What a morphometrical link between the eye and ear sizes in ancient and modern dolphins could mean for the world of evolution.
MIQUÉLA THORNTON
May 9, 2022
AT A GLANCE
The lineage of cetaceans has evolved massively over time, and as its legs were replaced with flippers as it transitioned from land to sea, the semicircular canal (a vestibular inner ear structure concerned with balance, head movements, and gaze stabilization) shrunk drastically. Since, cetaceans, the dolphin in particular, is an outlier in general rules concerning semicircular canal size in relation to body size.
Broad questions remain as to why the semicircular canal shrunk, as well as why this creature moved from land to sea. However, CT scans have opened doors in digital paleontology allowing researchers to nondestructively study parts of anatomy, particularly the vestibular system, previously inaccessible.
Prior research has shown associations between canal shape and semicircular canal size in relation to large eyes and visual acuity. This is put in the context of the animals agility and ability to stabilize gaze after spontaneous head movements, a context necessary because of dolphins’ evolved short necks. Understanding this relationship in cetaceans, specifically dolphins, would allow for strides in understanding dolphin perception.
One avenue of further study in perception is cross-modal research between senses. Advanced study on the interactions between audition and vision is paramount in conservation efforts concerning human interactions such as ocean noise pollution, that affect marine mammal sensory abilities.
THE BEGINNING
In reconstructing the Tethys Sea, an ancient tropical body of water that existed from the end of the Paleozoic Era until the Cenozoic, a paleontologist would find that it was the home of diverse flora and fauna, reefs constructed by rudist bivalves, or ancient mollusks, and numerous volcanic activity, both underwater and above the surface. Lying in what is now Pakistan and its surrounding regions, they would also find that it was home to the Pakicetus species, a sparsely-haired, hippopotamus-like ancestor of modern whales and dolphins that roamed the deep sea 49 million years ago. It had a long snout, sharp canines, and molars, a distinct, long flexible neck perfect, and was likely tailed. It also, unlike the marine mammals that roam our oceans and rivers today and unlike the majority of other cetacean fossils, had four fully-functional legs. It also likely had webbed feet as indicated by fossilized toe bones. However, how exactly this creature went from being a land-dweller to a legged-cetacean to modern dolphins, whales, and porpoises, might not lie in the feet or flippers. Instead, it may lie deep in the inner ear, specifically the semicircular canal.
INTO DEEP TIME
The Pakicetus species resembles a rather awkward transition phase between its terrestrial ancestors to a fully-aquatic species. It eventually evolved from the paddle-legged Ambulocetus species to the slender-jawed Protocetus species into the Basilosaurus species, the largest known advanced Archaeocete, a paraphyletic group of even-toed cetaceans. Unlike its predecessors, who led amphibious lifestyles, the Basilosaurus was the closest resemblance to modern cetaceans because it was fully aquatic. It arrived between 38 and 45 million years ago, approximately 4-5 million years ago after the Pakicetus species, during a time known as the Eocene Epoch. For context, the mass extinction event occurring at the Cretaceous–Paleogene (K–Pg) boundary that decimated the dinosaurs occurred 66 million years ago, marking the beginning of the Paleogene Period. We, the awkward transition species of the cetacean, are in the middle of this period, approximately 20 million years later. A lot has happened since the asteroid hit.
The Basilosaurus no longer had the long, voluminous legs of the Pakicetus or the short paddled legs of the Ambulocetus. It traded those for elongated flippers, perfect for navigating its full-time undersea lifestyle. It was complete with fused phalanges to prevent curling joints, and an enlarged sinus at the base of the skull that would eventually develop into structures necessary for deadly whale teeth. Most notably, its hind limbs were completely gone. While the Basilosaurus does not have any direct modern descendants, as shown through analyses of its skull, the family birthing whales and dolphins likely diverged from this lineage and underwent many evolutionary events since. 35 million years ago marks when baleen whales and toothed whales diverged from their common ancestor. 11 million years ago marks when the family Delphinidae diverged. And only 2-5 million years ago marks when the modern bottlenose dolphin appeared. Over the course of this evolution, not only did legs slowly disappear, but these lineages underwent many other evolutionary changes; one being, the size, and shape of its inner ear.
X-ray computed tomography or CT scans have changed the way paleontologists can study fossils and the way evolutionary biologists can compare those fossils to animals today. Researchers in this field use Micro-CT (written µCT) to create images by assembling monochromatic slices. Using CT scans not only allows scientists to explore fragile fossils they would have otherwise been unable to use, but it allowed them to nondestructively look at protected species like modern cetaceans, who in many cases are protected due to threatened statuses. “It has revolutionized the information that you can get from specimens,” said Annalisa Berta, paleontologist and professor emerita in the Department of Biology at San Diego State University. “Just for brain studies, it used to be that you had to find an endocast preserved somehow. And they are preserved. The inside of the brain is preserved in some situations, but because you can actually digitally look at the brain using scanning techniques you can reconstruct it without the 3D value of the brain without having to have a natural endocast in your hand,” she said. Among the doors CT scanning has opened, in recent years, CT scans have been paramount in looking at the minute bones that make up the inner ear.
DEEP INTO THE EAR
As ancient cetaceans morphed away their legs, their evolution also reshaped their inner ears and shrunk their semicircular canals, an organ essential for balance.
The semicircular canal sits in the labyrinth of the human inner ear and other vertebrates. It is made up of three canals that loop above the cochlea一the structure responsible for hearing in most mammals一like the crown of a conch shell. They are arranged at opposing right angles so that each can sense the head’s movement on three different axes and orient you, the human, in a three-dimensional space. This exemplifies why they are so essential for balance and coordination, as well as gaze stabilization. The canals are bony tubes filled with fluid called endolymph that slosh around inside of them like calm waves. The canals are lined with microscopic strands of hair called stereocilia that sway like water plants on an ocean’s reef. Your ears sense motion by detecting the ways in which these hairs move. These tubes are what allow humans and other animals to feel dizziness because the semicircular canal responds to head rotations. Specifically, dizziness occurs in mammals when inertia causes endolymph to be sloshed in a different direction from head movement. Because of the associations between semicircular canal size and agility, paleontologists have been able to infer that the larger the semicircular canal in an extinct animal, the more agile. The smaller, however, the more… well, dizzy.
The vestibular complex of modern cetaceans has long been perceived as abnormally smaller than expected in relation to the cochlea, the structure in the ear largely responsible for hearing in most mammals, as first identified in Andrea Comparettie’s Observationes anatomicae de aure interna comparata in 1789. Relative to body size, their semicircular canals are roughly three times smaller than the average terrestrial mammal, as found by one of the first studies investigating the cetacean inner ear using CT scans. While these animals rank in the highest percentile of hearing in the animal kingdom, their inner ear is largely irresponsible for that. Unlike humans, whose hearing largely depends on the inner ear, dolphins only employ their ear openings when above water. While underwater, these creatures employ their lower jawbone to conduct sound to their middle ear, as well as to echolocate.
In 2001, researchers Fred Spoor of University College London, Hans Thewissen of the Northeastern Ohio Universities College of Medicine, and their collaborators used x-ray tomography (CT scans) to reconstruct the inner ears in the skulls of four ancient cetaceans. In comparing these reconstructions to those of modern cetaceans, they found that extant cetaceans evolved to have small semicircular canals about 5 million years before the first whales swam the oceans. Both prior and modern research associates large semicircular canals with agility, with birds, for example, having the longest canals because of the fine balance necessary for aerial flight.
The smaller semicircular canals, they postulate, allowed ancient cetaceans to perform acrobatic swimming, by reducing sensitivity to locomotion. It also made it so they wouldn’t experience vertigo, or dizziness underwater. This dizziness, however, would have been experienced on land with canals of their size. To quote the authors, once the canals evolved to be smaller, cetaceans would have been "incompatible with terrestrial competence.” Instead, as they explain, the smaller canal size allowed cetaceans to extend the performance range of their vestibular system. No longer having the long necks of their ancestors, this system would have allowed fully-aquatic cetaceans to move their heads in much larger scopes, than those which larger, more sensitive vestibular systems. This allowed the researchers to conclude that the shrinkage of the semicircular canal was a “key point of no return” event in early cetacean evolution, leading to full independence from life on land.” However, it leaves much unexplained. That was 2002. Spoor’s and Thewissen’s theory that the semicircular canal shrunk to reduce sensitivity in the deep ocean is only one possible explanation.
The postcranial skeleton, including all bones and cartilages caudal to the skull, continued to develop over time, past the reduction of the inner ear. More gradual than the geologic time it took to shrink the canals, the rest of the body continued to morph for approximately eight million years after the ‘point of no return.’
This led subsequent researchers to wonder what other explanations there may be for small cetacean vestibular systems. In looking at the possible correlations between canal size and head movements in modern animals, researchers Benjamin Kandel and Timothy Hullar compared the head movements of dolphins and cattle, considering that cetaceans were once a two-toed terrestrial species. They found that the dolphin’s head movements were only slightly less vigorous than the cattle, allowing them to conclude that the small canal size may not be attributed to head movement range as Spoor and Thewissen hypothesized.
In looking at the small vestibular region in the context of a broad mammalian evolutionary framework, researcher Eric Ekdale of San Diego State University theorizes this is a synapomorphy of the group, meaning that it may be a novel trait evolved from the most recent common ancestor. However, the results of both of these studies leave the door open as to why these small canals evolved specifically in cetaceans. Since the establishment that this system evolved among mammals, cetaceans are often excluded from broader analyses of mammalian vestibular systems. Nevertheless, “whether aspects of cetacean behavior or physiology can be inferred from the vestibular region is debated,” in modern study according to evolutionary biologist and paleontologist Rachel Racicot in her recent article detailing the evolution of whale sensory ecology. In the article, Racicot anthologizes the frontiers in nondestructive anatomical investigations, leaving the reader with questions for future study in the field. In specifically focusing on the unsolved mysteries of semicircular canal shrinkage, Racicot poses the question of visual acuity and its possible impact on cetacean vestibular anatomy. When the head moves, the gaze must stabilize. In keeping in line with the theory that semicircular canal shrinkage may not be to accommodate head movement, further inquiry questions if it instead has to do the gaze that stabilizes when those head movements occur. Because of the association, the semicircular canal has with gaze stabilization, Racicot wonders what the relationship between eyes and ears has to say on the mystery of why cetaceans evolved such small inner ear canals.
DEEP GAZING
If there is a relationship between eye size and semicircular canal morphometrics, “it would tell us something radically new about dolphin sensory systems and open up new avenues of looking at their evolution,” Dr. Racicot says. It could change the marine mammal world.
According to the International Union for Conservation of Nature and Natural Resources Red List of Threatened Species, out of 41 species of dolphins, five species and six subspecies are considered endangered. Exploring possible correlations between eye and ear size would allow further understanding of their sensory system and further inquiry into how dolphins perceive the world: necessary research to conserve their species.
In 2014, researchers Addison Kemp and Christopher Kirk of the University of Texas at Austin published an article in The Anatomical Record exploring the relationship between eye size and vestibular anatomy in mammals.
In order to maintain visual fixation, semicircular canals detect head rotations and trigger movements to stabilize the gaze. Prior research shows that mammals with large eyes and high visual acuity require very precise mechanisms to stabilize their gaze. As outlined by Racicot, semicircular canal arc radii measurements are often used by researchers because they show a relationship between the canal length and agility and activity behaviors in mammals, while factoring in body size. This was found by Spoor et. al in a 2007 study on primate semicircular canal system and locomotion. Specifically, Spoor and his colleagues found that large canal arc radii are often associated with higher agility, while smaller canal arc radii are often related to slower movement due to the sensitivity large canals have to fluid movement inside of them. As previously discussed, this fluid movement triggers signals released by the hairs in the canal. Smaller canals are less sensitive to this movement, thus equating them with smaller ranges in agility.
In the present Kemp and Kirk study, they utilized the arc radii curvature of the semicircular canal and compared it to visual acuity in a large sample of mammals. This sample broadly ranged across the animal kingdom, including a variety of species from hoofed animals, to possums, to primates, to rodents, to carnivorans, to sea cows. In total, the sample used data from 104 species of 16 mammalian orders. However, due to the reason aforementioned, cetaceans were not included.
As found by previous studies, uncompensated head movement prevent visual acuity in mammals and impairs visual functionality. This problem is solved by stabilizing the image. Mammals like us do this by producing eye movements to compensate for movement. However, according to Kemp and Kirk, uncompensated head movements are more problematic for mammals with larger eyes or visual acuity. This has to do with the retinal ganglion cell receptive field, the area of the retina where stimulation with which alters the ganglion cell firing rate, the mechanism through which the eye communicates with the brain in order to fulfill visual functions. Species with highly adapted visual acuity, tend to have smaller retinal ganglion cell receptive fields, making it so they require more precise gaze stabilization. In comparing the relationship between eye size, visual acuity, and gaze stabilization using quantitative data, the researchers confirm a positive correlation between the mean semicircular canal radius of curvature in species (SCR) and both eye size and visual acuity. This aligned with the authors’ hypothesis. They suspect that the evolution of larger eyes and higher visual acuity lead to a selection for larger semicircular canals. In the paper, the researchers write that they hope their results will help explain the observed variation in semicircular canal sizes and shapes in both fossilized and living mammals.
While the evolutionary cause for the shrinkage of semicircular canals in cetaceans remains uncertain, exploring possible correlations between semicircular canal size and visual acuity could not only explain these variations in living and fossilized cetaceans as they can for other mammals, but it could answer specific questions regarding intraspecific variation and cetacean perception today. “There’s a lot of species to look at. In order to really be able to understand the evolution within the group, you have to really know what kind of variation there is in the modern sample,” said Annalisa Berta. “The present is the key to the past. If we study modern species we can find out how these characters evolved through time and how they changed and how they’ve transformed.”
DEEP BEYOND
The word Merkwelt describes a creature’s capacity to view things, manipulate that information, and use it to make meaning out of the universe. This is a crucial part of Umwelt, the biological foundations that lie at the heart of the way in which a creature experiences the universe. This is a theory proposed by pioneering researchers, Jakob von Uexküll and Thomas A. Sebeok. In a 2016 review article published in Frontiers in Ecology and Evolution, a plethora of leading researchers in the field encapsulated current knowledge about dolphin senses. In understanding dolphin’s Merkwelt, their sensory world, researchers, as the authors argue, must explore their cross-modal perception, or rather, how their senses interact with each other. To quote the article, “Probably the best-studied example of cross-modal perception in dolphins concerns their ability to link auditory and visual cues.” For example, using echolocation, dolphins can visually recognize objects picked up through an auditory function and vice-versa.
However, recent research largely centers interactions between vision and audition on movement and object recognition. In investigating other contexts (as well as other senses), researchers would learn so much more about how modern dolphins take in the world. The researchers outline a number of possibilities. Notably, studying the cross-modal relation between audition and vision can allow us to work towards understanding
Conspecific recognition: How dolphins recognize each other between auditory cues such as signature whistles and visual cues such as distinctive physical features.
Communication: How dolphins communicate between audition (such as jaw claps, tail hits, or “squawks”) and vision (such as body postures), calling and responding utilizing combinations of both senses.
Additionally, the researchers outline further areas of cross-modal study between other senses such as the authority trait of returning echo in combination with electroreception, chemoreception, and somatosensory perception. This study is encouraged to better understand prey location and food evaluation.
Understanding the interactions between vision and auditory perception on a deeper level would allow researchers to better understand how human-caused issues affect their perception and development says Rachael Racicot, one of these issues being the effects of ship noise on marine mammals.
Searching for the link between eyes and ears in cetaceans, specifically dolphins, has large possibilities for understanding its evolutionary framework and the age-old question of why this linage of species moved from land to sea and from terrestrial to amphibious to fully-aquatic lifestyles. It could be the key to unlocking the mysteries regarding the semicircular canal and its shrinkage throughout evolution. Further, links between canal size and shape and eye size/acuity could open the door to a better understanding of interactions between dolphin vision and audition as a whole, giving researchers a peephole into the animals’ perception and what their sensory worlds look like. Looking into their world through their eyes and ears could tell use fundamental information necessary on how to best conserve them.