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Q U E S T I O N A N D A N S W E R Open Access
Q&A: Morphological insights into evolution
Neal Anthwal
*
and Abigail S. Tucker
Abstract
In this question and answer article we discuss how
evolution shapes morphology (the shape and pattern
of our bodies) but also how learning about
morphology, and specifically how that morphology
arises during development, can shed light on
mechanisms that might allow change during
evolution. For this we concentrate on recent findings
from our lab on how the middle ear has formed in
mammals.
How does evolution help us understand
morphology?
Evolution is key to understanding why we look like we
do: it can explain why humans have four limbs each with
five digits, two forward facing camera eyes, and a mouth
full of teeth of different shapes compared to why fruit
flies have six limbs plus two wings, two compound eyes,
and a proboscis for a mouth. Our anatomy has been
slowly shaped over millions of years, and an understand-
ing of evolutionary history can help explain the similar
pattern of bones observed in vertebrate limbs. Humans,
bats, reptiles and whales evolved from a common ances-
tor, and the developmental programme to make limbs is
shared across these animals and is based on that of this
common ancestor. Although the limbs of vertebrates
have diverged functionally into the wings of bats, the
arms of humans, the forelimbs of reptiles and the fins of
whales, they are nevertheless homologous: the general
skeletal structure is similar in each, despite large differ-
ences in individual bone size and shape (Fig. 1). In
contrast, the common ancestor of humans and fruit flies
did not have any limbs, so our limbs and the limbs of
the fly are independently evolved and not homologous.
* Correspondence: n.anthwal@kcl.ac.uk
Department of Craniofacial Development and Stem Cell Biology, King’s
College London, Floor 27 Guy’s Tower, Guy’s Hospital, London Bridge,
London SE1 9RT, UK
It might be useful to be able to fly—why don’twe
evolve wings on our backs like the fly?
It would be useful, but unfortunately it’snighonimpos-
sible. This is because the form of an organism is made dur-
ing its embryonic development by following developmental
programmes encoded in our genes. These programmes
need to be adjusted to change anatomy, and adjustments
can only be made on what is already there. Any changes
made in earlier developmental programs will have effects
on all later programs. Therefore, the possibilities of form
(known as phenotype) encoded by the genes (or genotype)
are not infinite and form can only change by tinkering with
what’s already there. This is called developmental con-
straint[1].Insectwingsarelikelytohaveevolvedfrom
appendages on the exoskeleton of their ancestors that are
absent in our lineage, so they cannot be altered to form
wings. Although in principle one might evolve to fly in a
different way—bats and birds have both independently
evolved wings from their forelimbs, what we call conver-
gence—in this case other constraints are in operation. To
evolve wings like those of bats, we would have to lose the
current function of our hands and arms, which seems an
unlikely evolutionary path to take. Other constraints would
also be in operation—for example the power required for
flight, given the typical human’s weight, would be more
than could be generated by our pectoral muscles. When
the bones of vertebrates that fly are studied it is clear that
they have undergone adaptations to allow flight, with the
evolution of hollow or very slender bones.
What can we learn about evolution by studying
morphology?
Morphology is a very useful way of understanding evolu-
tionary processes. Charles Darwin famously noticed
differences in beak morphology of Galapagos finches,
which helped inform his theory of natural selection and
the ‘Origin of species’. Recently the developmental pro-
grams underlying shape variation in Darwin’sfincheshave
begun to be understood, with key gene networks—invol-
ving Bmp4,calmodulin,β-catenin,Tgf br2 and Dkk—hav-
ing been demonstrated to control the size and shape of
the beak. Strikingly finch-like beaks could be induced in
© Anthwal et al. 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
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Anthwal and Tucker BMC Biology (2017) 15:83
DOI 10.1186/s12915-017-0425-z
chick embryos by manipulating these signaling pathways
[2]. Understanding morphology, and how that morph-
ology is created in the embryo (developmental biology),
can illustrate how it is possible to modify structures
and thereby suggest mechanisms that may underlie
evolutionary change (evodevo).
Does this mean that understanding morphology
can only tell us about small changes that make
species different to each other within groups of
animals?
No, while the above examples are compelling examples
for the importance of morphological change at the micro
level, morphology can be very useful in understanding
changes that gave rise to different groups of animals, i.e.
evolution at the macro level. For example in our lab we
are interested in the morphological and developmental
changes giving rise to the evolution of mammals. This
work involves comparing embryonic development with
the fossil record.
How can we study mammalian evolution through
morphology?
To understand mammalian evolution we need to be able
to accurately identify what defines a mammal—but this
is somewhat difficult, especially in evolutionary history
as observed in the fossil record. Most of the specialisa-
tions mammals have are shared by other groups, and so
are not on their own sufficient to identify a mammal.
Mammals belong to the aminote clade—tetrapod verte-
brates that protect their developing embryos—either in
an egg or in the mother—in a membrane called the am-
nion. Other amniotes include the birds and reptiles, and
one needs to be able to distinguish mammals from their
amniote relatives. While almost all mammals are warm-
blooded (the naked mole rat is a possible exception) so
are birds, so this can’t be used as a defining feature. It is
likely that the common ancestor of mammals and birds
was cold blooded, so the presence of endothermy in
these two groups is another example of convergent evo-
lution. Most mammals have live births; however, some
reptile species such as Zootoca vivipara and Pseudemoia
entrecasteauxii also give birth to live young, while the
extant monotreme species (the platypus and two echidna
species) lay eggs but are still mammals. All mammals
produce milk and most have fur, but these features are
not useful since they are not usually preserved in fossils.
However, a useful defining feature to identify mammals
and distinguish them from other amniotes like reptiles
and birds is a specialised middle ear and jaw joint—and
this is often easier to find in the fossil record.
You mentioned the middle ear—what’s the
difference between the middle ear in reptiles,
birds and mammals?
The ears of reptiles, birds and mammals are made up of
three components. These are the outer ear through
which sound in the form of vibrating air enters the head,
the inner ear in which sound is converted into neuronal
signals by vibration of hair cells lining the cochlea, and
the middle ear that sits between the two structures.
The middle ear is an impedance matching apparatus
that facilitates the transmission of sound from the air
(low impedance) to the liquid filled inner ear (high im-
pedance). The middle ear consists of the tympanic mem-
brane (ear-drum) for sound capture that is connected to
a membrane window into the inner ear via small bones
called ossicles. In birds and reptiles there is a single os-
sicle, called the stapes or columella, whereas mammals
have a chain of ossicles, the malleus, incus and stapes
(Fig. 2) [3]. In both cases the middle ear ossicle or ossi-
cles are in an air-filled cavity that allows for free vibra-
tion and transfer of sound to the inner ear. In whales
and aquatic mammals, this air-filled cavity is still present
but in addition to sound transfer through the three ossi-
cles, bone and soft tissue conduction occurs through the
lower jaw to aid with underwater hearing. A more
extreme reliance on bone conduction is observed in
snakes. Here the middle ear cavity has been lost and is
Fig. 1. Comparative anatomy of vertebrate limbs. The general
skeletal structure of vertebrate limbs is similar in each species,
despite large differences in individual bone size and shape reflecting
the different functions
Anthwal and Tucker BMC Biology (2017) 15:83 Page 2 of 4
filled with tissue that surrounds the stapes. The tym-
panic membrane and external ear are absent and instead
sound is detected as vibrations by the lower jaw [3].
Why does the middle ear differ between
mammals and other amniotes?
The extra ossicles of the mammalian middle ear have a
surprising origin. The common amniote’s ancestor did
not have a tympanic ear—that is to say they had no tym-
panic membrane or air filled middle ear—and sound was
heard by the vibration of bones embedded in tissue con-
nected to the inner ear. In the mammalian lineage of
mammal-like reptiles, changes in the jaw musculature
and teeth resulted in the evolution of a new jaw articula-
tion (the temporomandibular joint; TMJ) between the
squamosal and dentary bones. This new jaw joint ap-
pears to have aided stabilisation of the jaw and initially
worked together with the original primary jaw joint,
located between the quadrate in the cranial base and
articular in the mandible. The fossil record reveals ex-
amples of mammal-like reptiles, such as Morganucodon,
which used both joints to articulate its jaw. The increased
efficiency of the new jaw joint allowed the primary joint to
become less integrated into the jaw over time, and as a
consequence the bones of the jaw reduced in size and
were freed up for a new role in hearing. Eventually the pri-
mary jaw joint separated completely from the lower jaw.
This final separation gave rise to the definitive mammalian
middle ear, with the articular being homologous to the
malleus, and the quadrate to the incus. The two extra ossi-
cles in the mammalian ear were therefore repurposed
from the jaw joint of reptiles—a rather remarkable change
in function.
What is the evidence for this?
The evidence for the transition of the primary jaw joint
into the middle ear takes three main forms. Firstly, the
fossil record of the transition is remarkably complete
and we are able to follow the formation of the TMJ and
middle ear ossicles though a wide range of mammalian
ancestors known as cynodonts. Secondly, embryology
and developmental biology have revealed the mandibular
origins of the new parts of the middle ear in mammals.
In fact, it was the embryology carried out by Reichert
and Gaupp in the 19
th
and early 20
th
centuries that first
demonstrated the homology between the mammalian
middle ear and non-mammalian jaw articulation. Thirdly,
we can study marsupials. Marsupials, such as opossums
and kangaroos, are born very early in development, before
the bones of the jaw are fully formed, yet the young pups
need to suckle. They therefore use their middle ear bones,
which are still attached to the jaw at this stage, to feed.
Once the mammalian jaw joint has formed, the ossicles
then revert to a role in hearing. The change from a role
in feeding to hearing, mimicking the transformation
observed during evolution, can therefore be followed in
a living animal.
You said that the embryology was done over a
century ago—what’s the modern take on this
problem?
We have recently been using modern developmental
biology techniques to try and understand the mechanism
of this evolutionary change. Specifically we looked at the
cellular and molecular mechanism of the final separation
of the ear from the jaw, a developmental process that
mirrors evolution. In doing so we were able do demon-
strate that a group of cells called clasts are recruited to
break down a structure called Meckel’s cartilage that
joins the malleus in the ear to the mandible in the lower
jaw. In mice the ear and jaw are still physically attached
to each other at birth but a wave of clast cell recruitment
to this region a few days after birth leads to their separ-
ation. In mice with a mutation in cFos these clast cells
Fig. 2. Schematics of a sauropsid (bird, lizard) and mammal ear. In sauropsids (a) sound is transmitted from the ear drum to the sensory cells of
the cochlea via a single bone, the stapes (S) in the middle ear cavity (MEC). Mammals (b) have two extra bones, the malleus (M) and incus (I).
Reproduced from [3]
Anthwal and Tucker BMC Biology (2017) 15:83 Page 3 of 4
fail to form, and as a result Meckel’s cartilage does not
break down, but instead ossifies, and thus forms a hard
connection between the jaw and ear. This is similar to the
morphology of cynodonts, and so this mutant copies the
long extinct cynodont anatomy in a modern mammal [4].
The recruitment of clast cells to this part of Meckel’scar-
tilage may therefore have been an important step in the
isolation of the ear from the jaw, to create the definitive
mammalian ear. We were able to confirm that the Tg f-
beta signalling pathway played an important role in the
separation of the ear from the jaw [5]. Furthermore, our
evidence also suggests that placental mammals and mar-
supial mammals have slightly different Meckel’s cartilage
breakdown mechanisms, and so may have independently
acquired the final step of middle ear evolution.
Why should I care about evolution and
morphology?
An evolutionary insight into morphology can offer ways
of understanding some human disorders and diseases.
For example one of the most common human develop-
mental disorders is a limb with fewer than five digits.
When the limb anatomy of these affected individuals
was compared with birds and amphibians that naturally
have fewer than five digits, a high degree of similarity
was found in the arrangement of muscular attachment
to the skeleton [6]. The development of organisms from
these phylogenetic classes could therefore offer insights
into the basis of the human conditions, and the genetics
of the human conditions could inform the understanding
of digit evolution.
A further example lies in the middle ear, and the
spread of middle ear infection (otitis media). In mam-
mals the epithelium in the lower regions of the cavity is
derived from a part of the early embryo called the endo-
derm, while the remainder, like the large part of the ossi-
cles themselves, is formed by another group of early
embryonic cells called the neural crest [7]. This dual
origin appears to be unique to mammals and allowed for
the creation of an air-filled cavity around the three-
ossicles in the middle ear. The endoderm-derived epithe-
lium is complex and covered in cilia while the neural
crest-derived epithelium is simpler and unciliated. The
two epithelia respond differently to damage, and regions
adjacent to the neural crest-lined part of the middle ear
(the cochlea and mastoid) are more susceptible to com-
plications due to the spread of middle ear infections,
compared to parts of the cavity lined by endoderm. The
pattern of spread of ear injections therefore only makes
sense in the context of how the ear
develops and why it formed in that way during evolu-
tion. Understanding how a structure evolved, and how
structures are linked during evolution and development,
can therefore shed light on why and how abnormalities
arise.
Authors’contributions
NA and AST wrote the article. Both authors read and approved the final
manuscript.
Competing interests
The authors declare that they have no competing interests.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
References
1. Smith JM, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B,
et al. Developmental constraints and evolution: a perspective from the
Mountain Lake Conference on Development and Evolution. Q Rev Biol.
1985;60(3):265–87.
2. Mallarino R, Abzhanov A. Paths less traveled: evo-devo approaches to
investigating animal morphological evolution. Annu Rev Cell Dev Biol. 2012;
28(1):743–63.
3. Tucker AS. Major evolutionary transitions and innovations: the tympanic
middle ear. Philos Trans R Soc Lond B Biol Sci. 2017;372(1713):20150483.
4. Anthwal N, Urban DJ, Luo Z-X, Sears KE, Tucker AS. Meckel’scartilage
breakdown offers clues to mammalian middle ear evolution. Nature. 2017;1:93.
5. Urban DJ, Anthwal N, Luo Z-X, Maier JA, Sadier A, Tucker AS, et al. A new
developmental mechanisms for the separation of the mammalian middle
ear ossicles from the jaw. Proc R Soc B Biol Sci. 2017;284:20162416.
6. Diogo R, Smith CM, Ziermann JM. Evolutionary developmental pathology
and anthropology: A new field linking development, comparative anatomy,
human evolution, morphological variations and defects, and medicine. Dev
Dyn. 2015;244(11):1357–74.
7. Thompson H, Tucker AS. Dual origin of the epithelium of the mammalian
middle ear. Science. 2013;339(6126):1453–6.
Anthwal and Tucker BMC Biology (2017) 15:83 Page 4 of 4
