We still know nearly nothing about synapsid integument

In 2018, I attended a talk about end-Permian ecosystem collapse by Smith et al. (2018) at that year’s Society of Vertebrate Paleontology conference in Albuquerque. The presenter mentioned a mass Lystrosaurus death site from earliest Triassic South Africa. That in itself is cool, but he offhandedly mentioned some preserved some individuals with mummified skin – showing us a picture – and then zoomed on to the next topic. Needless to say, the Q&A session was all about the mummified specimens. It left us all hungry for more information. Well, now it’s been published! The mummified specimens are only two individuals in a bone bed of hundreds of juvenile and subadult Lystrosaurus, who seem to have all died during a drought (Smith et al. 2022).

That’s a Lystrosaurus with skin on it! These are the only pictures freely out there right now, from Smith et al. 2022.

What does this mean for the greater picture of synapsid integument? Ultimately, not much.

There’s still extremely little evidence for what the integument of non-mammalian synapsids looked like. Very few skin impressions have survived from the Pennsylvanian-Early Triassic to now, and very few lagerstätten that would preserve non-mammalian synapsids exist. We have only scraps from which we can make our deductions. So what do we have, and does it mean anything?

The best evidence for synapsid integument is at the very base of the tree – maybe. Enter varanopids. Heleosaurus and Ellitosmithia both preserve dermal osteoderms (Botha-Brink and Modesto 2007), though this doesn’t necessarily tell us anything (as xenarthrans demonstrate, osteoderms and hair aren’t mutually exclusive). More recently, the excellently-preserved skin of Ascendonanus reveals overlapping, diapsid-like scales in this taxon (Spindler et al. 2018). The implication of this would be that amniotes ancestrally had diapsid-like scales, and that these were lost somewhere in eupelycosaurs. That would be neat!

Ascendonanus. From Spindler et al. 2018.

Except, varanopids might not be synapsids at all. Recent phylogenetic analyses by Ford and Benson (2018, 2020) found varanopids to be nested well within diapsids, based on among other things their similarity to the (mostly) unambiguous diapsid Orovenator. That would make scales completely unsurprising. The debate is still ongoing, with some more recent papers upholding synapsid affinities (e.g., Simões et al. 2022), so we’ll see where the pendulum settles.

Or are we? There is more very fragmentary evidence for the presence of scales in “pelycosaurs”. Possibly. In 2012, Niedźwiedzki and Bojanowski (2012) described a trace fossil from a putative pelycosaur from the Early Permian of Poland. The trace fossil consists of belly and tail imprints and a well-preserved foot that can be referred to the ichnotaxon Dimetropus leisnerianus, presumed to be made by pelycosaurs. The body imprints seem to show rectangular scales, which suggests that at least the ventral side of the body was scaly in whatever made this. We can’t know which pelycosaur taxon made this impression, though Romano et al. (2016) suggest that D. leisnerianus pertains to sphenacodontid footprints specifically. If this holds up, then this impression would support the presence of ventral scales in Sphenacodontidae. That would imply that synapsids may have had started off with scales regardless of where varanopids end up, and retained them right up to the base of Therapsida.

Thanks to a ?sphenacodontid deciding to sit down here in the early Permian, we know it may have had ventral scales. From Niedźwiedzki and Bojanowski 2012.

Therapsids, on the other hand, do have a few bits of unambiguous skin preserved, and they show that therapsids didn’t have scales, at least. The most famous piece of therapsid skin is the one from Estemmenosuchus uralensis. Chudinov (1968) reported some skin found associated with the skull of Estemmenosuchus. As preserved, the skin is extremely thin and basically adheres to the underlying bone. It’s got these tiny (0.3-0.45 mm) knobbles (see below) interpreted as glands. It’s been presumed that this is indicative of Estemmenosuchus having bare, hairless skin. I think it’s too fragmentary to say conclusively one way or the other – this is only a tiny chunk of skin from the head; we can’t say anything for certain about the rest of the body. And since this is only one specimen, we can’t confidently drag this out to all dinocephalians, let alone this necessarily being the basal state for all therapsids. Chudinov (1983) also reports skin associated with the anteosaurid Archaeosyodon praevenator and whatever Eotitanosuchus olsoni is*, but they’re described as poorly preserved, aren’t figured, and no further information is given about them, so they offer little help.

* Depending on who you ask, Eotitanosuchus is either a basal therapsid not in any major group (Hopson and Barghusen 1986, Sidor and Hopson 1998) or the adult of Biarmosuchus tener (Ivakhnenko 1999).

The skin of Estemmenosuchus uralensis. From Chudinov (1983).

Side note: parts of the Estemmenosuchus skin are colored much darker brown than the rest of it, and Chudinov (1968) suggests that this may be due to the presence of melanin persisting in the fossil. If so, this is the only preserved instance of pigment so far known in non-mammaliaform synapsids. This is fascinating and we’d probably have much more to learn from it… except the skin is seemingly AWOL now. Dang.

Next on the therapsid tree* is anomodonts, of which the only skin currently known is from the mummified Lystrosaurus murrayi (Smith et al. 2022). It’s dessicated, but it preserves a “pustular” texture. It’s hard to get details from the figures given, but it looks… almost toad-like. It’s also superficially similar in texture to the Estemmenosuchus skin, although the knobbles are on a much larger scale. Is that indicative of similar bare skin being widespread in basal therapsids, or is it in part a consequence of taphonomy? We don’t know. The Lystrosaurus skin hasn’t been described in detail yet (the paper focused on the taphonomy of the bone bed), though I expect that’s next on the agenda for the authors. Until it’s described, we won’t know how much the skin was affected by taphonomy, what it would have looked like in life, whether this truly rules out presence of hair, etc. So until then, we can presume that Lystrosaurus was probably mostly hairless, but until we get a full description we can’t say a whole lot more.

* By this I mean the “consensus” therapsid topology, which was first recovered by Hopson and Barghusen (1986) and hasn’t been thoroughly tested since Sidor and Hopson (1998). That topology could change… (Kammerer et al. 2013).

We have no good evidence one way or another for integument in gorgonopsians and therocephalians, and for that matter most of Cynodontia. But there may be some evidence supporting the presence of hair in Permian therapsids, though. In 2015, an assortment of coprolites from the Late Permian of western Russia were described (Bajdek et al. 2015). These coprolites hail from the Vyazniki site, the namesake of the Vyazniki Assemblage Zone (aka Archosaurus rossicus Fauna), which is considered to be uppermost Changhsingian (Golubev 2000, Ivakhnenko 2011). One of these coprolites preserves molds shaped like what looks for all the world like hair. Iron oxide outlines are present, suggesting that this isn’t an artifact of some sort. While we don’t have direct confirmation that that is an impression of synapsid hair, it certainly looks like one (it even has a putative root). Similar structures that may also be hairs have also been described in a carnivore coprolite from the Karoo Basin (upper Endothiodon Assemblage Zone) of South Africa (Smith and Botha-Brink 2011). Bajdek et al. suggest that these could be fungal in origin, but they also point out that both sets of coprolites also contain therapsid bones (so perhaps the hair came from the owner of those bones). If these are indeed therapsid hairs, then they… honestly could have come from anywhere in the therapsid tree. This suggests that hair may have evolved by the very end of the Permian, but we don’t know in what

This is what they look like, by the way. From Bajdek et al. 2015.

There is one piece of preserved skin impressions in therocephalians though, but it’s more or less useless. The matrix around one specimen of Promoschorhynchus platyrhinus preserved textured surfaces that suggest there used to be mummified skin there (but not anymore). Being that it’s just an impression of bare mummified skin in surrounding matrix, it’s basically uninformative and doesn’t say much about synapsid skin that we don’t already know. A mold was taken and then it was prepared away (Smith and Botha-Brink 2014).

There are bits of indirect evidence within cynodonts that may have more implications for the evolution of hair – and specifically whiskers. Whiskers (or vibrissae) are, as you probably know, specialized sensory hairs mostly located on the face of mammals. The maxillary whiskers (i.e. the “mustache” area) are innervated by the maxillary nerve, which runs through the infraorbital foramen of the maxilla; this gives the lip movement. Therefore, the absence of this foramen suggests the lip wasn’t mobile and the whiskers may not have been present. The infraorbital foramen first shows up in the clade Probainognathia, specifically with Probainognathus itself* (Benoit et al. 2016, 2020). This suggests that mobile whiskers, at least, evolved in the Middle Triassic at the (Probainognathus + mammals) clade. This, however, tells us nothing necessarily about full-body fur coverings. We don’t know whether whiskers evolved first and hair covered the body later (which has been suggested for ornithodiran feathers; Persons and Currie 2015), or whiskers evolved from modified hairs that already covered the body.

* Somewhat similar foraminae are also present in chiniquodonts; that may be a transitional state (Benoit et al. 2020)

As a side note, it’s also been proposed that evolution of hair is linked with mammary gland evolution, as mammary glands may be derived from hair-associated glands (Oftedal 2002), but this doesn’t seem to be widely accepted yet. Given mammary glands might have evolved as far back as the Carboniferous origin of synapsids (Oftedal 2012), I have my doubts that the link is 1:1.

There’s further indirect evidence that may point to when hair evolved within cynodonts, and it’s pretty consistent with the whisker evidence. It all links to the homeogene Msx2. Msx2 is involved in many things, including hair follicle maintenance, mammary gland development, cerebellum development, ossification of the middle ear bones, and condensing the dorsal skull bones – notably, closing the parietal foramen. The parietal foramen is the hole in the skull where the parietal eye sits. Knocking out this gene in mice leads to the foramen forming again (Satokata et al. 2000). The parietal foramen is lost in Probainognathia (Rubidge and Sidor 2001), suggesting that the Msx2 homeogene mutated to the modern mammalian state in this clade. Msx2 also regulates hair follicle maintenance – but not development – so this suggests that hair evolved either at this point or sometime before it (Benoit et al. 2016).

The next direct evidence that we get of fur in association with a skeleton is all the way in mid-Mesozoic Mammaliaformes. Several non-mammal mammaliaforms are known from the mid-late Jurassic Tiaojishan Formation of China, which is well-known for preserving integument in fine detail. Fur has been preserved in the docodont Castorocauda (Ji et al 2006) and the haramiyidans* Megaconus (Zhou et al. 2013), Arboroharamiya (Han et al. 2017), Maiopatagium (Meng et al. 2017), and Vilevolodon (Luo et al. 2017). Interestingly, the latter three haramiydians appear to have been gliders, based on morphometrics (Luo et al. 2017, Meng et al. 2017) and patagia preserved in many of these specimens (Han et al. 2017, Luo et al. 2017, Meng et al. 2017); they may have been comparable to colugos or gliding rodents ecologically. And I think that’s pretty cool. Back on topic – based on these, the presence of fur can be traced back to the (Docodonta + Haramiyida + crown-Mammalia) clade. We don’t know how far back on the branch of that clade fur was also present; we simply have no direct evidence.

* The interpretation of haramiyidans as stem-mammals follows the results of Luo et al. (2017) and Huttenlocker et al. (2018). But other studies (e.g. Han et al. 2017) find haramiyidans to be crown-mammals.

The holotype of Castorocauda lutrasimilis. Note that, like some rodents, it has scales on its tail and fur on the rest of the body. From Ji et al. 2006.

As another thing to factor in, we haven’t talked about endothermy yet. Mammals are ancestrally endothermic; synapsids were not. Insulating hair covering the body probably evolved after endothermy did (if you’re ectothermic, you don’t need a hairy covering). The problem is, we don’t know exactly when endothermy evolved on the synapsid line. A whole review of the evolution of endothermy in synapsids would be outside of the scope of this blogpost, but it’s been suggested that endothermy could have evolved anywhere from within Mammaliaformes (Newham et al. 2020) to as far back as sphenacodonts (Grigg et al. 2022) and everywhere in between (e.g., Faure-Brac and Cubo 2020, Benton 2021). And it’s even been suggested that endothermy evolved multiple times in therapsids (Rey et al. 2017). So until we start coming to a consensus this doesn’t help narrow it down much.

So where does that leave us? The scraps of information we have can show us a vague picture. Scales were definitely present in varanopids, so if those are synapsids that implies the presence of scales ancestrally in the clade. Scales might have remained up until Sphenacodontidae. Therapsids probably started out with scaleless glandular skin, and at least dicynodonts appear to have kept that. Mammaliaforms definitely have hair, and indirect evidence suggests that it may have appeared by the clade Probainognathia. But when exactly hair evolved between the base of Therapsida and Mammaliaformes is still an unknown.

What does this mean for paleoart? As long as you’re consistent with the above constraints, go wild.

Kudos to John D’Angelo for reviewing this post and bringing the therocephalian skin impression to my attention!

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