EXAPTATION
I would like to speak about EXAPTATION, an uncommon concept in the biology text books.
The assonance with the well known term ADAPTATION, a cornerstone in evolution theory with
many examples in biology books, is evident, but the term Exaptation is not so frequently used, and
its meaning is not as widely known by students. The Italian language lacks an equivalent term,
though we could translate the term “exaptation” with “cambiamento d’uso”, but this way is
obviously much less effective, although correct.
The concept of exaptation is well explained in the works of François Jacob and Stephan Jay Gould,
two great biologists, the former being even a Nobel Prize, and the latter representing - in my
opinion - the major and most influential writer of popular science, particularly of evolutionary
biology.
Exaptation, that is: evolution is a tinkerer
François Jacob, (Nancy 1920 - Paris 2013) got the Nobel Prize in 1965 together with Jaques Monod
and André Lwoff “for their discoveries concerning genetic control of enzyme and virus synthesis”.
These three biologists are usually known by students for the ‘Operon Lac’, that is a complex related
to genic regulation in bacteria.
But Jacob (as Monod, for that matter) has been also a great scientific writer, and he left us some
important writing of general biology and evolution. One of these, a paper wrote in 1977 for the
influential magazine Science, is titled Evolution and Tinkering. The tinkering (in french: bricoleur)
is a person which creates objects and machineries by using parts of broken or unused things,
proceeding sometimes without a well defined project.
«Often, without any well-defined long-term project, the tinkerer gives his
materials unexpected functions to produce a new object. From an old
bicycle wheel, he makes a roulette; from a broken chair the cabinet of a
radio. Similarly evolution makes a wing from a leg or a part of an ear from
a piece of jaw. Naturally, this takes a long time. Evolution behaves like a
tinkerer who, during eons upon eons, would slowly modify his work,
unceasingly retouching it, cutting here, lengthening there, seizing the
opportunities to adapt it progressively to its new use.
For instance, the lung of terrestrial vertebrates was, according to Mayr,
formed in the following way. Its development started in certain freshwater
fishes living in stagnant pools with insufficient oxygen. They adopted the
habit of swallowing air and absorbing oxygen through the walls of the esophagus. Under these
conditions, enlargement of the surface area of the esophagus provided a selective advantage.
Diverticula of the esophagus appeared and, under continuous selective pressure, enlarged into
lungs. Further evolution of the lung was merely an elaboration of this theme enlarging the surface
for oxygen uptake and vascularization. To make a lung with a piece of esophagus sounds very much
like tinkering.»
Jacob F., 1977 - Evolution and Tinkering, Science, ...
Some years later (1981) François Jacob wrote a book titled Le Jeu des possibles. Essai sur la
diversité du vivant (translated in 1982 as: The Possible and the Actual, and in 1983 as: Il gioco dei
possibili).
In this book Jacob resumes and develops the same topic and compares again the operating way of
evolutionary processes with the activity of an engineer:
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«The action of natural selection has often been compared to that of an engineer. This comparison,
however, does not seem suitable. First, in contrast to what occurs during evolution, the engineer
works according to a preconceived plan. Second, an engineer who prepares a new structure does not
necessarily work from older ones. The electric bulb does not derive from the candle, nor does the jet
engine descend from the internal combustion engine. To produce something new, the engineer has
at his disposal original blueprints drawn for that particular occasion, materials and machines
specially prepared for that task. Finally, the objects thus produced de novo by the engineer, at least
by a good engineer, reach the level of perfection made possible by the technology of the time.
In contrast, evolution is far from perfection, as was repeatedly stressed by Darwin, who had to fight
against the argument from perfect creation. In the Origin of Species, Darwin emphasizes over and
over again the structural and functional imperfections in the world. He always points out the
oddities, the strange solutions that a reasonable God would never have used.
In contrast to the engineer, evolution does not produce innovations from scratch. It works on what
already exists, either transforming a system to give it a new function or combining several systems
to produce a more complex one. Natural selection has no analogy with any aspect of human
behaviour. If one wanted to use a comparison, however, one would have to say that this process
resembles not engineering but tinkering, bricolage we say in French.
While the engineer’s work relies on his having the raw materials and the tools that exactly fit his
project, the tinkerer manages with odds and ends. Often without even knowing what he is going to
produce, he uses whatever he finds around him, old cardboards, pieces of string, fragments of wood
or metal, to make some kind of workable object. As pointed out by Claude Levi-Strauss, none of
the materials at the tinkerer’s disposal has a precise and definite function. Each can be used in
several different ways. What the tinkerer ultimately produces is often related to no special project. It
merely results from a series of contingent events, from all the opportunities he has to enrich his
stock with leftovers. In contrast with the engineer’s tools, those of the tinkerer cannot be defined by
a project. What can be said about an of these objects is that "it could be of some use." For what?
That depends on the circumstances.
In some respects, the evolutionary derivation of living organisms resembles this mode of operation.
In many instances, and without any well-defined long-term project, the tinkerer picks up an object
which happens to be in his stock and gives it an unexpected function. Out of an old car wheel, he
will make a fan; from a broken table, a parasol. This process is not very different from what
evolution performs when it turns a leg into a wing, or a part of a jaw into pieces of ear. (...).
When different engineers tackle the same problem, they are likely to end up with very nearly the
same solution: all cars look alike, as do all cameras and all fountain pens. In contrast, different
tinkerers interested in the same problem will reach different solutions, depending on the
opportunities available to each of them. This variety of solutions also applies to the products of
evolution, as is shown, for instance, by the diversity of eyes found throughout the living world. The
possession of light receptors confers a great advantage under a variety of conditions. During
evolution, many types of eyes appeared, based on at least three different principles: the lens, the
pinhole, and multiple holes. The most sophisticated ones, like ours, are lens-based eyes, which
provide information not only on the intensity of incoming light but also on the objects that light
comes from, on their shape, colour, position, motion, speed, distance, and so forth. Such
sophisticated structures are necessarily complex.
One might suppose, therefore, that there is just one way of producing such a structure. But this is
not the case. Eyes with lenses have appeared in molluscs and in vertebrates. Nothing looks so much
like our eye as the octopus eye. Yet it did not evolve the same way. In vertebrates, the
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photoreceptor cells of the retina point away from the light while in molluscs they point toward the
light. Among the many solutions found to the problem of photoreceptors, these two are similar but
not identical. In each case, natural selection did what it could with the materials at its disposal.»
Jacob F., 1982 - The Possible and the Actual
Exaptation, that is: redundancy and multiple use as the handmaidens of creativity
Stephen Jay Gould (New York, 1941-2002) was an American evolutionary biologist and historian
of science. Although he was a great scientist - he developed with Niles Eldredge, after years of
intensive studies in paleontology, the Theory of Punctuated Equilibrium in 1972 - he was known by
the general public mainly from his 300 popular scientific essays in the magazine Natural History,
and his books written for a non-specialist audience.
One of these essays, published in 1990 on the magazine Natural
History with the title An Earful of Jaw - collected with other essays in
the book Eight Little Piggies in 1993 and translated in 1994 as: Otto
piccoli porcellini - focuses on the evolution of the mammalian ear, an
organ, in the words of Darwin, of extraordinary complexity.
«For an optimal combination of fascination with excellent
documentation, no saga in the history of terrestrial vertebrates can
match the evolution of hearing. Two major transitions, seemingly
impossible but then elegantly explained, stand out at opposite ends.
First, at the inception of terrestrial life: How can creatures switch from
feeling vibrations through lateral lines running all over their bodies to
hearing sounds through ears? How, in other words, can new organs
arise without apparent antecedents? Second, at the last major innovation in vertebrate design: How
can bones that articulate the upper and lower jaws of reptiles move into the mammalian ear to
become the malleus and incus (hammer and anvil) in the chain of three bones that conduct sound
from the eardrum to the inner ear?
How, in other words, can organs switch place and function without destroying an animal’s integrity
as a working creature? How can we even imagine an intermediary form in such a series? You can’t
eat with an unhinged jaw. Creationists have used this difference between reptiles and mammals to
proclaim evolution impossible a priori: I mean, really, how can jawbones become ear bones? Get
serious! Yet, we shall see, once again, that the domain of conventional thought can be much
narrower than the capabilities of nature, although ideas should be able to extend and soar beyond
reality.
The key to the riddle of both these transitions lies in multiple modalities and dual uses.
You can pat your head and rub your stomach, walk and chew gum at the same time (most of us, at
least), feel and hear sound, chew and sense with the same bones. Nature writing in the lyrical mode
often exalts the apparent perfection and optimality of organic design. Yet, as I frequently argue in
these essays, such a position plunges nature into a disabling paradox, historically speaking. If such
perfection existed as a norm, you might revel and exult all the more, but for the tiny problem that
nature wouldn’t be here (at least in the form of complex organisms) if such optimality usually
graced the products of evolution. (...)
Mammals have three middle-ear bones-hammer, anvil, and stirrup, or stapes. And the stapes is the
homologue of the hyomandibular in fishes. In other words - but how can it happen? - a bone
originating as a gill support must have evolved to brace the jaws against the braincase, and then
changed again to function for transmission of sound when water ceded to air, a medium too thin to
permit “hearing” by the lateral line. As usual in a world of encumbrances, we must flush away an
old and conventional concept before we can understand how such an “inconceivable” transition
might actually occur without impediment in theory or practice. We must forget the old models of
horses and humans mounting a chain of improvement in functional continuity-from small, simple,
and not-so-good to larger, more elaborate, and beautifully wrought. In these models, brains are
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always brains and teeth always teeth, but they get better and better at whatever they do. Such
schemes may work for the improvement of something already present, for a kind of stately
continuity in evolution. But how can something original ever be made? How can organisms move to
a truly novel environment, with needs imposed for functions simply absent before? We require a
different model for major transitions and innovations, for King Lear was correct in stating that
“nothing will come of nothing.”
We need, in other words, a mechanism of recruitment and functional shift. Evolution does not
always work by enlarging a rudiment. It must often take a structure functioning perfectly well in
one capacity and shift it to another use. The original middle-ear bone, the stapes, evolved by such a
route, changing from a stout buttressing bone to a slender hearing bone.
If each organ had only one function (performed with exquisite perfection), then evolution would
generate no elaborate structures, and bacteria would rule the world. Complex creatures exist by
virtue of slop, multiple use, and redundancy. The hyomandibular, once a gill support, then evolved
to brace jaw and braincase. But this bone happens to lie right next to the otic capsule of the inner
ear-and bone, for reasons incidental to its evolution, can transmit sound with reasonable efficiency.
Thus, while functioning primarily as a brace, the hyomandibular also acquired other uses. (...).
Paleontological and functional evidence join the embryological data to construct a firm tripod of
support, giving this narrative pride of place among all transitions in the evolution of vertebrates by
combining strength of documentation with fascination of content. One theme stands as the
coordinating feature of this narrative (and of my entire essay): redundancy and multiple use as the
handmaidens of creativity. We might employ this theme to make an abstract prediction about the
character of intermediary forms in the fossil record. Contrary to creationist claims that such a
transition cannot occur in principle because hapless in-betweens would be left without a jaw hinge,
the principle of redundancy suggests an obvious solution. Modern mammals hinge their jaws
between squamosal (upper jaw) and dentary (lower jaw) bones; other vertebrates between quadrate
(upper jaw) and articular (lower jaw) bones destined to become the incus and malleus of the
mammalian ear. Suppose that mammalian ancestors, developed a dentary squamosal joint while the
old quadrate-articular connection still functioned-producing an intermediary form with a double jaw
joint. The old quadrate-articular joint could then be abandoned, as its elements moved to the ear,
while the jaw continued to function perfectly well with the new linkage already in place. (...).»
An Earful of Jaw (in: Gould S. J., 1993 - Eight Little Piggies)
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Since 1990 to the present, a lot of studies on mammalian ear evolution have been carried out by
paleontologists and biologists, and we can find several papers focusing on this argument, and many
popular scientific reports too, which refer about each improvement in the understanding of ear
ossicles evolution.
One of these reports, particularly effective for synthesis and clarity, is that proposed by the
paleontologist Hans-Dieter Sues in his blog:
An Earful of Jawbones
Posted by Hans-Dieter Sues of National Museum of Natural History on April 25, 2011
Hans-Dieter (Hans) Sues is a vertebrate paleontologist
based at the National Museum of Natural History in
Washington, D.C. He is interested in the evolutionary
history and paleobiology of vertebrates, especially
dinosaurs and their relatives, and the history of
ecosystems through time. A former member of the
National Geographic Committee for Research and
Exploration, Hans has traveled widely in his quest for
fossils and loves to share his passion for ancient life
through lectures, writings, and blogging.
«The middle ear of mammals contains a chain of three tiny bones (auditory ossicles), the hammer
(malleus), anvil (incus), and stirrup (stapes). This chain transmits and amplifies sound vibrations
from the eardrum to the inner ear. The eardrum (tympanic membrane) itself is stretched across an
additional bone, the ecto-tympanic. In all other land vertebrates, a rod-like stapes is the only bone
connecting the eardrum to the inner ear.
In 1837 the German anatomist C. Reichert, studying the development of the head in mammalian
embryos, first established that the malleus and ectotympanic were originally part of the lower jaw.
The malleus partially develops from a cartilaginous structure called Meckel’s cartilage. The joint
between the malleus and incus corresponds to the joint between the articular and quadrate, the
two bones that form the jaw joint in amphibians, reptiles, and birds. (Mammals evolved a new jaw
joint between the dentary and squamosal bones.) The questions of when and how many times
these elements became separated from the lower jaw during mammalian evolution have remained
unanswered until now.
The discovery, just published by Meng Jin (American Museum of Natural History, New York) and
his colleagues Yuanqing Wang and Chuankui Li (Chinese Academy of Sciences) in the scientific
weekly Nature, of an exquisitely preserved skeleton of a new 120-million-year-old mammal,
Liaoconodon hui, from Liaoning Province in northeastern China (Fig. 1), offers crucial new
evidence bearing on these questions. Liaoconodon belonged to an extinct lineage of mammals,
the Eutriconodonta, which were widely distributed and diverse during the Jurassic and Cretaceous
periods.
Figure 1.
Skeleton of Liaoconodon hui from the
Lower Cretaceous Jiufotang Formation
of Liaoning Province, China. Courtesy
of Meng Jin (American Museum of
Natural History). Overall length of
skeleton 35.7 cm.
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When Meng and his colleagues examined the skull of the new fossil they realized that its minute
ear bones were still preserved in their life position, connected to the lower jaw.
Liaoconodon and its kin are distinguished by the possession of an ossified Meckel’s cartilage (Fig.
2). In present-day mammals, a slender rod of cartilage, Meckel’s cartilage, forms early during
embryonic devel-opment. Subsequently, the single large bone (dentary) that forms the lower jaw in
mammals covers this rod. Most of the cartilage becomes resorbed, leaving only its back portion,
which turns into bone and becomes part of the malleus. In eutriconodonts, however, most of
Meckel’s cartilage became separated from the part of the malleus it formed and then turned into
bone in the adults. The ear bones became connected to this ossified cartilage.
Figure 2.
Three stages in the evolution of the ear bones in
mammals.
The Early Jurassic mammal
precursor Morganucodon still has its ear bones
fully connected to the lower jaw. Liaoconodon
shows further differentiation of the ear bones
while retaining a connection with the lower jaw.
Adult modern mammals have the ear bones
completely separated from the lower jaw.
Courtesy of Meng Jin (American Museum of
Natural History).
Figure 2.
Three stages in the evolution of the ear bones in mammals. The Early Jurassic mammal precursor
Morganucodon still has its ear bones fully connected to the lower jaw. Liaoconodon shows further
differentiation of the ear bones while retaining a connection with the lower jaw. Adult modern
mammals have the ear bones completely separated from the lower jaw. Courtesy of Meng Jin
(American Museum of Natural History).
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The superb preservation of the skeleton of Liaoconodon allowed Meng and his colleagues to trace
the separation between the two portions of the malleus. The front portion of the malleus, which is
not derived from Meckel’s cartilage, partially wraps around the ossified Meckel’s cartilage. The
ectotympanic contacts the malleus.
In modern mammals, the middle ear bones are attached to the skull, and researchers had long
sought the intermediate stage between this condition and that in the earliest mammals where the
ear bones were still part of the lower jaw. One suggestion for such an intermediate condition was a
persisting contact between Meckel’s cartilage and the malleus. Liaoconodon now provides the first
actual evidence of such a contact between the ossified Meckel’s cartilage and the bones of the
middle ear in an adult early mammal.
What functional role would the ossified Meckel’s cartilage in Liaoconodon have played? The
ectotympanic of Liaoconodon is completely separated from the skull and apparently only supported
part of the eardrum. By contrast, the ring-shaped ectotympanic is attached to the skull in presentday mammals and supports nearly the entire eardrum. Meng and his colleagues argue that part of
the eardrum in Liaoconodon would have been connected to the skull because the membrane has
to be stretched taut. The ossified Meckel’s cartilage would have held the malleus and ectotympanic
in place. Thus, it would have functioned as part of the ear, rather than of the lower jaw, even
though it was still connected to the jaw.
There has been a lively debate whether full separation of the middle-ear bones from the jaw took
place just once or perhaps more than once during the early evolutionary history of mammals. If this
change occurred only once in the common ancestor of mammals, the presence of an ossified
Meckel’s cartilage in Liaoconodon and some other early mammals would represent an evolutionary
reversal. This is possible because, based on modern developmental studies, such a reversal would
merely require slight changes in the timing of certain developmental events.
The alternative scenario is that the common ancestor of mammals retained Meckel’s cartilage
throughout its life. Complete separation of the ear bones from the lower jaw would then have
evolved independently in no fewer than three lineages of mammals - one leading to present-day
monotremes (echidnas and platypus), a second to a group of superficially rodent-like extinct
mammals known as multituberculates, and a third to the present-day marsupial and placental
mammals.
Meng and his colleagues favor the alternative scenario and argue that Liaoconodon and its kin
retained a transitional type of middle ear, which must have been more efficient in transmitting
airborne sound than the middle ear in the precursors of mammals because its ear bones were
already relatively smaller, the incus had greater freedom of motion, and the other ear bones were
separated from the lower jaw. The loose connection of the ossified Meckel’s cartilage to the lower
jaw and the contact between Meckel’s cartilage and the ear bones would have enhanced hearing
by separating it from feeding. However, the hinge joint between the malleus and incus and the still
incomplete suspension of the eardrum suggest that the middle ear of Liaoconodon was less
efficient in transmitting sound than that of present-day mammals.
The discovery of Liaoconodon fills in the last major gap in our understanding of one of the bestdocumented evolutionary transitions in the entire fossil record: the stepwise development of the
mammalian ear bones from bones at the back of the lower jaw in the precursors of mammals. As
my Smithsonian colleague John Burns put it so memorably in his Biograffiti, “With malleus
aforethought, mammals got an earful of their ancestor’s jaw.”»
http://voices.nationalgeographic.com/2011/04/25/an-earful-of-jawbones/
1,2
2
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Meng Jin , Wang Yuanqing & Li Chuankui , 2011 - Transitional mammalian middle ear from a new Cretaceous Jehol
eutriconodont. Nature, 472, 181: 185.
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2
Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA. Key Laboratory of Evolutionary Systematics of Vertebrates,
Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, P.O. Box 643, Beijing 100044, China.
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