LIFE SCIENCE

Scientists have revealed for the first time that the human middle ear was once the gills used by fish to breathe


The evolution of water spray holes from jawless gills to the middle ear of humans. (Courtesy of Gai Zhikun, painted by Shi Aijuan)

Gill silk marks were first found in the fossils of the early Devonian broad turtle in Qujing, Yunnan, revealing that our middle ear was once a gill used by fish to breathe (Photo by Gai Zhikun)

The four stages of the evolution of fish water jet holes into the human middle ear. A. True palm finfish and their water-jet hole sections; Axoruptera;C. Ichthyosaurus and its middle ear section; D. Reptile and its middle ear section; E. Mammals and their middle ear facet (A-E, from Gai et al. 2022, painted by Shi Aijuan)

At present, there is sufficient embryonic and fossil evidence to prove that our middle ear evolved from the water jet hole of the fish, and where does the water spray hole of the fish come from? This is a century-long problem that has plagued academia for a century.

Recently, Gai Zhikun, a researcher at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences, together with scientists from China, Britain and Sweden (Sweden), published the latest research results on the origin of vertebrate water spray holes in “Ecological and Evolutionary Frontiers” as the first author, revealing for the first time that the middle ear of humans was once a gill used by fish to breathe.

The human middle ear, which includes the tympanic membrane chamber, the three ossicles that conduct sound, and the Eustachian tube that leads to the mouth, is the secret of human beings having a sensitive sense of hearing. The water spray hole of the fish is located behind the eye, and between the jaw arch and the tongue arch is an incomplete gill fissure containing only false gills, which is a very important respiratory organ of the fish. In cartilaginous fish, the water jet hole is mainly used to inhale the water flow, which is the survival secret of benthic cartilaginous fish adapting to seafloor life, while in the primitive teleost fish, the water spray hole is mainly used to breathe air, which is an important reference for studying how early meat fin fish landed on land to breathe air and adapt to land life.

A century-old puzzle plaguing academia

As early as 1822, the French anatomist Saint Silan published his classic book “Philosophy of Anatomy”, which a priori proposed that similar organs of different phylatopods are likely to evolve from the same prototype. This is probably the earliest scientific conjecture in the history of science about the origin of fish jet holes. In 1872, the famous German anatomist Carl Gegenbaur was the first to propose a segmentation theory of the head of a vertebrate from the perspective of detailed anatomy (including gill arch, brain nerves, muscles, etc.), believing that the jaw arch and tongue arch of vertebrates are like the ordinary gill arch behind it, which is a series of homologous structures and is one of the subsections of the head.

In 1937, the British paleontologist Watson further proposed the “aphetohyoidean theory”, which held that the tongue arch supporting the jaw arch in the jaw class was not originally associated with the jaw arch, but a common gill arch, so there should be a complete, not degraded gill fissure between the jaw arch and the tongue arch, rather than a water spray hole, thus representing a primitive state of the early jawed class.

This view inspired twentieth-century paleontologists to search for such an undegraded gill fissure between the early jaw-like jaw arch and the tongue arch. After a century of searching, paleontologists in various countries have carefully examined the fossils of all shield fish, spiny fish, cartilaginous fish and teleost fish in the living jawless and early jawed species, and have not found any definite fossil evidence.

Fossil evidence from China

Since 2002, the research team has been working in the Field in the Changxing Silurian Strata of Zhejiang Province, and found one of the most primitive fossils of true armorfish here, which was later named Shuyu. These Aerobic fossils are precious specimens with three-dimensional cartilage brain preservation, and they are very small, only the size of our fingernails, which are very suitable for three-dimensional nondestructive scanning using synchrotron radiation X-ray microscopy technology, a large scientific device.

In 2006, the research team took a skull specimen of the akebono to a Swiss light source in Zurich, Switzerland, for nondestructive scanning.

After that, the three-dimensional reconstruction software was applied to the three-dimensional virtual restoration of the skull of the aquake, and a total of seven fossil skulls of the akebodis were completed in 5 years, and in the skull that was only the size of a fingernail, almost reproduced all the brain areas, sensory organs and nerves and blood vessels of the head of the akebodis.

Through an in-depth study of the three-dimensional virtual model of the skull of the aquamarine, the research team found that the so-called intergill ridge of the armor fish is actually the dorsal part of the gill arch, which is the same as the Swedish paleontologist Si Tianxiu’s 1927 speculation on the bone beetle, that is, the gill arch of the armor fish heals into a mainly protective head carapace, which is similar to the expansion and healing of the ribs of the turtle turtle into the turtle carapace.

Compared with bone beetles, the entire gill arch of the aeropus also maintains the original state of the entire vertebrate, so it is easy to identify the jaw arch and tongue arch from the topological position, its jaw arch is located just behind the orbital hole, forming the posterior orbital wall, and the armor turtle has only 7 pairs of pharyngeal arches, corresponding to the jaw arch, tongue arch and 5 pairs of gill arches with jaws.

At the same time, the Akebono cranial nerve has also been accurately restored, and the facial nerve is emitted from the back of the brain and leads along the anterior semicircular canal of the inner ear to the first gill sac after the eye. Thus, evidence of gill sac number, topology, morphology, and innervation points to the fact that one gill sac behind the turtle’s eye is the tongue-jaw sac located between the arch of the jaw and the arch of the tongue.

Judging from the morphology, the tongue and jaw sac are no different from the 5 gill sacs in the back, and the opening is on the ventral surface of the cephalic nail, not on the back of the cephalic carapace like a water spray hole, so it is basically judged that the tongue and jaw sac of the armor fish is still an undegraded gill sac. But to prove that it is a gill with normal respiratory function, the last link in the entire chain of evidence is missing, that is, to find fossil evidence of the presence of gill filaments in the gill sac.

To this end, the research team has carried out years of field excavations in the Early Devonian strata of Qujing, Yunnan. After the continuous and unremitting efforts of the research team, the new material of the first wide turtle with complete gill silk marks in the first gill sac behind the eye was finally collected for the first time in the dark gray siltstone of the Xishan Village Formation near the Qujing Miandian Reservoir, thus further proving that the first gill sac behind the armorfish’s eye is a gill with normal respiratory function, rather than a degenerate water spray hole, thus providing the most accurate anatomical evidence and fossil evidence for the origin of the water vent of vertebrates.

The Eustachian tube was once the main channel for fish to breathe

On this basis, the research team reviewed the evolution of the water spray hole from jawless to tetrapod, thus establishing the evolution sequence of the water spray hole from jawless gills to human middle ear.

This sequence shows that as the armor fish splits in pairs of nasal sacs, an unusually developed mid-back hole (single nostril) develops in front of the head to act as the main respiratory organ for inhaling water, so the tongue-jaw sac between the jaw arch and the tongue arch for the first time develops into a complete gill sac, which has a complete anterior and posterior half-gills like the 5 normal gill sacs behind it, and the half-gills have gills, which are the main places for gas exchange.

With the origin of the jaw and double nostrils, some jaws have successfully evolved double nostrils, but the double nostrils do not communicate with the mouth, have no respiratory function, only the function of smell. However, the breathing needs of fish have not decreased, so the first gill sac (tongue and jaw sac) behind the eye has been transformed into a water spray hole and become the main respiratory organ, which has already occurred in the most primitive jawed shield fish, because the most primitive shield fish carcassfish (groove scale fish) and the most advanced full jaw shield fish (unicorn fish) already have water nostrils, so the water spray holes are likely to have originated simultaneously with the appearance of jaws and double nostrils in the jaw companions.

Water spray holes are mainly used to suck in water streams in cartilaginous fish, while teleost fish are mainly used to breathe air, such as in living polyfin fish, they will expose their heads to the water, breathe air through the small holes on the top of their heads called “water spray holes”, and make a loud “inhalation sound”.

All of this evidence suggests that early teleost fish had the ability to breathe air from water vents, and as a new way of breathing, this is likely a pre-adaptive feature of fish leaving the waters and landing on land to breathe air, thus providing a prerequisite for fish to board land to breathe air.

With the origin of the inner nostrils in meatfin fish (such as Ken’s fish), the passage between the nasal cavity and the mouth was successfully opened, and the nostrils became the main respiratory organ, thus laying the foundation for the fish to land and breathe with their lungs. The quadrupeds that landed on land, faced with a whole new environment, had to develop new senses in order to survive better in the air.

In this way, the water jet holes that have lost their respiratory function have been modified and gradually evolved into our middle ear cavity, the tympanic membrane chamber, and the hyoid and jawbones and the square bones and joint bones with them have gradually degenerated and become smaller, and finally entered our middle ear, evolving into three auditory ossicles of our middle ear, and were renamed stapes, hammer bones and anvils, responsible for transmitting sound to the brain, and we humans eventually have a sensitive sense of hearing.

So, if it weren’t for the bold experiments of these prehistoric fish breathing air through overhead water vents, we might never have evolved such a keen sense of hearing. Our ears and mouth are still connected, and it is the Eustachian tube that evolved from the water spray hole that connects them.

Today, the Eustachian tube, like our cecum, seems to have no function anymore, but it was once the main channel for fish to breathe, and now it is an evolutionary remnant left to us by fish. In other words, our fish ancestors used to breathe with our ears, and biological evolution is so wonderful.

Co-authors of the study include Zhu Min, academician of the Chinese Academy of Sciences, Philip C.J. Donoghue, academician of the Royal Academy of Sciences, and Per E. Ahlberg, academician of the Royal Swedish Academy of Sciences.

The research has been funded by the Strategic Science and Technology Pilot Project of the Chinese Academy of Sciences, the National Natural Science Foundation of China, and the Frontier Science Key Research Program of the Chinese Academy of Sciences. (Source: China Science Daily Cui Xueqin)

Related paper information:https://doi.org/10.3389/fevo.2022.887172



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