Development Influences Evolution

A range of factors—including genetics and physics, location and timing-can either constrain an animaVs features or amplify changes

Katherine E. Willmore

In the animal kingdom, specifictraits distinguish one group of ani-

mals from another. The beaks andfeathers of birds, for example, setthem apart from mammals and am-phibians. Eurthermore, variations inthose traits differentiate one kind ofbird from another. Eor instance, duckshave long, wide and flat beaks, andgeese have shorter, thinner and tallerbeaks. Nonetheless, birds also sharemany features—eyes, feet, legs, a tailand so on—with many mammals andamphibians. What allows some traitsto vary so greatly, while other featuresremain relatively similar across a widerange of animals?

Some might say that a shared evo-lutionary history creates similarities,and adaptive responses to selectiveforces trigger differences. This answerprovides some insight, but it does notexplain all of nature's variation. Eorexample, similar ftaits can arise inde-pendently in different animal lineagesby a process called convergent evolu-tion. In convergent evolution, differentdevelopmental processes form similarstructures.

Many biologists point to the devel-opment of human and octopus eyes asan example of convergent evolution.Both eyes have an eyelid, iris, lens,pupil and retina, but they are formedby completely different mechanisms.The human eye is an extension of thebrain, whereas an in-pocketing of the

Katherine E. Willmore is a research associate inthe department of anthropology at PennsylvaniaState University. She earned her Ph.D. in medicalsciences in 2006 from the University of Calgary.Her research focuses on the evolution and develop-ment of the mammalian skull and face. She is alsoa freelance science writer and editor. Address: An-thropology Department, 409 Carpenter Building,Pennsylvania State University, State College, PA16802. E-mail: keiv20&psu.edu

220 American Scientist, Volume 98

iosphoto/Mafart-Renodier Alain/Peter Arnold

skin creates the octopus eye. Function-ally, these eyes differ as well. Our eyesreceive light through rod and conecells that point backward. In the octo-pus, rod and cone cells point forward.In addition, the focal length of the oc-topus lens is fixed; the octopus focusesby moving the entire lens relative tothe retina. In humans, changing theshape of the lens focuses the eye onobjects at varying distances.

This human-octopus example hintsat what can be learned from the fieldof evolutionary developmental biol-ogy, or evo-devo. Evo-devo is the studyof how developmental processes in-teract with selective forces to produceevolutionary change. In this context,development refers to the formationof physical traits and physiologicalsystems, from conception onward. Amajor focus of evo-devo is to deter-

Figure 1. Specific traits disfinguish animals. Among birds, for example, beaks come in manysizes and shapes. The roseate spoonbill (left) has a long, flat and wide beak, but a curlew's(upper right) is long and thin. On the other hand, a Leadbeater's ground-hornbill (lower right)relies on a robust bill that is relatively long and quite tall. Through evolutionary develop-mental biology, scientists can explore the constraints on animal traits, including bird beaks,as well as their history.

mine how development is constrainedor biased and to assess how that af-fects evolution. Although many evolu-tionary modificadons could arise, notall outcomes are equally feasible. Forinstance, some traits are not possiblein specific animals because of theirdevelopmental toolkit. Developmen-tal toolkits can be compared to Legobuilding blocks, because both dictatewhat can be built. A standard set ofrectangular LEGO blocks, for exam-ple, can serve as building material formany unique structures, but nothingwith truly rounded edges. In the sameway, an organism relies on limited de-velopmental processes, pathways andinteractions.

In this article, I highlight the rolethat development plays in the evolu-tion of the V ariety of natural forms. Anunderstanding of this developmentalrole reveals a set of rules that bias thedirection of evolutionary change, andthese rules help to demysfify the com-plexities of form that nature creates.

35 Shapes Fit AllEvery living animal fits one of 35distinct shapes, or body plans, all ofwhich originated in the Cambrianperiod around 500 million years ago.Because these new animal shapes ap-peared relatively rapidly, the event isreferred to as the Cambrian explosion.In this case, "rapid" is based on anevolutionary timescale; the explosionoccurred over a period of at least 5 to10 million years.

A common body plan often explainsmany of the similarides among differ-ent types of animals. For example, hu-mans are part of the phylum Chordata.All members of the Chordata share fourcommon traits at some point duringtheir development: a series of openingsthat connect the inside and outside ofthe throat; a bundle of nerve fibers thatruns down the back, connecting thebrain with other structures; a post-analtail (literally, a tail behind the anus); anda cartilaginous rod that supports thenerve cord. Humans share these physi-cal traits with amphibians, birds, fishand even sea squirts.

Even after many millions of years—10 dmes as long as the Cambrian ex-plosion itself—no new body planshave evolved, despite major changes,including the movement from living inwater to living on land. Consequent-ly, developmental processes mightconstrain the possibilides.

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human eye octopus eye

corneains ciliary

muscle

retina

opticnerve

Figure 2. Human and octopus eyes demonstrate convergent evolution, in which differentdevelopmental processes form similar structures. As shown here, both of these eyes—fromvery different organisms—consist of largely similar features: cornea, lens, retina and so on.This is even more compelling given that human and octopus eyes develop along completelydifferent pathways.

For one thing, structural constraintsimpede some forms. Consider the fic-tional King Kong, a scaled-up version ofa gorilla. AU of his proportions are thesame as a normal goriUa, but his overallsize is much larger. In real animals, thestructural properties of bone limit thesize and proportions of the creatures,especiaUy ones that Uve on land. Here'sa simplified mathematical explanationof Kong's impossibility based only onthe thigh bone, or femur

Let's say that King Kong is five timestaller than a normal-sized gorilla. Abone's strength depends on its cross-sectional area, which is a function of thesquare of its radius. King Kong's femuris five times bigger in all dimensions,including its radius, so its strength willbe increased by 5 ,̂ or 25. King Kong'svolume, on the other hand, varies withthe product of length and cross-section-al area, which means that it increases bythe product of 5 and 25, or 125. With thisgiant gorilla's weight increasing fivetimes more than his strength, his legswould be crushed. Such a discrepancybetween strength and weight wouldapply to the rest of Kong's body as weU.So apes could increase in size, but struc-tural constraints impose limits.

A Collection of ConstraintsElements beyond physics, such as theorganization of a genome, also con-

strain development. Certain genes andgene famiUes can be found in a widerange of animals and serve similarfunctions in different animals. For ex-ample, the Hox genes make up a well-studied set of these conserved genesthat have been identified in a varietyof animals including but not limitedto, frogs, fruit flies, humans, mice andworms. Hox genes help to set up ananimal's basic body plan, organizinghow structures get arranged along thebody from the head to the tail. More-over, the physical order of the Hoxgenes along the chromosomes corre-sponds to the order of the structuresof the body that they affect—startingwith genes that affect the head, thenthe thorax and then the abdomen. Hoxgenes are also arranged along the chro-mosome in the same order as the tim-ing of their eftects on body structures.That is, the genes in the complex thataffect the head are turned on first, fol-lowed by the genes that affect the tho-rax, and finally the genes that affectthe abdomen.

Beat Lutz, a physiological chemistat Johannes Gutenberg University inMainz, Germany, and his colleaguesdemonstrated the functional and spa-tial conservation of Hox genes be-tween fruit flies and chickens. Theseresearchers experimented with a genenamed labial, which is necessary for

proper head development. With thisgene turned off, flies die as embryos,but Lufz and his team showed thatthese flies can be rescued by placingthe labial gene in the proper place inthe embryo's genome at a specific timeduriiig development. Even more amaz-ing, Lutz and his colleagues added achicken version of labial to flies thathad labial turned off, and that manipu-lation rescued the flies with the sameefficiency as using the fly gene.

Although flies and chickens havemarkedly different heads, the geneticmachinery that drives part of theirhead development is sufficientlysimilar to allow swapping genes be-tween the two species. This similarityin genetic framework suggests thatsome aspects of the basic body planare constrained.

Beyond genetic constraints, sometraits depend heavily on other struc-tures. All structures are burdenedsomewhat in this way, because no traitexists in isolation. But some traits aremore heavily burdened than others.For example, the human vertebral col-umn supports the body, provides aplace for muscles to attach and servesas a conduit for nerve and blood sup-ply. If there is a change in the spine,then the structures that interact with itmust also change.

A process called canalization can alsoconstrain structures. This term camefrom the idea of depicting, for exam-ple, a structure on a landscape of pos-sibilities. If the desired structure lies ina valley, the surrounding ridges depictdevelopmental forces that confine thetrait and its development. Canalizationis one process that helps developmen-tal systems resist errors. For instance, ifa tissue develops from cells that mustcongregate in a specific location at aspecific time, a minimum number ofcells must migrate to that spot fromdifferent locations or the tissue will notdevelop properly. On the other hand,if the cells that did migrate properlydivided more quickly than normal,the increased division rate could cre-ate enough cells to meet the minimumrequirements, regardless of any prob-lems with migration.

Breaking FreeDespite the confining power of somedevelopmental systems, variations ap-pear. A mutation with a strong effector a drastic environmental change canoverwhelm the developmental con-

222 American Scientist, Volume 98

radius^ = strength

125-1King Kong

gorilla King Kong strength weight

Figure 3. Physical constraints make King Kong impossible. Imagine that King Kong (blue box) is five times bigger than an ordinary gorilla(yellow box), but with all proporiions maintained. Let's consider only King Kong's thigh bone, or femur. Like the rest of King Kong, his femur(left) is five times bigger than an ordinary gorilla's. Bone strength depends on cross-sectional area, which increases in King Kong by 5-, or 25.Weight, on the other hand, increases as the product of length and cross-sectional area, or 5 x 25 = 125. Consequently, King Kong's weight in-creases five times faster than his strength, and he would crush himself (right).

straints, driving a modification thatis so great that the rest of the systemcan't hide it. Moreover, one develop-mental change could even expose pre-viously hidden ones, or ones that hadbeen corrected or compensated for inthe past. Taken together, such devel-opmental changes might create vastlydifferent structures. In effect, canaliza-tion provides a cache of developmentalchanges that could be released undersome circumstances.

Suzannah Rutherford, a biologist atthe Fred Hutchinson Cancer ResearchCenter in Seattle, Washington, and hercolleagues elegantly demonstrated thisconcept in fruit flies by disrupting thenormal functioning of heat-shock pro-teins (HSPs), which exist in the cellsof every organism. HSPs help otherproteins assume or maintain theirproper shape, which is required forproper function. Under stressful con-ditions—such as exposure to a heatshock or other environmental Stressors,including toxins, starvation or infec-tion—some proteins unfold. The samestressful conditions, however, increasethe production of HSPs, which fix thedamaged proteins.

Drosophilaadult

Drosophilaembryo

head thorax abdomen

labialDrosophila Hox genes

Figure 4. Hox genes play a role in developing the body plan of many animals. As shown herein a fruit fly, the physical order of genes on the chromosome (bottom) dictates the order ofstructures in the embryo (middle) and, ultimately, the adult (top). For example, gene a (alsoknown as labial) appears first in the chromosome and the embryo, and it participates in theformation of the fly's head.

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\

Edd Westmacott/Alamy

Figure 5. Heterochrony, or changes in the timing of developmental events, explains some of the difference in appearance of a newborn kanga-roo (left) and human (right). Although a kangaroo is born at an earlier developmental stage compared with a human, the kangaroo needs theimmediate ability to feed from its mother in the pouch. At such an early stage of development, a human could never accomplish that task. Inthe kangaroo, accelerated production of neural crest cells pushes ahead the development of the facial features needed for this early feeding.

With high temperatures and muta-tions, Rutherford and her colleaguesdisrupted the normal functioning ofHSPs in fruit flies. This affected nearlyevery aspect of the flies—including theantennae, eyes, legs and wings—butnot directly. Instead, the disruptedHSPs could not do their usual job offnaintaining the shape, and therebyfunction, of the proteins involved inbuilding these structures. Mistakes inthe shaping of proteins can accumulatewithin cells because HSPs normallyfix the proteins before the impropershapes affect protein function in thedevelopment of structures. When HSPfunction is compromised, as it was inthese fruit-fly experiments, the build-up of changes in protein shape is re-vealed, leading to potential changes inform or function. Although the resultsare often extreme and are unlikely tobe advantageous, Rutherford's workshows how the mechanisms that helpto canalize a structure can also spawnchanges.

Evolutionary change can also arisefrom adjustments in developmentalFigure 6. Odontoehelys, the oldest knownfossil turtle, dates to about 220 million yearsago. Its lower shell, or plastron, was com-plete. As shown here, its top shell, or cara-pace, consisted of plates of bone along themiddle, but only ribs along its sides. Thispartial shell mirrors shell development insome turtles (see Figure 7).

timing. Heterochrony (based on theGreek hetero, or change, and chrono, ortime) describes a change in the timingof a developmental process. When thetiming of events relative to sensitivestages of development is shifted, radi-cally different structures can emerge.Marsupials, such as the kangaroo,provide an example of heterochron-ic change. Compared with placentalmammals—such as cats, dogs and hu-mans—marsupials are bom very early.At birth, a kangaroo looks more likea fetus than a newborn. The major-ity of a marsupial's development oc-curs in its mother's pouch. Therefore,even though marsupials are born rela-tively undeveloped, they must be ableto find the teat within their mother'spouch, attach to it and feed. At a simi-lar stage in development, a placentalmammal would not have the facialfeatures or motor skills necessary forthis task.

Kathleen Smith, an evolutionarybiologist at Duke University, and col-leagues discovered that newborn mar-supials can feed because the develop-ment of their facial muscles and bonesis accelerated compared to placentalmammals. Specifically, Smith found anearlier production of neural crest cells,which contribute to the developmentof many facial features.

In heterotopy—a combination ofthe Greek for change, and topo, or

224 American Scientist, Volume 98

carapaçial ridge and rib flattening

turtle embryo

forelimbcarapacial

ridge

hind limb

plane of cross-section

other amniotes

vertebrae-

rib

carapacialridge

scapula scapula

rib ossification

epithelialossifications

neural plate

costal plate

vertebrae

vertebraemarginal piafe

nuchal piafe nuchal plate dermal piafes

marginal plates

nuchal piafe

dermal piafes

nuchal piafe

cosfal plate —

marginal piafes

' neural plate

— marginal piafe

Figure 7. Turtle shell development starts with a carapacial ridge (CR) (a, red). As shown in cross section (relative to the dashed red line in a),the CR entraps the ribs, which get pulled to the side (b), unlike other amniotes in which the ribs grow forward, toward the breastbone (c). Asdevelopment continues, a turtle's ribs grow toward the sides even more (d and e). Then, dermal bones start to form around theEventually, the dermal bones fuse to form the complete shell (h).

place—change arises from a suite ofdevelopmental processes taking placein a new location. Relocation placesthe developmental structures in con-tact with others from which they arenormally separated. The result can bethe production of extra parts in a newlocation, such as an extra set of legs orwings, or entirely unique structures.

Tlie morphology of cheek pouches—structures that carry food—provide

an example of heterotopy. The cheekpouches of squirrels and many micerepresent the original condition. Theirpouches are found on the inside oftheir cheeks and are lined with mu-cus. These pouches develop from anin-pocketing of the skin on the insideof each cheek. Some other animals,including pocket gophers and kanga-roo rats, develop fur-lined poucheson the outside of their cheeks. In these

animals, the in-pocketing takes placecloser to the front of the face and al-lows for the skin of the lip to be in-cluded. In this more forward position,the developing pouch comes in con-tact with hair-forming cells, initiatingthe development of hair follicles in-side the pouch. Additionally, the for-ward placement of the pocket placesit in a new group of cells that follow adifferent growth pathway. These cells

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scapula

Figure 8. Scapula location (green) distinguishes a turtle (right) from a chicken (left), as well asall other vertebrates. The developmental events related to building a turtle's shell pull the ribs(blue) over the scapula, leaving them inside. In the chicken, the development of the ribs pullsthem into a semicircle from the spinal column to the breastbone, thereby leaving the scapulaoutside the rib cage. As this shows, one developmental change can trigger others, leading tosignificant differences in animals.

pull the fur-lined pocket so that it lieson the outside of the cheek. The sameprocesses are used to develop bothtypes of cheek pouches, but a slightdisplacement of the initial develop-mental steps lead to vastly differentstructures.

Every animal is a mixture of con-strained and unique features. There-fore, the development of an animalinvolves a combination of many of thedevelopmental phenomena describedabove. Turtles provide a great exampleof how these phenomena combine toproduce interesting structures.

Building a TurtleAlthough turtles have roamed theEarth for at least 220 million years,making them one of the most primi-tive animals, they possess several dis-dncdve features, including a shell anduniquely placed shoulder blades. Bothof these traits arise from simple tweaksof existing developmental programs.

In 2008, Chun Li of the ChineseAcademy of Sciences in Beijing andcolleagues described the oldest knownfossil turtle, called Odontochelys, whichdates to about 220 million years ago. InOdontochelys, the plastron—the part ofthe shell next to the belly—is completebut the carapace—the portion on theturtle's back—is incomplete. On thisturde's back, plates of bone developedalong the middle, but only ribs are evi-dent along its sides. This partial shellfits well with what is known aboutshell development in today's turtles.

Early in development, turtle embryosdevelop a bulge on both sides betweenthe limb buds, the stmctures that formthe front and hind legs. These bulgeslengthen along the sides of the turtleembryo, creadng a carapacial ridge (CR).Two embryonic dssues—mesenchymeand ectoderm—form the CR. Mesen-chyme is the embryonic precursor ofblood vessels, blood cells, bones, liga-ments and cartilage. Ectoderm givesrise to the brain and nerves, and to skinand other extemal features, includinghair, nails and scales. The CR consistsof a mesenchyme core with a thick ec-todermal covering. This arrangementof mesenchyme and ectoderm is foimdrepeatedly in animal development andis responsible for inidadng and organiz-ing the development of limbs and manyother structures.

In shell development, the CR trapsthe growing ribs. In all other tetra-pods, or four-limbed vertebrates, theribs grow from the spine to the breast-bone, thereby forming the rib cage. Inturtles, the ribs become ensnared inthe CR and are pulled to the side andinto the dermis, or the middle layer ofthe skin. Consequently, turtle ribs aresomewhat flattened out to the sides.This heterotopic placement of the ribswithin the dermis exaggerates thesideways growth of the CR and ribs.Moreover, a heterochronic growth rateof the dermis—side growth acceler-ated over front-to-back growth—am-plifies the movement of the ribs to theside. As a result, the embedded ribs are

pulled to the side faster than they cangrow toward the front.

The unique proximity of the ribs tothe dermis in turtles allows for anoth-er ectodermal (dermis)-mesenchyme(ribs) interaction. Initially cartilageforms the ribs, but through interac-dons with the CR, the cartilage is re-placed with bone. The new bone inthe ribs sends signals to the surround-ing skin that initiate further bone for-mation. These bones are called der-mal bones. Dermal bones continue togrow unHl they become fused witheach other and the underlying ribs.The heterotopic placement of the ribswithin the dermis allows for a newdevelopmental interaction, creatingthe bony carapace.

Although a turtle shell seems uniqueamong animals, dermal bones also de-velop in crocodiles and some amphib-ians and fish. The location of a turtle'sscapulae, or shoulder blades, makes upits truly unique aspect. In all other ver-tebrates, the scapulae lie on the outsideof the ribs, but they are on the inside inturtles. When the ribs get trapped inthe CR and are pulled to the side andthe back, they surround the scapulae.In all other vertebrates, the ribs growtoward the front of the body, leavingthe shoulder blades outside. The in-ward placement of the shoulder bladesin turtles represents a break from thecommon tetrapod body plan and is amajor evolutionary modification.

As turtles demonstrate, small chang-es early in development can triggerfar-reaching effects. Nonetheless, itwould be nearly impossible to predicthow a slight tweaking of a cell popu-lation—like the development of theCR—would create a completely dif-ferent skeletal arrangement and thedevelopment of a bony shell. To recre-ate the initial appearance of uniquestructures, we need specific details ofeach species' developmental programand information about intermediatespecies. This is yet another example ofwhat makes evoludon so complex—and so utterly fascinating.

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