Luo Lab | University of Chicago

Zhou, C.-F. Bhullar, B.-A. S., Neander, A. I., Martin, T. and Z.-X, Luo. 2019. New Jurassic mammaliaform sheds light on early evolution of mammal-like hyoid bones. Science. 365: 276-279. (doi: 10:1126/science.aau9345)

Abstract

We report a new Jurassic docodontan mammaliaform found in China that is preserved with the hyoid bones. Its basihyal, ceratohyal, epihyal, and thyrohyal bones have mobile joints and are arranged in a saddle-shaped configuration, as in the mobile linkage of the hyoid apparatus of extant mammals. These are fundamentally different from the simple hyoid rods of nonmammaliaform cynodonts, which were likely associated with a wide, nonmuscularized throat, as seen in extant reptiles. The hyoid apparatus provides a framework for the larynx and for the constricted, muscularized esophagus, crucial for transport and powered swallowing of the masticated food and liquid in extant mammals. These derived structural components of hyoids evolved among early diverging mammaliaforms, before the disconnection of the middle ear from the mandible in crown mammals.
 
Press Release

Jurassic fossil shows how early mammals could swallow like their modern descendants

By Matt Wood

Discovery of a new fossil in China sheds light on when early mammal ancestors first evolved sophisticated hyoid bones that gave them the ability to swallow food like modern-day mammals.

The 165-million-year-old fossil of Microdocodon gracilis, a tiny, shrew-like animal, shows the earliest example of modern hyoid bones in mammal evolution.

The hyoid bones link the back of the mouth, or pharynx, to the openings of the esophagus and the larynx. The hyoids of modern mammals, including humans, are arranged in a “U“ shape, similar to the saddle seat of children’s swing, suspended by jointed segments from the skull. It helps us transport and swallow chewed food and liquid – a crucial function on which our livelihood depends.

Mammals as a whole are far more sophisticated than other living vertebrates in chewing up food and swallowing it one small lump at a time, instead of gulping down huge bites or whole prey like an alligator.

“Mammals have become so diverse today through the evolution of diverse ways to chew their food, weather it is insects, worms, meat, or plants. But no matter how differently mammals can chew, they all have to swallow in the same way,” said Zhe-Xi Luo, PhD, a professor of organismal biology and anatomy at the University of Chicago and the senior author of a new study of the fossil, published this week in Science.

“Essentially, the specialized way for mammals to chew and then swallow is all made possible by the agile hyoid bones at the back of the throat,” Luo said.

‘A pristine, beautiful fossil’

This modern hyoid apparatus is mobile and allows the throat muscles to control the intricate functions to transport and swallow chewed food or drink fluids. Other vertebrates also have hyoid bones, but their hyoids are simple and rod-like, without mobile joints between segments. They can only swallow food whole or in large chunks.

When and how this unique hyoid structure first appeared in mammals, however, has long been in question among paleontologists. In 2014, Chang-Fu Zhou, PhD, from the Paleontological Museum of Liaoning in China, the lead author of the new study, found a new fossil of Microdocodon preserved with delicate hyoid bones in the famous Jurassic Daohugou site of northeastern China. Soon afterwards, Luo and Thomas Martin from the University of Bonn, Germany, met up with Zhou in China to study the fossil.

“It is a pristine, beautiful fossil. I was amazed by the exquisite preservation of this tiny fossil at the first sight. We got a sense that it was unusual, but we were puzzled about what was unusual about it,” Luo said. “After taking detailed photographs and examining the fossil under a microscope, it dawned on us that this Jurassic animal has tiny hyoid bones much like those of modern mammals.”

This new insight gave Luo and his colleagues added context on how to study the new fossil. Microdocodon is a docodont, from an extinct lineage of near relatives of mammals from the Mesozoic Era called mammaliaforms.  Previously, paleontologists anticipated that hyoids like this had to be there in all of these early mammals, but it was difficult to identify the delicate bones.  After finding them in Microdocodon, Luo and his collaborators have since found similar fossilized hyoid structures in other Mesozoic mammals.

“Now we are able for the first time to address how the crucial function for swallowing evolved among early mammals from the fossil record,” Luo said. “The tiny hyoids of Microdocodon are a big milestone for interpreting the evolution of mammalian feeding function.”

New insights on mammal evolution as a whole

Luo also worked with postdoctoral scholar Bhart-Anjan Bhullar, PhD, now on the faculty at Yale University, and April Neander, a scientific artist and expert on CT visualization of fossils at UChicago, to study casts of Microdocodon and reconstruct how it lived.

The jaw and middle ear of modern mammals are developed from (or around) the first pharyngeal arch, structures in a vertebrate embryo that develop into other recognizable bones and tissues. Meanwhile, the hyoids are developed separately from the second and the third pharyngeal arches. Microdocodon has a primitive middle ear still attached to the jaw like that of other early mammals like cynodonts, which is unlike the ear of modern mammals. Yet its hyoids are already like those of modern mammals.

“Hyoids and ear bones are all derivatives of the primordial vertebrate mouth and gill skeleton, with which our earliest fishlike ancestors fed and respired,” Bhullar said. “The jointed, mobile hyoid of Microdocodon coexists with an archaic middle ear — still attached to the lower jaw. Therefore, the building of the modern mammal entailed serial repurposing of a truly ancient system.”

The tiny, shrew-like creature likely weighed only 5 to 9 grams, with a slender body, and an exceptionally long tail. The dimensions of its limb bones match up with those of modern tree-dwellers.

“Its limb bones are as thin as matchsticks, and yet this tiny Mesozoic mammal still lived an active life in trees,” Neander said.

The fossil beds that yielded Microdocodon are dated 164 to 166 million years old. Microdocodon co-existed with other docodonts like the semiaquatic Castorocauda, the subterranean Docofossor, the tree-dwelling Agilodocodon, as well as some mammaliaform gliders.

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The study, “New Jurassic mammaliaform sheds light on early evolution of mammal-like hyoid bones,” was published in Science on July 19, 2019. The research was supported by the University of Chicago Division of Biological Sciences (Luo); the Deutsche Forschungsgemeinschaft (Martin); and the National Natural Science Foundation and Ministry of Land Resources of China, Shenyang Normal University, and Shandong University of Science and Technology (Zhou).

Authors and Contacts

Prof. Zhe-Xi Luo
University of Chicago, Chicago, IL, USA
+1.773.702.7816; zxluo@uchicago.edu

Prof. Thomas Martin
Universität Bonn, Bonn, Germany
+49.228.734.803; tmartin@uni-bonn.de

Prof. Bhart-Anjan S. Bhullar
Yale University, New Haven, CT, USA
+1.402.689-5998; bhart-anjan.bhullar@yale.edu

Prof. Chang-Fu Zhou
Paleontological Museum of Liaoning, Shenyang, China
+86.186.4028.3488; zhoucf528@163.com

Images

Attention: Artwork and photographs downloaded from here are for media use only. High resolution images available from April Neander at aisch@uchicago.edu.

Image 1: Microdocodon Fossil

The fossil of Microdocodon gracilis is preserved in two rock slabs, and consists of a main part (PMOL-AM00025A, left) and a counter part (PMOL-AM00025B, right). It was found in a site near the Wuhua village in the Daohugou area of Inner Mongolia, China, and the estimated age of the fossil site is at least 164 million years. The type specimen of this new mammaliaform is deposited in the Paleontological Museum of Liaoning (Shenyang, China) (Photo by Zhe-Xi Luo, the University of Chicago).

微小柱齿兽-辽宁古生物博物馆馆藏正型标本(BMNH-PM00025)照片。

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Image 2: Microdocodon Reconstruction

Life reconstructions of Microdocodon gracilis – a docodont mammaliaform. Microdocodon was a tiny animal. It has a skull length of 2 cm (3/4 inch), a head-body length about 6 cm (2 inches), and a long tail about 8 cm (about 3 inches) in length. The animal likely weighed between 5 grams to 9 gram (less than 1/3 of an ounce). Its slender and gracile skeletal elements suggest that it was an agile and active animal living on the tree. Its teeth were for insectivorous diet. This reconstruction depicts Microdocodon as a nocturnal animal active on a bennettitalean tree of the Jurassic (Illustration by April I. Neander, the University of Chicago).

骨骼复原和生活方式重建 (美国芝加哥大学April I. Neander)

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Image 3: Map of Fossil Site

Geographical location of the new fossil discovery. The specimen of Microdocodon is from a fossil site near the Wuhua village, a part of the famous Jurassic Daohugou fossil sites, in the Daohugous area of the Ningcheng County of Inner Mongolia Region of China. The Daohugou Sites are Middle Jurassic in age, and directly dated to be 165 million years.

柱齿兽类新化石的化石发现地点:微小柱齿兽发现于内蒙古宁城的中侏罗系道虎沟五华村。

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Image 4: Hyoid Evolution

Modern mammals, such as the dog and the platypus, have segmented hyoid bones with mobile joints, arranged in saddle-like configuration. The mobile hyoids apparatus support the tongue and link the pharunx with the larynx and the opening of esophagus. This structure plays a crucial function in transporting and swallowing of the masticated food and fluid in mammals. The new fossil of Microdocodon shows that its hyoids have the jointed segments, and arranged in a saddle shape, as those of modern mammals. This structure is different from the hyoid rods of the Triassic Thrinaxodon, a distant cynodont relative to mammaliaforms. This suggests that crucial transformation to the mammal-like hyoids occurred in the common ancestor of Mesozoic mammaliaforms and modern mammals, but before the rise of modern mammals. (Illustration by April I. Neander of the University of Chicago.)

哺乳动物舌骨构造演化:现代哺乳动物的舌骨构造由甲状舌骨、基舌骨、角舌骨和上舌骨组成,其形态特征独特:骨节之间有活动关节,结构呈鞍状,区别于更原始的犬齿兽和现代爬行动物的简单棒状结构。现代哺乳动物舌骨有活动关节的鞍状构造是咽咙的框架,对食物和液体的传输和吞咽中有关键作用。“微小柱齿兽”的新化石保存了现代哺乳型动物同样的舌骨结构特征。 微小柱齿兽的新发现表明:现代哺乳动物的舌骨构造起源并传承于更为原始的哺乳型动物,出现于哺乳型动物获得咀嚼能力的最早期阶段。(美国芝加哥大学April I. Neander.)

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Image 5: Evolution of Mesozoic Mammaliaforms and Extant Mammals

Mesozoic mammaliaforms are long-extinct relatives to the extant mammals (crown Mammalia). Docodonts are such a lineage of mammaliaforms. Morphologies of Mesozoic mammaliaforms provide evidence of the ancestral condition from which modern mammals have evolved. The newly discovered Jurassic mammaliaform Microdocodon offers the earliest-known evidence of the derived, mammal-like hyoids in the Mesozoic mammal evolution. (Illustration by April I. Neander of the University of Chicago.)

齿兽哺乳型物与代哺乳物的演化:哺乳型动物是现生哺乳动物的已绝灭的近亲支系。柱齿兽类是哺乳型动物多个支系中的一个广泛分布的支系。柱齿兽哺乳型动物的特征代表了哺乳动物起源演化过程中原始的形态。最新发现微小柱齿兽化石所保存的舌骨构造,就为哺乳动物最早期的舌骨构造形态的演化模式和过程,提供了新证据和新认识。(美国芝加哥大学April I. Neander.)

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Movie: New Fossil of Microdocodon and Evolution of Mammalian Hyoids

Tiny hyoid bones are preserved below the skull in the Jurassic mammaliaform Microdocodon. Comparison of Microdocodon to distant cynodont relatives and modern mammals reveals new information about hyoids and middle ears of Mesozoic mammals. The discovery of modern mammal-like hyoids of a mammaliaform sheds light on the first appearance of the swallowing function in mammal evolution. (Movie by April I. Neander/UChicago.)

mp4 Movie 12.1MB

 

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