GEOL 431 Vertebrate Paleobiology

Spring Semester 2015

Squamate superlatives: mosasaurs and snakes

Mosasauroidea: (Cretaceous)

Mosasaurs, a particularly spectacular scleroglossan group, appeared and thrived in the second half of Cretaceous, but were extinguished by K-T extinction. During that interval, they ranked among the oceans' dominant predators. Mosasaurus was the first fossil reptile to be studied scientifically by Georges Cuvier, who identified it as a lizard.

A look at the quadrate of Tylosaurus (right) clearly shows the apomorphic squamate quadrate. Other interesting mosasaurian features include:

• Transformation of the limbs into flippers
• Elongation of the snout
• Retraction of the nares
• Development of a distinct hinge joint at the mid-length of the jaw.
• Organization of the palatal teeth into a single stout row.

Despite this long history of study, mosasaurs continue to surprise us. E.G. the mosasaur tail has always been reconstructed as laterally flattened but similar to other lizard tails. Lundgren et al. 2013 demonstrated that the mosasaur Prognathodon, at least, had a full-blown tail fin. Could other mosasaurs have been that different?

All agree that mosasaurs are monophyletic and derived from "Aigialosaurs," a paraphyletic group of semi-aquatic medium-sized scleroglossans. Their close relatives are Dolichosauridae, containing medium-sized marine scleroglossans with long necks.

Serpentes:

(Late Jurassic - Rec.) The most subtle of beasts.

Rather than giving a synapomorphy list, we will note major evolutionary trends:

• Limbs reduced or absent.
• Lidless eyes protected by a transparent scale.
• A unique pattern of rods and cones in the retina resulting in a reduction of color vision (typically well-developed in sauropsids.)
• External ear opening lost.
• The temporal region is long in comparison to the snout (a condition found in other "head hunters" like aistopods.)
• Braincase reinforced anteriorly by laterosphenoid ossification.
  
• Bones of the dermal skull roof and braincase fuse into a solid cylindrical unit.
• The quadrates, palate bones, maxillae and premaxillae become very loose and mobile, allowing manipulation and swallowing of large food items.
• The supratemporal, the skull bone to which the quadrate attaches, also becomes mobile with respect to the braincase.
• The teeth of the palate are organized into a pair of rows.
• The jaws are jointed at their mid-length and flexible, and in most cases, the two sides do not connect in front, allowing swallowing of even larger objects.

The comparison of the skulls of the Nile monitor lizard and reticulated python (a snake showing a relatively ancestral serpentine morphotype) underscore these differences.

These trends are even more pronounced in derived snakes like vipers.

The ancestral condition of snakes: Two hypotheses have been proposed, both of which address snakes odd sensory systems:

• The aquatic hypothesis: The ancestral snake's visual system was modified for the lower lighting underwater. Loss of the tympanum reflects lack of need for impedance-matching ear underwater.
• The fossorial (burrowing) hypothesis: The ancestral snake's visual system was reduced in an ancestor that mostly lived underground and had little to see. Reduction of tympanum reflects advantage, underground, of picking up vibrations with jaw.

Systematists are drawn into this debate because the discovery that the sister taxon of Serpentes was either aquatic or fossorial would lend weigh heavily in the dispute.

Basal snakes: Proponents of the fossorial hypothesis derive comfort from the cladogram of living snakes.

• The basal branches of the snake tree, including Leptotyphlops, the blind snake and Cylindrophis, the pipe-snake are definitely fossorial.
• Although their skulls definitely display the derived features of snakes, they definitely lack the extreme modification of more derived snakes. (See Cylindrophis)
• These snakes lack the large flexible jaws and jaw-articulations characteristic of the "big-mouthed" macrostomatan snakes.

Note: both of these groups are ancestral enough that they lack the broad belly scales that we typically associate with snakes.

Amphisbaenians and skinks, also with fossorial adaptations, have both been proposed as sister taxa of snakes.

Pythonomorpha hypothesis: But since the 19th century mosasaurs, and their close relatives the dolichosaurs, have been proposed as sister taxa of snakes based on the morphology of their palate and jaws. Similarities include:

• A single row of stout palatal teeth
• Mobile joint at the mid-lenght of the jaw.
• Reduction of limbs and limb girdles.

A sister taxon relationship between snakes and mosasaurs was first hypothesized by Cope, 1869, who coined the group name Pythonomorpha, and proposed that they belonged to Anguimorpha.

Renewed debate: In the 1990s, gasoline was thrown onto the issue of snake origins and relationships by a volley of descriptions or redescriptions of primitive snakes from the Cretaceous, including Pachyrachus problematicus (Lee and Caldwell, 1997), Haasiophis terrasanctus, and Eupodophis descouensis. Stimulating because:

• they were definitely marine
• they retained small but functional hindlimbs.

At first glance, a snake with legs ought to be a basal primitive snake, and a marine basal primitive snake ought to cinch the marine ecology of the ancestral snake, and support the pythonomorph hypothesis. But not so fast.

Their skulls proved to have the derived characters of macrostomatan snakes. Thus, despite the presence of legs, most cladistic analyses continue to place them well within the crown of living snakes. Apparently the presence of legs in them is a reversal. Strange! Of course, if they are derived snakes then they do not represent the ancestral condition.

More recently, Caldwell et al., 2015 have revealed leggy snakes from the Late Jurassic. These, in contrast, to Pachyrhachis, occupy a basal position in Serpentes.

The Krypteia Hypothesis:

Gauthier et al., 2012, attacked these an many other issues at once with an authoritative comprehensive phylogenetic analysis that assembled a large data set with substantial new character information. Their result included two surprising elements:

• Mosasaurs and dolichosaurs were banished to a position near the base of Scleroglossa.
• Serpentes emerged as the sister taxon to the fossorial dibamids and amphisbaenids in a "fossorial group" called Krypteia.

The fossorial hypothesis seems to have won the day, and yet as recently as Palci et al., 2013, publications in support of the marine hypothesis and mosasaurian relationship have continued to appear.

Why hasn't this issue gone away? Ongoing disagreement about the actual identity of the elements of the skull of the Cretaceous leggy snakes. Alternate hypotheses of the identity of bones that might be, for instance, the jugal (a dermal skull-roof bone) or the ectopterygoid (a dermal bone of the palate) greatly influence how characters in a taxon-character matrix are scored. With only a few changes in scoring, for instance, mosasaurs and dolichosaurs can be returned to the crown of the Scleroglossan tree and united with Serpentes.

A vivid example of this uncertainty concerns the identity of the presacral vertebral column. According to Palci et al., 2013, the anterior third of presacral vertebrae in Haasiophis display unfused intercentra. Intriguingly, unfused cervical intercentra are seen in other squamates. If the free intercentra of Haasiophis are homologous to these, it would imply that the front third of its "torso" is actually its neck (not easy to determine in a snake.)

The Toxicofera Hypothesis: When molecular methods are applied, things get interesting. Wiens et al., 2012 obtained a result in which Scleroglossa does not appear. Instead:

• Iguania joins Anguimorpha at the crown of the tree
• Their sister taxon is Serpentes. Together these form a clade called Toxicofera - the poison-bearing ones.
• Dibamids are the sister taxon of Gekkota. These form the basal branch of Squamata.

Reeder et al., 2015 have confirmed this result with an analysis that:

• Combines molecular and morphological characters
• Includes extant and fossil taxa

The result confirms Toxicofera and places Mosasauroidea as the sister taxon of Serpentes. Moreover, morphological synapomorphies are identified for Toxicofera.

Before we dismiss this radical idea, the Toxicofera hypothesis cleans up a loose end: Fossil iguanians don't appear until well after members of other major squamate groups, despite their basal position in morphological phylogenies. Placing them in the crown of the tree puts them in a stratigraphically congruent position.

Stay tuned.