Their dorsal aorta and esophagus actually "drift"?

Produced by: Science Popularization China

Author: Gai Zhikun, Meng Xinyuan (Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences)

Producer: China Science Expo

Recently, the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, published the latest research results on the armored fish Yuhai Pterygoscelis. The study reported new materials of Yuhai Pterygoscelis discovered in the Xujia Chong Formation of the Early Devonian Pragian Stage (about 410 million years ago) in Qujing, Yunnan. It revealed for the first time the positional relationship between the esophagus and dorsal aorta of armored fish, and solved the mystery of the asymmetry of the dorsal aorta and esophagus drifting to the right in lampreys and bony fishes [1].

The "vampire" lamprey in the water & the bone turtle that often looks "surprised"

Before revealing the mystery of the rightward drift of the dorsal aorta and esophagus of lampreys and bony fishes, let us first get to know our two protagonists.

The lamprey is a jawless vertebrate that lives in water and is semi-parasitic . It has an eel-shaped body, no paired fins, and only dorsal and caudal fins. There is a round funnel-shaped suction organ on the front ventral side of the head, which is used to attach to other fish. Inside the funnel is the mouth, which has a special "file tongue" with keratin teeth on it, which can be extended from the bottom of the mouth. When the lamprey sucks its prey, the file tongue acts as a piston to suck the blood of the prey.

Figure 1. “Water vampire” lamprey

a. Sea lamprey (Petromyzon marinus), side view (Photo credit: D. Pulera);

b. Sea lampreys in the Great Lakes region of the United States (Photo credit: Photo taken by Zhikun Gai in Chicago, USA)

The nostrils of lampreys are located on the top of their heads. Unlike other animals, lampreys have only one nostril. The single nostril is a very interesting phenomenon among cyclostomes among living vertebrates.

Behind the nostrils is the pineal eye, which has a light-sensitive function and can be called the lamprey's "third eye". The eyes are located on both sides of the head, and from the eyes to the back is a row of 7 small round gill openings, hence the name lamprey.

Although the lamprey's nervous system is relatively primitive, its senses are very sensitive. As long as there is a fish swimming within 30 meters of it, it will shoot straight at the other party like a sharp arrow and instantly suck the fish with its suction cup. Usually, it only takes 2 hours for the sucked fish to die because of being sucked dry of blood, and then the lamprey will let go and "go away".

In the sea, even huge whales are often visited by lampreys. Whales have no way to deal with these "hateful" guys, and can only let them suck their blood and have a full meal. So lampreys are really the real "vampires" in the water!

The second protagonist of the story, the armored fish, is the most successfully developed group of armored fish in the Silurian-Devonian period. There are about 200 species, mainly living in North America, Europe, Siberia and Central Asia.

Most bony fish seem to have paired pectoral fins and a flexible caudal fin (a caudal fin), which indicates that bony fish may be the most flexible and athletic group of armored fish.

Figure 2 Various types of bony fish

(Photo credit: Yang Dinghua)

The entire back of the head of the bony fish is covered by a complete semicircular bone armor. The ventral side is the location of the mouth and external gill openings, surrounded by tiny bone pieces or scales. There is a pair of orbital holes (the location of the eyes) in the front of the head armor, a single nasopituitary hole in the middle, and a small pineal hole in the back. The "mouth" of the bony fish that looks like it is open in surprise is actually its "nostrils".

The "nostrils" (nasopituitary apertures) of bony fish are strikingly similar to those of modern lampreys, so scientists initially thought that the two groups might be directly related. However, current research results suggest that their similarities may be the result of parallel evolution.

Oh, the seniority is messed up.

There is a rather peculiar phenomenon in the jawless lamprey larvae and some bony fish: their dorsal aorta is unpaired and asymmetrical, that is, their aorta does not extend completely along the midline of the body, but has a significant rightward drift behind the gill area.

The blood circulation route of fish is a single circulation. The single circulation refers to the oxygen-deficient blood that is squeezed out of the ventricle, exchanges gas through the gills, and then merges into the dorsal aorta on the back of the body and below the spine, and then transports the oxygen-rich blood to various organs and tissues in the body. The oxygen-deficient blood that leaves the organs and tissues will eventually return to the venous sinus of the heart, and then a new round of blood circulation will begin.

The dorsal aorta is the first functional intraembryonic blood vessel to appear in vertebrates. It arises as two separate bilateral vessels in the trunk and undergoes a lateral translocation from the lateral position to the midline, where it eventually fuses into a single large vessel. Therefore, the evolution of the dorsal aorta serves as an ideal model to help us understand the mechanisms that control the establishment and remodeling of larger blood vessels in the body.

At present, the asymmetric phenomenon of the dorsal aorta and esophagus drifting to the right has only been found in the larvae of lampreys and bony fishes. It was once one of the evidences supporting the close relationship between living lampreys and bony fishes. Scientists speculate that lampreys are descendants of bony fishes that evolved after the exoskeleton degenerated.

With the development of cladistics, more and more evidence shows that the lack of exoskeleton in lampreys may represent a primitive characteristic of vertebrates, that is, lampreys are a more primitive jawless fish; while bony armored fish have more advanced characteristics of jawed fish, such as paired pectoral fins, osteoderms, and upwardly crooked tails, and are the sister group most closely related to jawed fish.

Therefore, the asymmetric phenomenon of the rightward drift of the dorsal aorta of lampreys and bony fishes may be the result of parallel evolution! In this case, it is very important to understand the situation of Chinese armored fishes, which are located between lampreys and bony fishes.

Figure 3 Comparison of the distribution of the esophagus and dorsal aorta of lampreys (a), bony fishes (b, c), armored fishes (d, e) and modern cartilaginous fishes (f, g)

(Photo credit: Meng Xinyuan)

The "star" of my country's armored fish

In the past, due to the limitations of preservation techniques and the scarcity of fossils, scientists knew very little about the ventral and internal anatomical features of armored fish. The new specimen of Yuhai Pterygophorus clearly preserves key morphological information of the ventral surface and is the first key fossil to clearly reveal the positional relationship between the esophagus and the dorsal aorta.

In the early 1990s, Academician Zhu Min, a famous Chinese paleoichthyologist, discovered the Yuhai winged hornfish fossil for the first time during a field geological survey in Qujing, Yunnan. The fossil was found in the Xujia Chong Formation of the Prague Stage of the Early Devonian.

Figure 4 Photo of the Yuhai Pterygophorus fossil

(Photo credit: Photo by Gai Zhikun)

In 1992, Academician Zhu Min officially named the fossil "Yuhai Winged Hornfish" and published his results in the Journal of Vertebrate Paleontology. The genus name indicates that it has a pair of wing-shaped horns extending laterally, and the species name is given to Mr. Liu Yuhai, the first person to study armored fish.

The Yuhai Wingfish belongs to the order Eusarcheidae in the subclass of armored fishes. It is a special group in the order Eusarcheidae with a snout and lateral horns. The armored fish is a genus and species unique to East Asia. It is currently only found in the Silurian and Devonian strata in southern China, the northern edge of the Tarim Basin and northern Vietnam. It is a group with a strong indigenous color.

Figure 5 Ecological restoration of the Yuhai winged anglerfish

(Photo credit: Yang Dinghua)

Figure 6 Reconstruction of the Jade Sea Wingfish

(Photo credit: Guo Xiaocong)

Although the research history of armored fish is only a short 50 years, thanks to the efforts of the older generation of paleoichthyologists such as Liu Yuhai, Pan Jiang, Wang Nianzhong, and Wang Junqing, a classification unit at the subclass level has been established. More than 90 species have been discovered so far, and together with bony armored fishes and heteroarmored fishes, they constitute the three major groups with the richest species and the greatest population diversity among jawless fishes.

The "driving force" behind the aorta's rightward drift: asymmetric Cuvier's duct

In the new specimen of Yuhai Pterygium, two openings are retained on the midline of the posterior gill wall. The opening near the ventral side is much larger than the opening near the dorsal side, so the former is more likely to be the passage of the esophagus, while the latter may be the passage of the dorsal aorta.

Figure 7 Photo of the Yuhai Pterygophorus fossil

(Photo credit: Photo by Gai Zhikun)

Previously, an opening was preserved on the gill posterior wall of the Silurian true armored fish Xikeng split snout fish in Jiangxi, and this opening was once thought to be the passage of the neural tube (Figure 7e). However, the three-dimensional reconstruction image of the brain CT of the dawn fish shows that the neural tube should be located on the dorsal side of the top of the oral branchial cavity, while the hole is close to the ventral side of the oral branchial cavity. Therefore, the hole cannot be the passage of the neural tube, but should be the passage of the esophagus.

Comparative anatomical studies of early fish have shown that the dorsal aorta of armored fish is the same as that of jawed fish, which is also paired and extends along the midline of the body without obvious rightward drift. Since the same situation also exists in the cephalochordate amphioxus and the jawless hagfish, this may represent the ancestral state of vertebrates.

This proves that the rightward drift of the aorta of lampreys and bony armored fishes may be an evolutionary convergence phenomenon caused by the asymmetry of the Cuvier duct . The Cuvier duct is an anatomical structure named after Georges Cuvier (1769-1832), a famous French zoologist and founder of comparative anatomy and paleontology in the 18th and 19th centuries. It refers to the blood of the left and right anterior cardinal veins and the two posterior cardinal veins all converging into a pair of transverse common cardinal veins (Figure 8). Including us humans, the Cuvier ducts on the left and right sides are not symmetrical, and the right one is much larger than the left one (Figure 8).

In the body structure of lampreys, the left and right Cuvier tubes are asymmetrical, with the right one being thicker than the left. Since the lamprey's esophagus is connected to the dorsal aorta through connective tissue, in order to prevent the esophagus from collapsing on the heart that is not protected by the pericardium, the dorsal aorta and esophagus will bend to the right (Figure 8).

In bony fish, the heart is already protected by the pericardial cavity, so why do the dorsal aorta and esophagus drift to the right?

This may be due to the narrow space caused by the dorsal and ventral flattening of the head armor of bony fish, as well as the squeezing of the thick Cuvier's tube on the right side. The combined effect of the two ultimately leads to the bending phenomenon of the dorsal aorta and esophagus drifting to the right (Figure 8).

Figure 8 The Cuvier tubes on the left and right sides of humans are not symmetrical. The right side is much larger than the left side.

(Image source: Wikipedia, the free encyclopedia)

In addition, the dorsal aorta and esophagus of bony fishes share a semi-enclosed cartilaginous groove, which may represent an intermediate state between lampreys (no cartilage covering) and armored fishes and gnathostomes (completely covered with cartilage) (Figure 9).

Figure 9 The evolution of some key features in chordates

(Photo credit: Meng Xinyuan)

Conclusion

The re-study of Pterygophorus yuhaiensis not only fills the gap in the anatomical information of armored fishes and helps to understand the internal anatomy of armored fishes, but also has important significance for exploring the phylogenetic relationship between lampreys, armored fishes, bony fishes and jawed vertebrates, and understanding the origin and evolution of key features of jawed fishes. This study is also a moving achievement made by generations of paleontologists over 30 years.

References:

[1] Meng, X.-Y., Zhu, M., Li, Q., & Gai, ZK* 2022. New data on the cranial anatomy of Pterogonaspis (Tridensaspidae, Galeaspida) from the lower Devonian of Yunnan, China and its evolutionary implications. The Anatomical Record, 1–14.

[2] Gai Zhikun and Zhu Min, “The Evolution of Jawless Groupers and the Chinese Fossil Record”, 2017.

Note: The relevant results of this article were completed by Master's graduate Meng Xinyuan under the guidance of researcher Gai Zhikun, and have been published online in the international academic journal "The Anatomical Record". "The Anatomical Record" is the official publication of the American Anatomical Association, founded in 1888. The journal focuses on the latest progress in the field of morphology and anatomical research, covering multiple fields such as molecular, cellular, systemic and evolutionary biology.