GEOL 431 Vertebrate Paleobiology

Spring Semester 2023

The Reptilian Stem

Synapsida is only half of Amniota. The other half - "reptiles" - contains living turtles, squamates, Sphenodon, crocodylians, and birds, and their fossil relatives. Traditionally, and for most of the age of cladistics, most of its diversity was taken up by Diapsida, characterized by creatures with classic diapsid temporal fenestration or its derivatives. But things have changed. Alas, we have no consensus on:

• The exact shape of its cladogram
• Exactly who is a member
• Proper taxonomic nomenclature for this part of the tree, especially its more basal part.

The last decade has seen no consensus. Consequently the 2023 strict consensus cladogram above is actually less resolved than our naive view from 2015. And yet it is not so bad. Living amniotes, as well as most fossil forms clearly nest within either:

• Synapsida
• Neodiapsida

The wild cards are Paleozoic forms that in one way or another, are not far from the common ancestry of Amniota.

What has changed since 2015:

• Several analyses (E.g. Szostakiwskyj et al., 2015) of "microsaurs" have placed members of Recumbrirostra like Rhynchonkos on the Sauropsid stem. Maybe upon analysis, other "microsaurs" will join them.
• Varanopidae - long regarded as basal synapsids - appeared on the sauropsid side in analysis of Ford and Benson, 2019
• Parareptilia may (Simões et al., 2022) or may not (Ford and Benson, 2019) be paraphyletic.
• Captorhinidae, Hylomonus, and Paleothyris - long regarded as stem sauropsids - recovered by Simões et al., 2022 as stem amniotes!
• Even more disruptively, Simões et al., 2022 recover Araeoscelidia as stem amniotes! Especially problematic as these are the earliest creatures to display classic diapsid fenestration. Most cladistics definitions of Diapsida are hung off of them. If Simões et al. are right, Amniota is nested within Diapsida!

And yet there is a general consensus of research over the last quarter century. Time will tell whether the results of the last five years will demand a wholesale revision of our taxonomy. GEOL431 will follow the structure of this consensus in its 2023 presentations.

Reptilia or Sauropsida?

Both terms have been used for the sister-taxon of Synapsida and neither has a "clean title" to the clade because of issues that haunt us from the early, revolutionary days of cladistics when:

• Systematists were overconfident in the permanence of the phylogenetic hypotheses they developed
• And did not feel obliged to respect rules of priority

Ford and Benson favor Reptilia, however this name has at least four phylogenetic definitions in the literature (Modesto and Anderson, 2004.) Respecting priority, GEOL431 goes with the definition of Gauthier et al., 1988 which is:

"The most recent common ancestor of extant turtles and saurians, and all its descendents."

Given Gauthier et al.'s convictions that:

• Turtles belonged in Parareptilia
• Saurians belonged in Diapsida

...this yielded a nice amniote dichotomy between Synapsida and Reptilia. Alas, the position of turtles in the amniote tree has become one of the most contentious issues in vertebrate phylogeny, with very disparate competing hypotheses, each implying its own roster for Reptilia or making it redundant with other common group names like "Sauria."

Sauropsida is defined by Laurin and Reisz, 1995 as:

"The last common ancestor of mesosaurs, testudines and diapsids, and all its descendents."

This anchors the definition on Mesosauridae - a basal group never appearing on the synapsid side. But alas:

• Ford and Benson place Mesosauridae, along with other members of Parareptilia, far up the tree
• Simões et al. move Araeoscelidia - classic "diapsids" outside Amniota. All of which Laurin and Reisz' definition useless to us as well.

So we punt!

For now and until a proper definition appears, the sister taxon of Synapsida will be referred to as Sauropsida, a name that is at least free of cultural association with traditional definitions of "reptiles."

Sauropsida

We begin in the shadows. Recumbrostran "microsaurs" like Rhynchonkos were covered in a previous lecture, along with concerns indicated in recent redescriptions that they are actually sauropsid amniotes. Evidence includes:

• The presence of an unambiguous supraoccipital element in the braincase. (Ambiguous at best in other non-amniotes.)
• Detailed descriptions of three recumbirostrans by Szostakiwskyj et al., 2015 noting that their supraoccipitals resembled those of basal sauropsids in detail, including the presence of lateral and median ascending processes.
• New redescriptions accompanied by phylogenetic analysis supporting the sauropsid hypothesis. (Mann et al., 2022)

Eureptilia

Euraptilian synapomorphies include:

• Suborbital opening (foramen (right) or fenestra) in palate beneath orbits. Compare with synapsids.
• Single coronoid in jaw. (Link to image.)
• Tabulars reduced or absent

Among living members we also note:

• Color vision.
• Dry aglandular skin with a new kind of scale made of keratin-B (mechanically similar to the keratin-A of your hair and fingernails but chemically distinct - NOT homologous to the scales of fish or temnospondyls.) Note: Mann et al., 2021 describe fossil impressions of the fine squamation of the recumbirostran Joermungandr bolti, but do not specifically conclude that they are keratinous.

Basal Eureptilia

Includes Hylonomus lyelli, a Joggins tree-stump victim and the earliest well-known fossil amniote.

Diversity: Neoreptilia comprises the majority of Eureptilia, but we should note some stem-neoreptilians.

• Captorhinidae: (Late Carboniferous - Late Permian) Eureptiles characterized by adaptations to a strong, slow bite with trends toward rounded crushing teeth in multiple tooth-rows. Including Eocaptorhinus (right) but also larger forms such as Labidosaurikos (~1.5 m).

  Synapomorphies:

  • Complete loss of the ectopterygoid.
  • Complete loss of the tabular.

  
  

  
  Paleothyris acadiana from Carroll, 2009
• "Protorothyridids": (Late Carboniferous - Early Permian) Eureptiles with incipient adaptations to a weaker, quick bite. These include:
  • Paleothyris acadiana (right)
  • Hylonomus lyelli, from Joggins, NS. Arguably the earliest known amniote, but co-occurs with the fragmentary Protoclepsydrops, which might be the earliest synapsid.

  
  

  
  Paleothyris acadiana from Carroll, 2009
  Potential synapomorphies with Neoreptilia:
  • The snout is longer than the temporal region
  • Cervical vertebrae are keeled ventrally.
  • Metatarsals overlap proximally.

  Noteworthy plesiomorphies:

  • The stapes is robust.
  • There is no suggestion of an otic notch.
  I.e. Creatures in this part of the tree did not have an impedance-matching ear.

Diapsida

(Late Carboniferous to Quaternary.) Diapsids are among the first amniotes of the Late Carboniferous, however during the Paleozoic they were a minor component of the terrestrial fauna. That changed during the Mesozoic, when they achieved ecological dominance. Modern diapsids include :

• Birds
• Crocodylians
• Squamates (lizards and snakes)
• Sphenodon, the New Zealand tuatara.

Their fossil members have included the largest/scariest land animals ever, however at their root, they were adapted to life as small, fast-moving predators of small prey items.

Synapomorphies are visible in Petrolacosaurus (Right - Late Carboniferous) the earliest and among the most primitive diapsids:

• Infratemporal and supratemporal fenestrae.
• Suborbital opening in the palate appears as a broad suborbital fenestra.
• Limbs long and slender, emphasizing zeugopodium and autopodium. Typically, radius is at least 70% length of humerus. (Compare Claudiosaurus with non-diapsid Captorhinus.)
• Complex joint between tibia and astragalus that creates a relatively solid immobile articulation between the two. (In extreme cases, as with birds, these elements fuse into a tibiotarsus.)
• Metatarsal IV at least twice the length of metatarsal I. (Link to pes of Petrolacosaurus.)

There are two general patterns here:

• The jaws are long and slender, and the leverage of their adductor muscles limited by the shortening of the temporal region, resulting in a quick but weak bite, suitable for hunting the insects that were diversifying during the Carboniferous.
  Arguably connected with the presence of temporal fenestrae. Abel et al., 2022 used Captorhinus to model the distribution of stress generated by biting across the elements of the skull roof. Their model identifies the location of the infratemporal and supratemporal fenestra as zones of weakness where there may be selective pressure not to deposit bone.
• Lengthening of the limbs (especially of the distal elements) suggest adaptations for faster locomotion.

Diapsid diversity: Diapsids, as generally conceived, are an apomorphy-based group - the sauropsids that ancestrally possess the diapsid pattern of temporal fenestration, They were among the first groups to be studied with the methods of cladistics (See Gauthier, 1984 and Benton 1985).

• Sauria: The crown-group of living diapsids - the last common ancestors of lizards and birds and all of its descendants.
• Araeoscelidia: The monophyletic group at the base of Diapsida

Between them on the saurian stem is an array of fossil stem saurians.

Araeoscelidia: (Late Carboniferous - Early Permian). Small slender animals characterized by:

• Relatively long neck and cervical series (eight cervical vertebrate).

Araeoscelidians are specialized either as arboreal or aquatic animals. Remarkable more for their plesiomorphies, including retention of:

• caniniform teeth
• a lacrimal that extends, unrestricted, to the naris
• the postsplenial of the jaw
• the posterior coracoid
• the cleithrum

At least one member, Araeoscelis secondarily closes the infratemporal fenestra, prefiguring the widespread modifications to the diapsid pattern seen in Diapsida.

Orovenator mayor: (Early Permian). Known only form the anterior skull of a single specimen with diapsid fenestration. Notable because Ford and Benson's, 2018 redescription revealed potential synapomorphies of it and the varanopid "synapsids," causing its inclusion in existing matrices to pull varanopids into Diapsida despite the fact that no varanopid has an open supratemporal fenestra. Recall Dr. Holtz's review of Varanopidae in his discussion of basal synapsids. If Ford and Benson, 2018 are right, then:

• Varanopids' stratigraphic pattern is more congruent with this new phylogeny.
• The enigma that they had presented as a major clade of "pelycosaur-grade" synapsids surviving well into the Middle Permian is resolved.
• Maddin et al. 2020's description of potential parental care in the Late Carboniferous varanopid Dendromaia unamakiensis remains the oldest instance on record among amniotes, but no longer illuminates parental behavior in synapsids.

Possible case study in character polarization: When moved into Diapsida, many of the characters that had made varanopids seem derived with respect to other synapsids suddenly seem plesiomorphic.

• Narrow lower temporal (zygomatic) arch
• Loss of double-canine teeth

While others including:

• Absence of supratemporal fenestrae

Become apomorphic.

But wait! Benoit et al., 2021 dispute Ford and Benson, 2018, noting that the anatomy of the maxillary canal for the maxillary branch of the trigeminal nerve in Orovenator strongly resembles that of the well-established sauropsid Prolacerta whereas those of varanopids resemble other synapsids. They do not provide a phylogenetic analysis. For GEOL431, we stick with tradition for now and regard varanopids as synapsids, but await future news with interest.

Neoreptilia

(Early Permian - recent) The last common ancestor of Parareptilia and Sauria and all of its descendants. Depending on where you place turtles, this could also be the diapsid crown-group.

Synapomorphies:

• Lacrimal excluded from margin of naris
• Caniniform teeth (synapomorphy of Amniota) are lost

Parareptilia

(Early Permian - Late Triassic) This group has historically included reptilian-grade organisms closer to Eureptilia that did not have living members. The arrival of phylogenetic systematics allowed it to be phylogenetically defined as monophyletic, however its precise membership has been fuzzy because of uncertainties about the position of turtles. Here we address the definite monophyletic core of this historical group.

Synapomorphies:

• A median embayment on the posterior margin of the skull roof (in dorsal view.)
• Absence of a subtemporal process of the jugal.
• Absence of a supraglenoid foramen (typically between quadrate and quadratojugal in other aimals.)

Parareptilian diversity. Great diversity during the Late Paleozoic and earliest Mesozoic.

Mesosauridae: (Early Permian) Mesosaurus, Braziliosaurus, and Stereosternum. Inhabiting the incipient basin of the South Atlantic, their fossils are from southern South America and Africa. Mesosaur distribution was among the data of Alfred Wegener supporting continental motion. The first amniotes with clear adaptations to aquatic life. Known from many well-preserved specimens, yet phylogenetically enigmatic. Characteristics:

• Broad, paddle-shaped limbs adapted for swimming.
• Blade of scapula shortened, as often seen in secondarily aquatic tetrapods
• Ribs pachyostotic thickened with dense bone tissue acting as ballast
• A "snout-hunter" - Elongate rostrum with long slender teeth for capturing prey with rapid sideways motion of head. (Living analogs include: gars, gavials).
• Viviparity: Piñeiro et al., 2012b report the presence of late stage embryos in the abdominal cavities of mesosaurs. Viviparity is a common adaptation to marine life in amniotes.

Mesosaur issues:

• For a century, the presence or absence of an infratemporal fenestra has been debated. Piñeiro et al., 2012 seems to have resolved this in favor of its being present. Whether this autapomorphic or characteristic of a larger group (possibly even Amniota) depends on the resolution of...
• The phylogenetic position of mesosaurs, which have been regarded as:
  • Basal members of Parareptilia (Gauthier et al., 1988)
  • Stem sauropsids (Laurin and Reisz, 1995)
  • Stem amniotes (Hill, 2005)
  However the weight of recent opinion (E.G. Tsuji et al., 2012) favors the basal parareptile position, in which case...

Millerettidae: (Permian) Small (20 - 40 cm.) probably ecological generalists with simple peg-like teeth. Synapomorphies:

• Embayment of squamosal and quadratojugal forms recess for tympanum
• Small infratemporal fenestra frequently present between postorbital, squamorsl, and jugal. (Presumed convergent with those of synapsids and diapsids.)

Lanthanosuchoidea: (Early - Late Permian) Small (20 - 40 cm.) probably ecological generalists with simple peg-like teeth. Contains:

• Lanthanosuchidae: with flat, heavily sculpted skulls. (E.G. Lanthanosuchus right.)
• Acleistorhinidae: with short deep skulls (right). Acleistorhinus, itself, is the oldest known parareptile.

Synapomorphies:

• Elongate basipterygoid process
• Small but distinct infratemporal fenestra low on the cheek, enclosed by jugal, squamosal, and quadratojugal. (Again presumed convergent.)

Bolosauridae: (Early - Middle Permian) Small (20 - 40 cm.) probably ecological generalists to herbivores with complex teeth. Although bolosaurids had been known through the 20th century, it was Berman et. al, 2000 who demonstrated their parareptilian nature phylogenetically. Synapomorphies:

• Teeth with cusps and ridges
• Extremely tall coronoid process

Bolosauridae contains the earliest known facultative biped - Eudibamus cursorius. Eudibamus was redescribed by Berman et al., 2021 as actually being capable of moving its limbs in an upright "parasagittal" digitigrade posture, a definite first for the Early Permian.

Procolophonoidea: (Late Permian - Late Triassic) Small (20 - 40 cm.) probably ecological generalists to herbivores with bulbous blunt teeth. Typically stocky with short tails, Many members sport cranial ornamentation and armor of dermal scutes. Contains:

• Owenettidae: (Late Permian). Link to Owenetta
• Procolophonidae: (Late Permian - Late Triassic).

Synapomorphies:

• Naris circular or dorsoventrally expanded
• Maxillary depression present (cheeks?)
• Three - four premaxillary teeth
• Maxillary teeth with transversely expanded bases
• Ten - twelve maxillary teeth

In addition, procolophonoids tend to expand the orbit posteriorly into the temporal region, however in contrast to many more basal parareptiles, there is no temporal fenestration. In most, the cheeks are broadly flaring.

Nycteroleteridae: (Middle Permian - Late Permian) Small (20 - 40 cm.) Mostly known from skulls, however Emeroleter shows a large skull on a relatively gracile bodies and limbs. These include the parareptiles with the most extensive embayments of the posterior cheek margin and small slender stapes - strongly indicative of impedance-matching ears. Their phylogeny is poorly resolved but Tsuji et al. 2012 find Macroleter to be the most basal. Synapomorphies:

• distinct emargination at the posterolateral edge of the skull concave
• smooth depression in the temporal region extending across most of the squamosal and large parts of the quadratojugal
• remaining area of the temporal region is characterized by distinctive dermal sculpturing
• a well developed, laterally protruding rim at its dorsal margin of the otic notch formed by the overhanging supratemporal and postorbital.

Pareiasauria: (Late Permian). Medium - big, squat, ugly, bumpy. These were major herbivores in the Late Permian world. They competed ecologically with therapsid dicynodonts, and were hunted by therapsid gorgonopsians. Indeed, to judge from paleo-art, provisioning gorgonopsians was their only task.

General trends:

• Proportions: Medium to large herbivorous reptiles. Short, deep and wide bodies, presumably with large digestive systems. Probably similar ecologically and metabolically to living giant tortoises.
• Skull: Short and wide, characterized by flaring armored cheeks, bumps and horns. E.G.: Bunostegos. There is no temporal fenestration or anything analogous to it.
• Teeth: Teeth are phyllodont, similar to those of large herbivorous iguanas.
• Armor: Pareiasaurs have extensive dermal armor. In some, the armor is interlocking.

Thus, everything points to these creatures having been large, slow moving armored herbivores with extensive digestive systems.

Synapomorphies:

• A ventral flange of the quadratojugal
• A posterior extension of the squamosal that covers the area occupied by the quadrate emargination in other parareptiles.
• A large boss on the supratemporal
• A large ventral process on the angular.

Neodiapsida: (Early Permian - Quaternary) First coined in the 1980s to encompass diapsids closer to Sauria than to Araeoscelidia, its definition has been contentious. The last word belongs to Ford and Benson, 2019, who apply it to the sister taxon of Parareptilia. In Neodiapsida, the diapsid morphotype and fenestration pattern stabilizes around something like the traditional concept of a "diapsid."

Synapomorphies:

• Lacrimal tapers anteriorly and excluded from Paris by contact of maxilla and nasal.
• Infratemporal fenestra approaches or confluent with cheek margin ventrally.
• Posterior coracoid lost.

Lanthanolania reflects these trend by:

• Excluding the lacrimal from the naris altogether.
• Reducing the posterior process of the jugal, opening the question of whether the lower temporal bar might be breached by the infratemporal fenestra.

Note: The posterior skull elements in the reconstruction are entirely speculative!

Drepanosauromorpha: (Late Triassic) Odd arborealists - convergent on certain saurians, but lacking key saurian synapomorphies like evidence for an impedance-matching ear:

• Megalancosaurus (Late Triassic - right) Link to reconstruction. With:
  • prehensile tail
  • opposable digits on manus and pes
  • long neck
  • barrel chested with ribs fused to vertebrae
  • thoracic vertebrae fused into notarium
  • pointed snout
• Drepanosaurus (Late Triassic) Link to description. Like a large, headless Megalancosaurus, but with strangely developed forelimbs.
• Avicranium (Late Triassic) The best known drepanosaurid cranium, described by Pritchard and Nesbitt, 2017 reveals that for all its outward similarity to a bird's, it's skull lacked saurian features like an embayment for a tympanum.

The oversized ungual phalanges of some drepanosaurids (e.g. Drepanosaurus) has invited speculation about their function. Jenkins et al., 2020 determined that larger unguals closely resemble those of "hook-and-pull" diggers like the living tamandua and silky anteater - creatures that combine arboreality with the ability to dig into ant and termite nests.

Wiegeltisauridae: (Late Permian - Early Triassic) The first gliders, employing a patagium supported by dermal elements of the trunk. Also the earliest obligate amniote arborealists.

• Coelurosauravus (Late Permian)Ornate triangular head with "casque" resulting from enlargement of the infratemporal fenestra. Most recently redescribed by Buffa et al., 2021.

  A gliding membrane supported on elongate dermal "palatial" elements that are not ribs (in contrast to the extant gliding squamate Draco Volans.) Buffa et al., 2022 propose that these could be elongate versions of lateral gastralia, as they appear to be continuous with the gastralia and originate low on the trunk. They also note that, like Draco, Coelurosauravus could have grabbed the leading edge of of its patagium with its manus to stabilize it.

• Possibly related, Longisquama (Middle-Late Triassic) Triangular head and elongate plume-like display (?) structures.

Claudiosaurus: The lower temporal bar is definitely incomplete in Claudiosaurus (right). In life, its place would be occupied by an unossified ligament. Various diapsids would eventually reossify that ligament in various ways, but from this point forward, we deal with diapsids who are descended from creatures whose infratemporal fenestrae have been transformed to broad embayments in the lower margin of their cheeks.

Claudiosaurus was a limb-propelled swimmer with a relatively long neck. When first described it was called a "plesiosaur ancestor." That's probably wrong, but it demonstrates that even in the Permian, diapsids displayed a tendency opportunistically to evolve aquatic forms. Claudiosaurus was fresh-water aquatic, however, not marine.

"Younginiformes:" (Late Permian) Our first relatively complete stem-neodiapsid belong to this probably paraphyletic group. Members of this grade contain the last diapsids to retain a fully-enclosed infratemporal fenestra, such as Youngina (right). Youngina was terrestral. Others, such as Hovasaurus were fresh-water aquatic.

Note: It's not clear that all members of this grade had complete lower temporal cheek bars.

Potential synapomorphy of Younginiformes:

• The postorbital posterior process extends past the end of the supratemporal fenestra.

Potential synapomorphies of "younginiformes" and Sauria:

• The postfrontal forms part of the anterior margin of the supratemporal fenestra.
• The femur is sigmoid in shape. (Link to comparison.)

Phylogeny: The more derived stem saurians display considerable convergence on other forms, leading to a diverse range of phylogeny hypotheses. Some highlights:

• Senter, 2004 found drepanosaurids and wiegeltisaurids to form a monophyletic group that he called Avicephala.
• More recently, Renesto et al. 2010 found Avicephala to be polyphyletic, with the drepanosaurids as members of sauria.
• With the benefit of Avicranium, Pritchard and Nesbitt, 2017 recovered the pattern we cite here.

Sauria:

(Late Permian - Rec.) The most recent common ancestor of living lizards, Sphenodon, crocodylians, and birds.

Here, for once, in a pleasing cladogram is the arrangement of Gauthier, 1984, in which two crown-groups were recognized in Sauria:

• Archosauria: The most recent common ancestor of crocodylians and birds and all descendants.
• Lepidosauria: The most recent common ancestor of squamates and Sphenodon and all descendants.

Anchored on these, he defined total-groups that contained them:

• Archosauromorpha: All organisms more closely related to archosaurs than to lepidosaurs.
• Lepidosauromorpha: All organisms more closely related to lepidosaurs than to archosaurs.

This setup was embraced so firmly that even though there were technical difficulties with his definition of Lepidosauromorpha, (ask me sometime) most systematists continue to use the term, and so shall we.

Synapomorphies:

• Of the skull:
  • Prominent retroarticular projection of jaw: An extension to the jaw that projects behind the jaw joint.
  • Quadrate is embayed posteriorly:
  • The stapes is slender: These three features together strongly suggest the convergent evolution of an impedance-matching ear.
  • The adductor muscles of the jaw originate on the dorsal surface of the skull table.
  • The paroccipital process of the opisthotic firmly sutured to the skull roof.
• Of the appendicular skeleton:
  • The cleithrum is lost.
  • The fifth distal tarsal is lost.
  • The fifth metatarsal is hooked.

Stay tuned.