Science - USA (2020-01-17)

breakdown of all kinds of food by intensify-

ing the transverse movement and integrating

long-axis rotation (that is, rolling) ( 2 ). Chew-

ing reduces the size of food to facilitate ac-

cess to nutrients. The smaller the particles,

the larger the surface available to gut micro-

biota, and acquiring the ability to digest a

new diet is a fundamental driver for the evo-

lution of new species ( 3 ). Mammalian teeth

play a key role in food processing because

they function as tools for breaking food into

pieces. In therian mammals, a typical form of

molars evolved (the tribosphenic, or multi-

functional molar) with a characteristic cusp

and basin pattern. This molar type is consid-

ered a revolution in mammalian evolution.

Its functionality widened the range of food

resources ( 4 ), and that this tooth type is re-

tained in the majority of omnivorous and in-

sectivorous mammals living today speaks for

its universal utility. It is consensus that the

tribosphenic molar gave rise to the variety

of tooth forms of extant mammals ( 5 ). How-

ever, the morphology combining cutting and

crushing functions is only fully functional in

combination with a transverse movement of

the lower jaw.

By definition, mammals possess a single

bone (dentary) as the tooth-bearing lower

jaw, and multiple tiny ossicles in the middle

ear (malleus, incus, and stapes). In mamma-

lian ancestors (nonmammalian cynodonts),

the lower jaw was composed of multiple

bones (angular, quadrate, and articular)

that transmitted sound by bone conduction

through the so-called mandibular ear, in ad-

dition to its function in catching prey and

chewing. In these early forms, the quadrate

and articular formed the primary jaw joint,

an articulation found in all jawed (gnathos-

tome) vertebrates ( 6 ). Transitional taxa like

Morganucodon had a double cranioman-

dibular joint; this consisted of a primary jaw

joint that coexisted with a derived secondary

articulation between the condyle (rounded

hinge area of a bone) of the lower jaw and

the squamosal (bone part of the vertebrate

skull of the cranium). In these early mam-

malian forms, the primary jaw joint was still

involved in both feeding and transmitting

sound to the inner ear. The middle ear bones,

still attached to the lower jaw and sitting

in grooves on the inner side of the dentary

(postdentary trough) were limited in their

mobility. In such close connection, hearing

and feeding functions interfered. Transverse

shift or even rolling of the dentary bone was

limited, because these movements would en-

tail displacement of the middle ear elements

inside the postdentary trough (see the fig-

ure). During the evolution of the mammalian

feeding function, the secondary jaw articula-

tion prevailed. The middle ear bones shrank

and shifted posteriorly, and the innovative

secondary jaw joint allowed more powerful

jaw movements and effective control of the

dentary during chewing ( 7 ).

Homology of the primary jaw joint bones

and the mammalian middle ear elements

is a classic case study of embryology, and

similarities were identified in the 19th cen-

tury. Supporting tissues, like the Meckelian

and palatoquadrate cartilages of the first

vertebrate pharyngeal arch, are embryonic

precursors to the articular and quadrate of

nonmammalian gnathostome vertebrates

and malleus and incus of living mammals ( 8 ).

Genetic mechanisms controlling the forma-

tion of the mammalian jaw and middle ear

became an area of interest in developmental

biology in the past 25 years. A series of cellu-

lar and molecular drivers in the developmen-

tal program of vertebrate pharyngeal arches

were identified, which also control formation

and detachment of the mammalian middle

ear ossicles from the lower jaw ( 9 , 10 ).

The complex developmental process of

the detachment of the middle ear elements

is well understood from an ontogenetic per-

spective, but timewise, the separation in the

stem lineage of therians was not known from

the fossil record. O. lii is the first fossil that

pinpoints the moment of detachment of the

middle ear ossicles from the Meckelian carti-

lage to Lower Cretaceous (~123 million years

ago). Other stem therian representatives like

Yanoconodon allini or Maotherium asiati-

cus, slightly older than O. lii, show separate

SCIENCE sciencemag.org

GRAPHIC: ADAPTED FROM (

1 ) AND (

15
) BY N. CARY/

SC IENCE

Position of Origolestes lii in the mammalian phylogeny

Origolestes

Yanoconodon

Monotremata

Monodelphis and Didelphis

Equus

2

1

3

4

Tr a n s v e r s e

movement

or roll

Schematic of the posterior side of the mammalian

dentary during the decoupling process (left ossicles

still connected to lower jaw, right detached)

Middle ear bones Meckel’s cartilage

1 Mammalia

2 Theriamorpha

3 Trechnotheria

4 Theria

Specimens of Origolestes lii were discovered

in the Lujiatun beds of the Yixian Formation,

Liaoning Province, China. The illustration shows

that the animals died at rest, a condition

similar to those found for other vertebrates from

the same locality, including dinosaurs.

Evolution of the therian dentary

and middle ear

The connection of the middle ear elements (teal)

to the lower jaw by means of the ossified Meckelian

cartilage (orange) is lost.

17 JANUARY 2020 • VOL 367 ISSUE 6475 245

Published by AAAS