessorische Bulla tympanica bei rezenten Vermilingua und Eurotamandua aus dem Eozän von Messel (Mammalia: Xenarthra).Zeitschrift für Säugetierkunde 56, 257-271.

Szalay, F. S. & Schrenk, F. 1998. The Middle Eocene Eurotamandua and a Darwinian phylogenetic analysis of ‘edentates’. Kaupia 7, 97-186.