October 2014 continues – for no particular reason at all – to be Lizard Month here at Tet Zoo and right now it’s time for more skinks. The previous article is a sort of general introduction to the group as well as a review of the limbless acontiines/acontids and weird feylinines. This time, we move on in the phylogeny, here dealing with the large number of groups conventionally grouped together as the lygosomines...

Criminally simplified depiction of lygosomine skink phylogeny (topology mostly based on Pyron et al. 2013). Photos (top to bottom) by Wolfgang Wuster, H. Zell, $Mathe94$, Benjamint444 (all CC BY-SA 3.0), Mark Stevens (CC BY 2.0), W.A. Djatmiko, S. Caut et al. (both CC BY-SA 3.0).

Lygosomines account for about half of all named skink species and occur across Asia, Africa and Australasia, and also on many island groups across the Indo-Pacific region. Unlike most other skinks, many (but not all) have an extensive bony secondary palate and fused frontal bones (a complete bony palate evolved independently at least twice elsewhere within skinks: in the Seychellean Janetaescincus + Pamelaescincus clade, and in Gongylomorphus from Madagascar). The group has been found to be paraphyletic with respect to Asian and North American eumecines in some studies (Whiting et al. 2003) but monophyletic in others (Brandley et al. 2005, Pyron et al. 2013).

I think it should be obvious why the Lygosoma species are sometimes called 'writhing skinks'. This is the Asian species L. quadrupes. Photo by W. A. Djatmiko, CC BY-SA 3.0.

At its core, the group of course includes the writhing skinks (Lygosoma), a massive group that includes species in Africa, India, the Philippines and elsewhere [adjacent photo by W. A. Djatmiko]. Like just about all of those speciose, widespread skink genera (see the previous article for discussion), Lygosoma is almost certainly not a clade. The genus was thought to be even bigger in the past that it is now: Allen Geer noted in one of his articles that Lygosoma was “applied at one time to almost one-half (43%) of all the species in the family” (Greer 1977, p. 515). Skinks included within Lygosoma are – morphologically – somewhat nondescript, being long-bodied, streamlined skinks that are often reddish-brown or golden-brown. The biggest (like the west African Fire skink L. fernandi) reach about 40 cm in total length. And even the modern, restrictive version of Lygosoma isn’t monophyletic: it’s paraphyletic with respect to Lepidothyris and Mochlus (Pyron et al. 2013).

Enough about Lygosoma. In the new taxonomic scheme discussed by Hedges (2014), the disparity and diversity recognised for lygosomines in total is such that the group is now elevated to a ‘higher-level’ clade – Lygosomoidea – that houses the seven ‘family-level’ clades Ateuchosauridae, Sphenomorphidae, Eugongylidae, Lygosomidae, Egerniidae, Ristellidae, and Mabuyidae (Hedges 2014). Mabuyids are one of the youngest groups within this clade.

Many-lined sun skink or Common sun skink (conventionally Mabuya multifasciata but now Eutropis multifasciata... should the species name really be multifasciatus?); photo by Lip Kee, CC BY-SA 20.

And I have to resist talking here about the examplar genus of Mabuyidae – the Afroasian-Madagascan-American Mabuya – because... well, there’s a whole world of hurt there [adjacent photo by Lip Kee]. Studies have often suggested that Mabuya sensu lato might not be monophyletic (e.g., Honda et al. 2003) and there’s a push to get the name restricted to American members of the group. Hedges & Conn (2012) erected a full 16 genera for Caribbean species conventionally included within Mabuya and also argued that each of the major clades closely related to Mabuya – the Afro-Madagascan Chioninia and Trachylephis groups and Asian Dasia group – should be recognised as ‘subfamilies’ within Mabuyidae (see Pyron et al. 2013, Hedges 2014). At least some of the 38 or so island-endemic Caribbean mabuyid species are critically endangered or already extinct, predominantly (it's thought) because of mongoose predation (Hedges & Conn 2012).

There are too many eugongylid-type skinks for me to really cover them here. This is a Pacific bluetail skink (Emoia caeruleocauda), one of the many Emoia skinks (sometimes called emo skinks) included within this group. This is a good time to ask that perennial question: why do some skinks (and other lizards) have tails that are so different in colour from the rest of the body? Photo by Ariefrahman, CC BY-SA 4.0.

Phylogenetic studies find the ‘Eugongylus group lygosomines’ of Tasmantis (New Caledonia, New Zealand and Lord Howe Island) to form a clade, with the skinks of New Zealand and Lord Howe Island being nested within an ancestrally New Caledonian clade (Smith et al. 2007) [photo above by Ariefrahman]. This major group is termed Eugongylidae in the new taxonomic scheme (Hedges 2014) and considered to be closely related to Lygosomidae. The young geological age of the taxa concerned indicate that they colonised these islands via over-water dispersal: they are not relicts of Gondwanan fragmentation, as has also been suggested (checks over shoulder for panbiogeographers...).

Where the terror skinks are

Within this eugongylid clade are some of the world’s most interesting skinks. Nannoscincus, for one, has been reported to make squeaking noises when handled (Sadlier et al. 2006).

THE TERROR SKINK LIVES!! Live Phoboscincus bocourti captured on Brosse Islet in 2005. Photo from Caut et al. (2013), CC.

I’m especially fond of Phoboscincus, predominantly because the gigantic ‘terror skink’ P. bocourti supposedly belongs here (though note that “there is some morphological evidence that it may not be congeneric with P. garnieri” (Smith et al. 2007, p. 1161)). This large skink – reaching 50 cm in total – has especially long, curved anterior teeth and “is probably a fearsome super-predator of lizards and possibly birds” according to one source. In fact, most people only know of this skink because of its mention in Tim Flannery’s notorious book The Future Eaters where we read that “There is no doubt that the terrific skink ruled over the smaller reptiles of New Caledonia as effectively as Tyrannosaurus rex did over the lesser dinosaurs of its era, or the lion does on Africa’s Serengeti today” (Flannery 1994, pp. 48-49). Wow – the T. rex of the skink world! Hold that thought.

P. bocourti was long known only from a single specimen, collected sometime around 1872. In the absence of further specimens or sightings, it was then thought to be extinct for decades. It even features in Flannery’s A Gap In Nature, accompanied by a beautiful Peter Schouten painting.

Rendered image of P. bocourti skull (with close-ups of maxilla and mandible) from Caut et al. (2013). The robust, recurved teeth are more formidable than those of most other skinks. Image CC.

However, the ‘terror skink’ was rediscovered unexpectedly in 2003, with subsequent expeditions finding another four individuals and seeing (or ‘camera-trapping’) another four (Caut et al. 2013). Still virtually nothing is known about the ecology or behaviour of P. bocourti, however. Its curved teeth certainly indicate that it might prey on smaller lizards, and the isotope analysis performed by Caut et al. (2013) appears to be in agreement with this hypothesis. It’s certainly good news that P. bocourti isn’t extinct, but there’s every indication that it’s extremely rare, and quite plausibly threatened with genuine extinction.

Land mullets, crevice skinks, and sociality

A montage of species once all included within 'Egernia'. Top to bottom: Gidgee skink or Stoke’s skink (E. stokesii), Land mullet (Bellatorias major), White's skink (E. whitii). Photos by (top to bottom) Mark Marathon, $Mathe94$, and Liese Coulter; all CC BY-SA 3.0.

Egernia-group lygosomines (Egerniidae of the Hedges (2014) scheme) are also very neat. Egernia itself is a large, Australian genus, conventionally thought to contain about 30 species of terrestrial, sometimes burrow-dwelling, skinks that tend to be broad-bodied and proportionally short-tailed. [Adjacent photos by Mark Marathon, $Mathe94$, and Liese Coulter.]

As suggested by the common name used for some of these skinks – spiny-tailed skinks – long spines (actually tall keels on the dorsal surfaces of the scales) project from the broad, flattened tails of these lizards, and they use these tails to block the entrances to their burrows or resting crevices (Pianka & Vitt 2003). Some species (like the Pygmy spine-tailed skink E. depressa) have raised, spike-like scales on the head, neck and body as well as the tail. Big species are more herbivorous than the smaller ones.

As is the case with most speciose skink genera, Egernia encompasses a lot of variation in terms of size, proportions, scale anatomy and overall look. Accordingly, some authors have wanted to see it split into four: Egernia proper (the generally large and bulky crevice skinks and spiny-tailed skinks), Bellatorias (containing the brilliantly named Land mullet B. major and kin), Liopholis (the desert and rock skinks), and Lissolepis (the mourning skinks). Furthermore, Gardner et al. (2008) found Egernia in the traditional sense to be paraphyletic with respect to blue-tongued skinks (Tiliqua) and slender skinks (Cyclodomorphus) and recommended application of this revised taxonomy, the ‘Egernia’ clade close to the blue-tongues being Liopholis (see also Pyron et al. 2013).

I really love this 1846 illustration of a Gidgee skink or Stoke’s skink (E. stokesii). It's from John Lort Stokes's book Discoveries in Australia (anyone know who the artist is?). Image in public domain.

Anyway, the main reason these skinks are so interesting is that they are highly social, complex, apparently intelligent lizards that typically live in family groups. About 23 of those 30-odd species, in fact, have been reported occurring in social aggregations (Chapple 2003), those of Cunningham’s skink E. cunninghami and the Gidgee skink or Stoke’s skink E. stokesii consisting of up to 17 individuals. Members of some species have been shown to recognise other individuals (and to kill newborns that aren't closely related to them), and several species are monogamous and form pairs that stick together for decades. The Great desert skink Liopholis kintorei constructs complex warren-like tunnel systems that can spread over 13 m and contain 20 entrances. Genetics confirms that the individuals that inhabit these burrow systems are relatives: these are colonial, co-operative lizards (McAlpin et al. 2011). Why this sociality evolved is a good question. Did it originate for the same reason that it did in social, burrow-dwelling mammals, like molerats?

And crocodile skinks and monkey-tailed skinks...

Famous Red-eyed crocodile skink (Tribolonotus gracilis) of New Guinea; photo (c) Wolfgang Wuster.

The weird crocodile skinks (Tribolonotus) of New Guinea, the Bismarck Archipelago and the Solomon Islands also belong in this egerniid clade, seemingly as the sister-group to a clade that includes the arboreal Solomon Islands skink or monkey-tailed skink (Corucia), the Cyclodomorphus-Tiliqua complex, and those social skinks (Skinner et al. 2011, Pyron et al. 2013). Given that there are heavily armoured, strongly terrestrial skinks here, specialised arboreal ones, numerous burrowing, desert-dwelling lineages, and short-limbed, massive-headed omnivores, it’s fun to imagine what the ancestral lifestyle and body shape was for the group.

Cyclodomorphus skinks can be imagined as 'prototype' versions of the more robust, generally larger Tiliqua bluetongues. This is a Slender bluetongue (C. melanops melanops) mother and juvenile, photographed in WA. Photo (c) Stephen Zozaya.

The presence of some egerniids on far-flung islands raises interesting questions about their history. Fossils and molecular distance data indicates that various of these lineages split from one another during the Oligocene, so did they use over-land dispersal to get to various of those island locations? In the case of Corucia, genetics indicate that populations on adjacent islands are not necessarily closely related, and that isolated modern populations are young – the overall pattern indicating that the animals have (again) mostly colonised the islands via overwater dispersal within the last few million years (Hagen et al. 2012). In the case of Corucia, this means that there’s still a massive chunk of its inferred history that remains cryptic. Was it somewhere on the Solomon Islands during all of that time, or did it only colonise the islands recently?

The rightly famous Corucia zebrata. There are supposed to be two subspecies: C. z. zebrata and C. z. alfredschmidti. The latter has dark (rather than orange) sclera and hence the animal shown here should belong to that subspecies. Photo by H. Zell, CC BY-SA 3.0.

So, there we have it – a very brief whistlestop tour of yet more of the skinks. For a fuller view as goes the diversity and biology of the groups discussed here, do see Eric Pianka and Laurie Vitt’s 2003 book Lizards: Windows the Evolution of Diversity (Pianka & Vitt 2003) if you can. And we’re not done yet; there are more skinks to come...

Tet Zoo now features some fairly reasonable coverage of squamate diversity, but there is still so much to do.

Dibamids and amphisbaenians

Gekkotans

Iguanians

Lacertids

Skinks and cordylids

Anguimorphs

Snakes

Refs - -

Caut, S., Holden, M., Jowers M. J., Boistel, R. & Ineich, I. 2013. Is Bocourt’s Terrific skink really so terrific? Trophic myth and reality. PLoS ONE 8(10): e78638.

Flannery, T. F. 1994. The Future Eaters: An Ecological History of the Australasian Lands and People. Reed Press, Port Melbourne, Australia.

Gardner, M. G., Hugall, A. F., Donnellan, S. C., Hutchinson, M. N. & Foster, R. 2008. Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae). Zoological Journal of the Linnean Society 154, 781-794.

Greer, A. 1977. The systematic and evolutionary relationships of the scincid lizard genus Lygosoma. Journal of Natural History 11, 515-540.

Hagen, I. J., Donnellan, S. C. & Bull, C. M. 2012. Phylogeography of the prehensile-tailed skink Corucia zebrata on the Solomon Archipelago. Ecology and Evolution 2, 1220-1234.

Hedges, S. B. 2014. The high-level classification of skinks (Reptilia, Squamata, Scincomorpha). Zootaxa 3765, 317-338.

- . & Conn, C. E. 2012. A new skink fauna from Caribbean islands (Squamata, Mabuyidae, Mabuyinae). Zootaxa 3288, 1-244.

Honda, M., Ota, H., Köhler, G., Ineich, I., Chirio, L., Chen, S.-L. & Hikida, T. 2003. Phylogeny of the lizard subfamily Lygosominae (Reptilia: Scincidae), with special reference to the origin of the New World taxa. Genes & Genetic Systems 78, 71-80.

McAlpin, S., Duckett, P. & Stow, A. 2011. Lizards cooperatively tunnel to construct a long-term home for family members. PLoS ONE 6 (5): e19041

Pianka, E. R. & Vitt, L. J. 2003. Lizards: Windows the Evolution of Diversity. University of California Press, Berkeley.

Pyron, R. A., Burbrink, F. T. & Wiens, J. J. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 2013, 13:93 doi:10.1186/1471-2148-13-93

Sadlier, R. A., Bauer, A. M. & Smith, S. A. 2006. A new species of Nannoscincus Günther (Squamata: Scincidae) from high elevation forest in Southern New Caledonia. Records of the Australian Museum 58, 29-36.

Skinner, A., Hugall, A. F. & Hutchinson, M. N. 2011. Lygosomine phylogeny and the origins of Australian scincid lizards. Journal of Biogeography 38, 1044-1058.

Smith, S. A., Sadlier, R. A., Bauer, A. M., Austin, C. C. & Jackman, T. 2007. Molecular phylogeny of the scincid lizards of New Caledonia and adjacent areas: evidence for a single origin of the endemic skinks of Tasmantis. Molecular Phylogenetics and Evolution 43, 1151-1166.

Whiting, A. S., Bauer, A. M. & Sites, J. W. 2003. Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata: Scincidae). Molecular Phylogenetics and Evolution 29, 582-598.