Inner ear sensory system changes as extinct crocodylomorphs transitioned from land to water

Abstract

Major evolutionary transitions, in which animals develop new body plans and adapt to dramatically new habitats and lifestyles, have punctuated the history of life. The origin of cetaceans from land-living mammals is among the most famous of these events. Much earlier, during the Mesozoic Era, many reptile groups also moved from land to water, but these transitions are more poorly understood. We use computed tomography to study changes in the inner ear vestibular system, involved in sensing balance and equilibrium, as one of these groups, extinct crocodile relatives called thalattosuchians, transitioned from terrestrial ancestors into pelagic (open ocean) swimmers. We find that the morphology of the vestibular system corresponds to habitat, with pelagic thalattosuchians exhibiting a more compact labyrinth with wider semicircular canal diameters and an enlarged vestibule, reminiscent of modified and miniaturized labyrinths of other marine reptiles and cetaceans. Pelagic thalattosuchians with modified inner ears were the culmination of an evolutionary trend with a long semiaquatic phase, and their pelagic vestibular systems appeared after the first changes to the postcranial skeleton that enhanced their ability to swim. This is strikingly different from cetaceans, which miniaturized their labyrinths soon after entering the water, without a prolonged semiaquatic stage. Thus, thalattosuchians and cetaceans became secondarily aquatic in different ways and at different paces, showing that there are different routes for the same type of transition.

Keywords: CT scanning; bony labyrinth; morphology; thalattosuchia; vestibular system.

Fig. 1.

Left bony labyrinth of the extinct thalattosuchian crocodylomorph Pelagosaurus typus (NHMUK PV OR 32599) based on CT data; (A) lateral view of the skull. (B) Transparent skull showing the position of the endosseous (bony) labyrinth; (C) lateral view; (D) medial view; (E) posterior view; (F) anterior view; and (G) dorsal view of the bony labyrinth. Abbreviations: asc, anterior semicircular canal; cc, crus commune; cd, cochlear duct; col, columella; lsc, lateral semicircular canal; psc, posterior semicircular canal; ve, vestibule. (Scale bars equal 1 cm.)

Fig. 2.

Simplified time-scaled phylogeny showing right bony labyrinth shapes of key extinct and extant crocodylomorphs of different habitats. Labyrinths are not to scale.

Fig. 3.

Bony labyrinth shape morphospaces, showing the distribution of extinct and extant crocodylomorphs of different habitats, based on principal component analysis of 3D landmarks. (A) PC1 vs. PC2; (B) PC1 vs. PC3. Labyrinth outline diagrams correspond to morphological extremes at the ends of PC axes, in lateral and dorsal views. For taxa abbreviations see SI Appendix, Table S1.

Fig. 4.

Bony labyrinth shape morphospace, showing the distribution of extinct and extant crocodylomorphs of different habitats, based on canonical variate analysis of PC scores (Fig. 3), with mean labyrinth shapes for each habitat group, in lateral (Top) and dorsal (Bottom) views.

Fig. 5.

Pelagic adaptions plotted on a time-scaled crocodylomorph phylogeny. PC1 scores of labyrinth shape, which are correlated with habitat (Figs. 3 and 4), are optimized on the phylogeny to predict ancestral states for the major clades, demonstrating a trend of increasing PC1 scores (increasingly pelagic-shaped ears) in thalattosuchians. Key cranial and postcranial features related to aquatic lifestyles are listed next to the nodes at which they appeared, based on optimizations (43). This demonstrates that thalattosuchians first developed features permitting aquatic locomotion before they developed a modified pelagic labyrinth morphology.