I spy, with my (not so little) eye

Busy week, so just a short post this week about some bones in the eye (yes, they actually are in the eye); it's not entirely random - Lars Schmitz, my former anatomy professor, is coming to UTM to give a talk on the evolutionary signals in vertebrate eyes (an unsurprising topic selection if you know him).

Examples of scleral rings in vertebrates. Common names in alphabetical order of images: great barracuda, cownose ray, mahi mahi, tarpon, wahoo, king mackerel, wild turkey, rock monitor lizard, eagle-owl, scarlet macaw, goose, crocodile monitor lizard, caiman lizard (figure from Franz-Odendaal, 2018)

....there are bones in the eye?
Well, not in your eye (I hope). Mammals are relatively unique among vertebrates in that we don't have any kind of supporting bones in our eyes. This extends far back in the fossil record as well. Unsurprisingly, monotremes like the platypus are not like other mammals and have a sclerotic cartilage, which is found in cartilaginous fish and lungfish, for example. But many other animals, both extinct and living, have bony plates sitting in a layer within the eye (see below phylogeny for distribution).

Reconstruction of Branchiosaurus salamandroides, scleral rings in green (modified from Fritsch, 1883).

Examples of sclerotic rings in mosasaurs (large marine reptiles frequently mistaken for dinosaurs), figure from Yamashita et al. (2015).

Okay, so what are these bones?
There are two types of ocular (eye) ossifications that can be found in temnospondyl eyes, neither of which are exclusive to temnospondyls and which are probably best identified in other clades as far as extinct tetrapods go (see ichthyosaurs for a good example).

Scleral (sometimes 'sclerotic') plates form the sclerotic ring, a circular structure that supports the eye (among other functions), particularly in aquatic animals and animals without spherical eyes. The name comes from the sclera, one of the many layers of the eye that is most commonly referred to as the "white of the eye." The ring can be cartilaginous but is most often preserved as bony plates. They are usually thin, although not necessarily flat. 

​Palpebral bones, sometimes referred to as a singular palpebral cup unit, are the second type of ossification. As the name implies, these sit near the eyelids, even though the presence of an eyelid is usually not known (eyelids are not found in all vertebrate groups, being most noticeably absent in reptiles). In many instances, they are found in many pieces, like the sclerotic plates, but asymmetry between the shape of the various pieces within and between eyes suggests that they originally formed a single plate (e.g., Carroll, 1964). The somewhat loose terminology used in many early tetrapods should not be confused with the 'palpebral' as defined in many reptiles, which is a discrete element and which has been determined to be an osteoderm (the same as the bony plates on the back) in crocodiles (Vickaryous & Hall, 2008). Homology of these elements also hasn't been established across all tetrapods, only within particular groups.

Distribution of the ocular skeleton among vertebrates. Blue = cartilage; red = bone. 'X' represents loss of a structure, colours as above. (A) all vertebrates; (B) focus on teleost fish. Figure from Franz-Odendaal (2018).

Photographs and illustrations of a specimen of the Permian amphibamiform Tersomius texensis, figure modified from Maddin et al. (2013). Extensive plates in the orbits (coloured in red) are interpreted to be fragments of the palpebral bones.

Palpebral bones ('ppb') in the Permian amphibamiform Rubeostratilia texensis, figure from Bourget & Anderson (2011).

How do you differentiate a scleral ring plate from a palpebral bone (or fragments of it)?
Obviously when either is articulated or fully complete, it's a little easier to differentiate them. When they're not, palpebral bones are often ornamented as well, like the skull roof, whereas scleral rings are smooth. The palpebral bone also tends to break into pieces of various sizes, whereas the plates just disarticulate but are otherwise of about the same size.

So what do we actually know about these ossifications' function in temnospondyls?
There isn't very much research into the eye ossifications in temnospondyls because they occur fairly rarely and are often broken or disarticulated. Because the scleral ring comprises many plates that disarticulate after death, and the palpebral bone seems to break readily into many pieces, loss during preservation is highly likely, which compromises the use of their presence / absence in phylogenies, similar to other small and mostly unattached bones. The palpebral bone probably acted in a similar fashion to those in living vertebrates where it mainly supports the eyelid. 

The function of temnospondyl scleral rings are more difficult to infer. They occur in both large and small, aquatic and terrestrial temnospondyls, so like many other aspects of their anatomy, they may serve relatively limited functions and be inherited through phylogeny. Although it's appealing to try to draw some sexy ecological inference from what appear to be relatively large rings and relatively large orbits in temnospondyls, different selection pressures affect and maintain scleral rings (i.e. there is no simple explanation), so aquatic versus terrestrial animals probably evolved scleral rings with different primary functionalities, sometimes for improving vision, sometimes for reinforcing the eye, muscle attachment for accommodating the lens, etc. Presence / absence and number of sclerotic plates in other groups of vertebrates is sometimes correlated with differing ecologies; deep-sea and relatively inactive fish, for example, either lack scleral ossicles altogether or reduce the number of these ossicles (e.g., Franz-Odendaal, 2008). The relative size of the scleral ring to the eye has also been used to infer activity patterns of various terrestrial animals (e.g., Schmitz & Motani, 2011, see below figure). Unfortunately, sclerotic ossicles are too uncommon (and rarely articulated) in the temnospondyl record to make much of them, and modern amphibians have lost them (but do occasionally have other ossified structures), so there isn't a good living homologue (or analogue). They may just as well as served a function for maintaining the structure of the eye in temnospondyls.

Comparisons of the scleral ring in scotopic (nocturnal) animals, with the gecko Rhacodactylus (E) as an example, and photopic (diurnal) animals, with the monitor lizard Varanus as an example, figure from Schmitz & Motani (2011).

There's been a ton of work looking at the sclerotic ring in particular as a proxy for inferring activity patterns (diurnal, nocturnal, etc.) in other tetrapods! If you're looking for some good (and short) examples:

• Angielczyk KD, Schmitz L. 2014. Nocturnality in synapsids predates the origin of mammals by over 100 million years. Proceedings of the Royal Society B: Biological Sciences 281(1793): 20141642. doi: 10.1098/rspb.2014.1642
• Schmitz L, Motani R. 2010. Morphological differences between the eyeballs of nocturnal and diurnal amniotes revisited from optical perspectives of visual environments. Vision Research 50(10): 936-946. doi: 10.1016/j.visres.2010.03.009
• Schmitz L, Motani R. 2011. Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science 332(6030): 705-708. doi: 10.1126/science.1200043​​

​Refs

• Bourget H, Anderson JS. 2011. A new amphibamid (Temnospondyli: Dissorophoidea) from the Early Permian of Texas. Journal of Vertebrate Paleontology 31(1): 32-49. doi: 10.1080/02724634.2011.539652
• ​Carroll RL. 1964. Early evolution of the dissorophid amphibians. Bulletin of the Museum of Comparative Zoology 131: 161-250.
• Franz‐Odendaal TA. 2008. Scleral ossicles of teleostei: evolutionary and developmental trends. The Anatomical Record 291(2): 161-168. doi: 10.1002/ar.20639
• Franz‐Odendaal TA. 2018. Skeletons of the eye: an evolutionary and developmental perspective. The Anatomical Record (early view). doi: 10.1002/ar.24043
• Fritsch A. 1883. Fauna der Gaskohle und der Kalksteine der Permformation Böhmens. Von Dr Ant. Fritsch. F. Rivnaǒ.
• Maddin HC, Fröbisch NB, Evans DC, Milner AR. 2013. Reappraisal of the Early Permian amphibamid Tersomius texensis and some referred material. Comptes Rendus Palevol 12(7-8): 447-461. doi: 10.1016/j.crpv.2013.06.007
• Vickaryous MK, Hall BK. 2008. Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. Journal of Morphology 269(4): 398-422. doi: 10.1002/jmor.10575
• Yamashita M, Konishi T, Sato T. 2015. Sclerotic rings in mosasaurs (Squamata: Mosasauridae): structures and taxonomic diversity. PloS one 10(2): e0117079. doi: 10.1371/journal.pone.0117079