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Embryonic Ideas

CARL LINNAEUS (1707–78), the father of modern taxonomy, studied hundreds of plants and animals during his lifetime. His scientific classifications left little room for sentiment—except in one case. Of the thousands of animals Linnaeus investigated, he reserved one in particular for scorn and derision. Kids know salamanders and newts as gentle big-eyed creatures with large heads, four limbs, and long tails. But Linnaeus, for some unknown reason, thought them such “foul and loathsome animals” that he proclaimed it fortunate that “the creator has not exerted his powers to make many of them.”

If Linnaeus saw salamanders as the nadir of creation, others claimed them to be elemental, almost magical, creatures. Philosophers from Pliny the Elder to Saint Augustine envisioned newts and salamanders as creatures born from lava, inferno, or flame. To Augustine, salamanders were physical evidence for the reality of damnation in fire. Augustine’s idea derives from the claim that salamanders were resistant to flames or able to spring forth from bonfires. These superpowers may have reflected their biology. As aquarists and aficionados know, some salamander species have an affinity for the rotting undersides of logs. These wet habitats were likely hidden from those who in Augustine’s day collected logs for firewood. When they ignited salamander-infused logs, they would have had some wiggly surprises that undoubtedly led to awe-inspired speculation about devilry.

While there are relatively few salamander species in the world, perhaps five hundred by some recent estimates, their relevance to the human condition lies well beyond visceral hatred, thoughts of damnation, and life emerging from fire. They have been a catalyst for a new approach to understanding the major transformations in the history of life.

In the 1800s zoological expeditions roamed the world exploring continents, mountains, and jungles. They described thousands of new minerals, species, and artifacts. Exploration vessels often had a naturalist on board whose job it was to collect and study the species, rocks, and landscapes that the ship encountered. The eminences of the day were the people who were in a position to analyze and publish on the specimens that arrived on the docks and at the train stations of London, Paris, and Berlin.

If ever a zoologist had a birthright, it was Auguste Duméril (1812–70), a professor at the Museum of Natural History in Paris. Like his father, André, also a longtime professor at the museum, he had a passion for reptiles and insects. Father and son did research together and collaborated to build a menagerie at the museum where they could observe living creatures in addition to preserved ones. Duméril Senior published an influential classification of the animal kingdom, using his son’s anatomical descriptions. When André died in 1860, Auguste set out with a vengeance to describe new species.

In January 1864 Duméril received a shipment of six salamanders from a collecting team who were exploring a lake outside Mexico City. The salamanders were large adults, and unlike any adult salamanders known at the time, they had a full set of feathery gills that extended like plumes of feathers from the base of the skull. The creatures even had a keel on their back that extended to a flipper-like tail. The implication was clear: with gills and an aquatic body shape, these adult salamanders lived in water.

Unknown to the explorers, the salamanders had long been part of Aztec culture. The species may have been new to science, but in Mexico they were a favored delicacy, often roasted for feasts and special rituals.

Prompted by Darwin’s newly proposed theory of evolution, Duméril thought that these aquatic amphibians might provide clues to how fish evolved to walk on land. He placed his new creatures in the menagerie that he and his father had built. Happily, he had both males and females, and after about a year, Duméril got them to mate and produce fertilized eggs. In 1865 the eggs hatched with perfectly healthy juvenile salamanders. Salamanders are easy to care for and, under the right conditions, do not require much food for long periods of time. All was going well with his charges, so Duméril left them alone.

Later that year he looked inside the enclosure. His first thought must have been that someone had fiddled with the cage, because there were now two kinds of salamanders inside. First, there were the parents, the big aquatic adults with gills. But there was another kind living right beside them. These others were also large but looked completely terrestrial, having no gills, no aquatic tail, nothing to suggest they could inhabit water. Looking closely at their anatomy, and comparing them to species already described in the scientific literature, Duméril realized the new creatures had been given a name by scientists years before. They had the exact traits of the genus Ambystoma, a well-known species of salamander that were fully land-living.

These animals were so different from each other that, to use Linnaeus’s scheme, they could be classified into two different genera, not just species. It was as if Duméril had put chimpanzees in an enclosure one year and returned the next to find both gorillas and chimps happily cohabiting the cage.

Had a new form of life appeared out of thin air? Had a major transformation happened in Duméril’s enclosure in Paris? What magic were salamanders revealing this time?

Developing Stories

For centuries people have looked at embryos with the intuition that somewhere inside the transformation from egg to adult lay clues to the laws that make species different from one another. Indeed, by the time Duméril was puzzling over his salamanders, the development of an embryo, whether of a fish, a frog, or a chicken, was seen as a lens through which to view the biological diversity of every single animal on Earth.

Ever since Aristotle peered inside their eggs, chicken embryos have been objects of fascination. Chicks come in their own container that can be opened much like a window. You can cut a hole in the shell, slide a light along the side of the egg, and pop it under a microscope to see the embryo inside. The embryo begins as a small clump of white cells sitting directly on top of the yolk. Over time it grows, and recognizable landmarks gradually emerge—head, tail, back, and limbs. The process feels like a well-scripted dance. At the very beginning, the fertilized egg undergoes division—one cell becomes two, two become four, four become eight, and so on. As the cells multiply, the embryo eventually becomes a ball of cells. Over a few days the embryo transforms from a hollow ball to a simple disk of cells surrounded by structures that will protect it, provide it with nutrition, and create the right environment for it to develop. From this simple disk of cells emerges an entire creature. No wonder embryonic development has been a source of speculation and scientific investigation.

Charles Bonnet (1720–93) argued that the embryo was, in essence, a small but fully formed miniature being. Its time in the womb was spent growing organs that already existed. These “homunculi,” as they were called, were the basis for his view of evolution. Females carried all future generations inside them. The homunculi they carried were able to survive catastrophes, and over time new forms of life would spring de novo from preceding generations of females. The final stage, sometime in the future, would see angels sprout from homunculi in human wombs.

In the century that followed, diverse kinds of embryos were brought to the lab, and new optical technologies were employed to examine them. While Bonnet’s idea perished in the face of scientists seeing real embryos, the quest to explain how creatures as different as elephants, birds, and fish are built remained alive.

In 1816 two medical students were among the first to uncover deep insights about biological diversity inside embryos. Both Karl Ernst von Baer (1792–1876) and Christian Pander (1794–1865) were from noble families in the German-speaking regions of the Baltics. Entering medical school in Würzburg, they took a cue from Aristotle and began to look at chicken embryos. Pander incubated thousands of eggs, opened them at different times of development, and put the embryos under a magnifying glass to see how organs formed. He had a distinct advantage over his friend in these early days: coming from a wealthy family, he could afford to build racks to hold thousands of eggs, hire an assistant to draw the embryos, and commission high-quality engravings for publication. Lacking Pander’s wealth, von Baer was relegated to the sidelines.

Technological advances worked in Pander’s favor—he was able to obtain top-of-the-line magnifying glasses to zoom in on tissues and cells. With an abundance of embryos of different ages, and new lenses with which to view them, he encountered something that no human had ever seen. Embryos in their earliest stages had no recognizable organs; least of all were they the homunculi that Bonnet envisioned. In early stages, embryos did not look like adults, being simple disks of cells sitting on top of the yolk.

Pander wasn’t interested only in the external shape of the embryos—he wanted to see what was going inside. Focusing in, he noticed that an embryo started off as a simple disk the size of a few grains of sand. Getting larger through the course of development, the disk eventually became composed of three layers of tissue, set like sheets one atop another. The embryo at this stage looked something like a disk-shaped cake with three layers.

With thousands of eggs at his disposal, Pander traced what happened to each of those layers as the chick embryos developed and grew from a simple three-layered disk to an adult chicken with head, wings, and legs. He watched organs emerge gradually.

Working under the magnifying glass, and making detailed drawings of every possible stage of development, Pander saw a simple unifying concept in this complex process. The entire organization of the body broke down to these three layers. The inner layer eventually gave rise to the organs of the guts and the glands associated with them. The middle layer transformed to become bones and muscles. And the outer later became the skin and nervous system. To Pander, and to von Baer, who was a friendly spectator to these discoveries, these three layers were an essential organizing principle of the emerging body of the chicken.

Von Baer had a hunch that there were even more insights to come from these layers. Unfortunately, lacking funds, he was unable to do research of his own until a decade later, when he took a professorship at the University of Königsberg. With the income from his new position, he was now able to explore the vast unknown about embryos of different species. His passion occasionally led him astray. To demonstrate the organ that gave rise to mammalian eggs, he sacrificed his director’s pet dog. While von Baer is forever associated with the discovery that mammalian eggs come from the follicles in the ovary, lost to history is how the director felt about his experimental methods.

Von Baer asked: What are the mechanisms at work that make one kind of animal different from another? He collected embryos of as many species as he could find, from fish to lizards to turtles. Extracting the embryos from their eggs or wombs, he would keep them in vials with alcohol as a preservative. Then, like his friend Pander before him, he began to see what was common to all animal development and what made each species unique.

Viewing all the different species under the magnifying glass, he made fundamental observations about animal diversity. Every single species began development with three layers: an inner one, an outer one, and a middle one. And as he traced the layers, he found that their fates were exactly the same. The cells of the deepest layer, at the base of the disk, became the organs of the guts and glands associated with them. The middle layer became the kidneys, reproductive organs, muscles, and bones. The outer layer became organs of the skin and nervous system. Pander’s original discovery was not only about chickens—it held for animal life more broadly.

This simple observation revealed a universal connection between every organ in every known animal species. Whether the creature is a deep-sea anglerfish or a soaring albatross, its heart comes from cells of the middle layer, its brain and spinal cord from the outer one, and its intestines, stomach, and digestive organs from the inner one. This rule is so fundamental that if you pick any organ in the body of any animal on Earth, you can know which cell layer built it.

Then von Baer made a mistake. He forgot to add labels to a few of the vials that housed different species. Not knowing which species were in which vials, he had to look closely to try to differentiate them. In describing the unlabeled embryos, von Baer said, “They may be lizards, small birds, or very young mammals. The formation of the heads and trunks in these animals is quite similar. The extremities are not yet present in these embryos. But even if they were in the first stages of development, they would not indicate anything; since the feet of lizards and mammals, the wings and feet of birds, as well as the hands and feet of men develop from the same fundamental form.”

With his labeling mishap, von Baer saw an order to animal life that unfolds as development continues. Adult bodies often mask profound similarities in early development. While the adults, or even neonates, can look extremely different, in their earliest stages of development they are very similar.

These embryonic similarities run very deep even in their details. The head of an adult fish has few apparent resemblances to that of an adult turtle, bird, or human. But a short time after conception, all these embryos have four swellings that lie at the base of the head. These so-called gill arches, which have a cleft between them externally, develop in any creature that will have a bony skull. Indeed, their presence forms the baseline for the development of different types of skulls. In fish, the cells inside the swellings become the muscles, nerves, arteries, and bones of the successive gills. The clefts that separate the swellings become the gill slits. Even though people don’t have gills, we have the swellings and clefts in our embryonic stages. In us, the cells of the swellings become the bones, muscles, arteries, and nerves of parts of the lower jaw, middle ear, throat, and voice box. The clefts never become full slits but seal over to become parts of our ears and throats. We have them as embryos, not as adults.

Example after example—from kidneys and brains to nerves and backbones—made von Baer’s case potent and enduring. Sharks and fish have a connective tissue rod running from head to tail underneath the spinal cord. Filled with a jelly-like substance, it forms a flexible support for the body. A human’s backbone is composed of vertebrae, blocks of bone separated from one another by intervertebral disks. No rod runs from our head to our hips. Yet our embryos have a fundamental similarity to those of sharks and fish: they have that rod. During development, it breaks up into small blocks that eventually become the inner part of our intervertebral disks. If you’ve ever ruptured a disk, a painful trauma, you have injured this ancient remnant of development we share with sharks and fish.

Von Baer’s observations about the similarity of early-stage embryos of different species caught Darwin’s eye. Von Baer’s work was published in 1828, and Darwin was aware of it three years later, when he departed on the HMS Beagle for his life-changing trip around the world. When he published On the Origin of Species three decades later, he offered embryos as evidence for his theory of evolution. To Darwin, the fact that creatures as different as fish, frogs, and people had a common starting point meant they shared a common history. What could be better evidence for the common ancestry of different species than common embryonic stages in development from which they sprang?

Following von Baer’s discoveries with embryos, the German scientist Ernst Haeckel (1834–1919), a generation after von Baer, explored a link between embryonic stages of development and evolutionary history. Haeckel trained to become a physician, but he couldn’t tolerate seeing sick patients, so he went to Jena to study with a leading comparative anatomist. His life changed when he read and met Charles Darwin.

Haeckel scoured the animal kingdom for embryos and produced more than one hundred monographs describing and illustrating embryonic stages of diverse species. He envisioned a seamless connection between art and life: the diversity of life was a form of art to him. He produced some of the most beautiful color lithographs ever made. His voluminous renderings of corals, shells, and embryos reflect an age when careful anatomical drawing bridged science and aesthetics. Embryos in particular were celebrated not only for their beauty but for the way they connected to Darwin’s new theory. Haeckel, always quotable, coined a phrase linking the two that was to linger like an advertising jingle for many who studied biology in the twentieth century: “Ontogeny [development] recapitulates phylogeny [evolutionary history].”

Haeckel’s claim was that animal embryos, as they develop, track the creature’s evolutionary history: a mouse embryo looks successively like a worm, a fish, an amphibian, and a reptile. The mechanism that produces these stages lies in the way new features arose in evolution. He proposed that new evolutionary features were added to the end stages in development; for example, amphibians arose by adding amphibian-specific features to the end stages of the development of a fish ancestor, reptile features to those of amphibians, and so on. Over time, according to Haeckel, this process resulted in embryonic development tracking evolutionary history.

Haeckel’s comparison of embryonic development of different species. This was an influential yet controversial figure. Some argued that he overemphasized the similarities among embryos and took liberties with his diagrams.

Who needed intermediate fossils to trace life’s history if, as Haeckel supposed, it could be read in embryos? Haeckel’s notion was so influential that it launched people on expeditions to obtain embryos of different species. On one of these expeditions, Robert Falcon Scott’s 1912 Antarctic expedition to reach the South Pole, three members became consumed with the search for emperor penguin eggs. The explorers thought that the embryos of emperor penguins, which were considered primitive at the time, would hold clues to how birds arose from reptiles. Somewhere in their embryonic development would be a stage that looked like their reptilian ancestor.

In the middle of an austral winter, the three crew members departed on a monthlong sledge trip from their base to Cape Crozier, where the penguins had their rookery. In pitch-darkness, with temperatures dropping to minus sixty degrees Fahrenheit, the three nearly died several times when their tents blew away or when they slipped into crevasses. One of them, Apsley Cherry-Garrard, wrote in his classic travelogue, The Worst Journey in the World, that the team managed to return to camp with three penguin eggs. The expedition later lost Scott and four crew members, including two of Cherry-Garrard’s compadres from the penguin trip, in their tragic and failed attempt to reach the pole. Afterward Cherry-Garrard returned to Britain and tried to deliver the eggs to the British Museum. The museum made him wait in the hall for several hours as they decided whether to accept the eggs. Reluctantly, they took them, but as Cherry-Garrard wrote to the museum head later, “I handed over the Cape Crozier embryos, which nearly cost three men their lives and cost one man his health….Your representative never even said thanks.”

Apsley Cherry-Garrard (right) after returning from his worst journey to get penguin eggs

The reason the museum was reluctant to accept the eggs was that in the interval between the expedition’s departure for the pole and Cherry-Garrard’s return, Haeckel’s recapitulation theory had been widely discredited and, in addition, the supposed primitive nature of penguins had been challenged by new discoveries. Haeckel had stirred such interest in embryology that he sowed the seeds for his own downfall. Eager to find evolutionary history in embryos, scientists studied embryonic development in diverse species. For the most part, von Baer’s idea of a similarity among embryos of different species held up, albeit with some exceptions. But the new data didn’t support Haeckel’s recapitulation theory; in fact, it did quite the opposite. At no stage of embryonic development could an ancestor be seen. Human embryos may look in some ways like fish embryos, as von Baer suggested, but never in their development do they look like one of our ancestors, whether it is a fish with legs or an Australopithecine; nor does a bird embryo look like Archaeopteryx during its development.

Haeckel’s idea was wrong, but it guided the research of countless scientists. It lingers even in some quarters today, despite the fact that it has not been a topic of scientific inquiry for over a century. Perhaps Haeckel’s most lasting influence was on the person who loathed his idea the most.

The Axolotl

Walter Garstang (1868–1949) so despised Haeckel’s idea that he developed a critique that led to a new way of thinking about life’s history. He had two lasting, if eccentric, pursuits—tadpoles and verse. When he wasn’t doing science on larvae, he was writing limericks and jingles about them. His passions came together in a book published two years after his death, Larval Forms and Other Verses, where he transformed a career of scientific research into poetry.

“The Axolotl and the Ammocoete” may not sound like a promising title for verse: it refers to a salamander (axolotl) and a tadpole-like animal (ammocoete). But the idea expressed in the poem changed the field and defined research programs for decades. Garstang’s notion explains not only what happened in Duméril’s magical enclosure but also some of the revolutions that made our own presence on this planet possible. To Garstang, larval stages weren’t simple detours of development; they were rich with artifacts of the history of life and potential for its future.

Most salamanders live in water for much of their development on the undersides of rocks, on fallen branches in streams, or at the bottom of ponds. Their larvae hatch with a wide head, small flipper-shaped limbs, and a broad tail. A cluster of gills projects from the base of the head like a bunch of feathers extending from the shaft of a feather duster. Each of the gills is broad and flat, maximizing the surface over which it can take up oxygen from the water. With their finlike limbs, broad flipper-like tails, and gills, these creatures are clearly built for life in water. Axolotl larvae are born with very little yolk in the egg, meaning they must feed voraciously if they are to grow and develop. The broad head serves as a huge suction funnel: when they open their mouths and expand their gapes, water and food particles get pulled inside.

A portrait of Walter Garstang that appears at the beginning of *Larval Forms and Other Verses*

Then, at metamorphosis, everything changes. The larvae lose their gills and reconfigure the skull, limbs, and tail, changing from an aquatic creature into a land-living one. New organ systems allow the creatures to inhabit a new environment. Feeding is different on land from in water. The head structures that were so useful in sucking prey into the mouth in water don’t work in air. So the creatures reconfigure their skulls to allow their tongues to flop out and pull in their prey. A simple switch affects the entire body—gills, skull, circulatory system. The shift from water to land, something that happened over millions of years in our own fishy past, happens over a few days of metamorphosis in these creatures.

After encountering these striking changes to the salamanders in his menagerie, Duméril traced their entire life cycle. These salamanders—the axolotls of Garstang’s verse—normally metamorphose from aquatic larvae into terrestrial adults. But, as Duméril later found, they don’t always—they have two different pathways, depending on the environment they experience as larvae. Salamanders that grow in a dry environment will undergo metamorphosis and proceed to lose all their aquatic traits to become terrestrial adults. Those reared in wet environments never undergo metamorphosis and grow to look like big aquatic larvae, with a full set of gills, a flipper-like tail, and a wide skull best suited for feeding in water. Unknown to Duméril at the time, the specimens he obtained from Mexico were big adults that did not undergo metamorphosis because of their wet habitat. Their offspring, which developed in the dry menagerie, underwent metamorphosis and lost all their aquatic larval traits in the process.

The magic that happened in Duméril’s enclosure was a simple shift in the ways animals develop. We now know that the major trigger for metamorphosis is a spike in the levels of thyroid hormone in the bloodstream. The hormone triggers some cells to die, others to proliferate, and still others to transform into different types of tissues. If the levels of hormone stay flat, or if the cells cease to respond to it, then metamorphosis will not happen, and the creatures will keep their larval features into adulthood. Changes in development, even small ones, can produce coordinated modifications of the entire body.

Picking up on Duméril’s work, Garstang promoted a general principle: small changes in the timing of development can have huge consequences for evolution. Let’s say there is an ancestral sequence of developmental stages. If development is slowed or stopped early, then the descendants will look like juveniles of their ancestors. In salamanders, this alteration would cause their bodies to look like aquatic larvae, retaining external gills and having limbs with fewer fingers and toes. Alternatively, if development is extended or sped up, new exaggerated organs and bodies emerge. Snails develop their shells by adding whorls during development. Some snail species have evolved by extending the time of development, or by developing faster. These descendant snails have a larger number of whorls than their ancestors. The same kind of process explains a wide variety of large or exaggerated organs, whether the antlers of elk or the elongated necks of giraffes.

Salamanders can slow or stop their development and change their bodies dramatically.

Tinkering with embryonic development can make dramatically new kinds of creatures. Ever since Garstang, scientists have generated taxonomies of the ways developmental timing can be altered to produce evolutionary changes. Slowing the rate of development is a different process than terminating it early; each mode can produce similar outcomes—juvenilized descendants—but the causation is different. The same relationship between causation and outcomes holds for the process that can produce exaggerated or larger features when development is sped up or extended.

In searching for different causes, scientists have probed for genes that may control these events or for hormones, such as thyroid hormone, that may trigger them. This approach to development and evolution, known as heterochrony (from the Greek hetero meaning “other” and chronos meaning “time”), has become its own subfield of research. In more than a century of comparing embryos and adults of diverse species, zoologists and botanists have shown how changes in the timing of developmental events can make new kinds of bodies in animals and plants.

Garstang himself revealed one stunning example from our own history—when our ancestor was a worm.

The Ammocoete

Garstang’s poem “The Axolotl and the Ammocoete” explored two of the most classic revolutions that happened by retaining larval features in the course of evolution. The axolotl shows the extent of changes that occur when development is stopped early. The larva, a transitory stage in the life of a salamander, becomes the endpoint of development. The ammocoete is a small wormlike animal with a backbone. While it may live by quietly sucking mud at the bottom of rivers and streams, its biology tells a much larger story.

Over two thousand years ago, Aristotle identified and described hundreds of species of snails, fish, birds, and mammals. He distinguished animals with blood inside (enhamia) from those without (anhamia). This distinction broadly correlates to what we recognize today as vertebrates and invertebrates. There are two kinds of animals on the planet, those with backbones and those without them. The bodies of people, reptiles, amphibians, and fish are fundamentally different from those of flies and clams. At the core of vertebrate architecture is what von Baer saw in fish, amphibians, reptiles, and birds: every vertebrate at some stage of its embryonic development has gill slits, a cartilage rod that supports the body, and a nerve cord running above it. As we’ve known since von Baer, some of these traits may be obscured or lost in the adult body, but they are present at an embryonic stage. The speculation has been that the ancestor of vertebrates was a simple wormlike creature that had these three features.

For Garstang and many of his contemporaries, the key question was how this body plan came about. Were there invertebrate animals that had these traits in some form? If so, how did our branch of the tree of life evolve from them? Earthworms don’t have gill slits or the cartilage rod in either their embryos or adults. Nor do insects, clams, starfish, or most any other animal without a backbone. The answers came from a most unexpected animal, one that is shaped like a lump of ice cream and spends almost its entire life attached to rocks in the ocean.

There are about three thousand known species of sea squirt in the world’s oceans. With some species shaped like a scoop of ice cream topped by a large chimney-shaped structure, they sit, sometimes for decades, attached to the rocks beneath the surface, simply pumping water. Water gets pulled into a big tube at the top and goes through the body, only to be expelled by a tube that projects from the center of body. As water travels through their bodies, they filter particles out to feed. Sea squirts take any number of shapes, from clumps to twisted tubes, but they have no obvious head, tail, back, or front. You could not imagine a creature less likely to tell the story of one of the most basic events in human history.

Garstang was interested in their larvae. He explored something remarkable, first seen by Russian biologists in the late 1800s: when sea squirts hatch from the egg, they are free-swimming tadpoles. Not until metamorphosis do they sink to the bottom of the water column and attach to rocks. If there is any tadpole that could capture the imagination, this is it. It swims about looking nothing like the adult. With a big head, it maneuvers by flexing its long tail back and forth. Inside the body a nerve cord runs along the animal’s back, and a connective tissue rod extends from head to tail. It even has gill slits at the base of the head. The three great features that are the basis for the putative ancestor of animals with backbones are present in the larval sea squirt.

Then larval sea squirts lose it all, or at least the features that from our anthropocentric viewpoint are important. After a few weeks, the tadpole swims to the bottom of the water column. As it descends, it loses the tail, the nerve cord, and virtually all of the connective tissue rod; it modifies the gill slits to become part of the pumping apparatus. It attaches to the rocks to spend the rest of its days in one place pumping water. A tadpole, a creature with our vertebrate body plan, transforms into something that has been mistaken for a plant.

A sea squirt looks like an amorphous lump but begins its development with many traits that we share.

Garstang proposed that a shift in the timing of development was a first major step in the transition from invertebrate to vertebrate. An adult human or fish has no resemblance to a sea squirt; many would find the comparison insulting. But its larvae contain the essence. The ancestor of all vertebrates came about by stopping sea squirt development early, freezing the traits of the larval stage, and letting the creature grow to adulthood with them. The result was an adult that looks like a tadpole of its sea squirt ancestors. This creature, with the nerve cord, connective tissue rod, and gill slits, in a freely swimming animal, would become the mother of all fish, amphibians, reptiles, birds, and mammals.

A Picture of Change

Examples of evolution occurring as a result of changes in the timing of developmental sequences abound; it is hard to pick up certain scientific journals nowadays and not see papers on it. Arguably one of the most seminal examples is also one of the most personal.

The years spanning 1820 and 1930 were an age of big ideas in biology. Von Baer, Haeckel, Darwin, Garstang, and countless others looked to anatomy, fossils, and embryos for rules to explain why animals appear the way they do. At the same time, the mechanisms that brought about the diversity of life were becoming known.

In this intellectual milieu, the Swiss anatomist Adolf Naef (1883–1949) rose through the academic ranks, studying with some of the leading lights of the day in Switzerland and in Italy. His goal, as he described it to his brother in 1911, was to formulate “a general science of the form of organisms, a subject on which I have a number of new ideas.”

Naef was a meticulous anatomist who knew the impact a good picture or image could have in making a scientific argument. His life, however, was defined in many ways by argument. As he wrote to his brother, “My demeanor alienates most people; some appreciate me all the same, others will have to accept me as pure intellect. I expect enemies rather than friends.” In an earlier letter, he asserted that “there exists in Switzerland no abundance of first-rate intellects which is what I take myself to be.” With this type of attitude, Naef was never able to find employment in Switzerland, so he spent most of his career at a post in Cairo.

While in Cairo, Naef developed a theory of biological diversity that reflected the philosophy of Plato two thousand years before. In his Republic, Plato held that all physical objects were but physical manifestations of ideal essences, the timeless universals that underlay all diversity. The diversity of all objects, from drinking cups to houses, could, to Plato, be boiled down to a metaphysical essence from which each physical manifestation was derived. Naef applied this idea to biological diversity. In his idealistic morphology, as it became known, animals, too, have an essence within their physical diversity. And for Naef, this essence was seen in similarities among animals during embryonic development.

Naef’s theoretical framework has largely been forgotten, replaced by new data from genetics and evolutionary relationships. His most enduring contribution is, fittingly, one of the images he used in making arguments for his failed theory. The photo shows a neonate chimpanzee and an adult. Struck by the large cranial vault, erect head, and small face of the young chimp, Naef proclaimed that “of all animal pictures known to me, this is the most manlike.” He was trying to show how the essence of humanity appears in early development. His theory may have been wrong, but this picture was so influential, it continued to catalyze research decades after its initial publication in 1926.

Naef’s influential photo comparing a juvenile with an adult chimp. The juvenile, likely a taxidermy specimen, is depicted to emphasize its human proportions and posture.

Adult humans have smaller brow ridges than adult chimpanzees, larger brains relative to body size, more delicate skull bones, smaller jaws, and different skull proportions. But in each of these features, humans are more similar to juvenile chimps than they are to adult chimps. Development also appears to have slowed, as humans have a longer gestational period and childhood than do chimps. By developing more slowly, humans retain many of the proportions and shape of the juveniles of our ancestors, which, as Naef showed, are so very human in many ways.

This notion became a lens through which to view much of human evolution. Paleontologist Stephen Jay Gould and anthropologist Ashley Montagu later observed that essential components of humanity could emerge simply by tinkering with rates of growth and development: couple proportionately large brains for our body size with an extended childhood rich in opportunities to learn, and much of what makes us special may relate to modifying developmental timing. While this explanation of human evolution is simple and elegant, new comparisons reveal that the story is more than an overall slowdown of development. Some human features look like those of juvenile chimps, but others, such as the shape of the legs and pelvis that enable humans to walk on two legs, do not. One hypothesis is that different parts of the body evolve by developing at different rates, the skull evolving by slowing its rates of development while legs and bipedality do the opposite.

Using these and other ideas from anatomy, D’Arcy Wentworth Thompson (1860–1948) postulated a mathematical approach to understanding biological diversity. His goal was to reduce the differences in shape among creatures to simple diagrams and equations.

D’Arcy Thompson’s grids show how changes in proportion can account for many differences in the shape of skeletons, as in this case of humans and chimps.

Written during the First World War, his book On Growth and Form spawned many an anatomy career, with its diagrams that were as simple as they were influential. Place a Cartesian grid over the skulls of a baby chimpanzee and a baby human, making the lines go through similar points in each. Then do the same for the adult skulls, making the grid lines go through the same locations that they went through in the babies.

The result is that the neat grid lines in the neonates become warped in the adults, and the deformation reflects changes in shape. This depiction reveals that during growth, the chimpanzee and human begin with relatively similar proportions, but then the chimp’s cranium shrinks in relative size while the lower face and brow ridges expand. In humans, the cranium expands while the face expands only moderately. In Thompson’s view, differences between humans and chimps result less from new organs than from shifts in proportions of different parts of the body, much like those produced by slowing down or speeding up rates of development.

One Cell to Rule Them All

Altering the timing of events is but one way of making evolutionary changes by tweaking embryonic development.

Ever since the days when Pander studied embryos under a magnifying glass, we’ve known that the development of diverse body parts is often highly coordinated. A simple shift in the working of a single cell, or a handful of them, could cause alterations to many parts of the adult body. The effect can be seen even in the names we give developmental maladies. Hand-foot-genital syndrome, for example, is a genetic mutation that affects the behavior of cells early in development. That single change affects the size and shape of the fingers, the configuration of the feet, and the tubes that carry urine from the kidneys. With such wide-ranging impacts from small alterations, changes in the kinds of cells that build bodies may hold clues to some of the revolutionary changes we see in history.

To understand this way of evolving, we need to return to sea squirts. As Garstang showed, and as recent DNA evidence has confirmed, one crucial step in the transformation from invertebrate to vertebrate occurred when larval features of sea squirts were retained to make a vertebrate ancestor. This tadpole-like adult had the basic architecture upon which the vertebrate body is built. But there was another step in the origin of vertebrates.

Vertebrates such as humans and fish are not simply larval sea squirts. From the bony skeletons that support the body, to the fatty myelin sheaths that surround nerves, to the pigment cells that lie in skin, all the way to the nerves that control the muscles in the head, vertebrates have hundreds of features that invertebrates do not. A list of all the differences between invertebrates and vertebrates would include organs and tissues from head to tail. Clearly more than changes in the timing of developmental stages was involved with this transformation.

Raised by a mother who was widowed soon after her birth, Julia Barlow Platt (1857–1935) was a biology prodigy. After graduating from the University of Vermont in three years, she attended Harvard University, where she dove in to study the embryos of chicks, amphibians, and sharks. True to her talent and ambition, she set an audacious goal for herself. The head is arguably the most complicated part of the body; not including teeth, the human skull has almost thirty bones, and there are more in the skulls of fish and sharks. The head’s anatomical complexity derives from the fact that these structures are supplied by a tangle of special nerves, arteries, and veins that are situated in a relatively small container. Platt traced adult structures, such as jaws and cheekbones, to their earliest embryonic stages. Perhaps by studying how skulls develop, she could distill essential similarities hidden in the adult body. Whether she knew it or not, she was entering one of the most contentious areas of science.

The academic climate of the time was not friendly to women pursuing higher degrees. After struggling at Harvard, Platt found a more open culture in Europe and entered a graduate program in Germany. Thus began a nomadic existence that would take her across Europe to the Marine Biological Laboratory in Woods Hole, Massachusetts. There Platt met O. C. Whitman, the director of the marine lab, and she followed him to the University of Chicago, where he was later to become chair of the zoology department.

In Whitman’s freewheeling lab, ambitious young scientists were treated as junior colleagues and could follow their own leads for research. In this setting, Platt thrived. Using specimens she collected at Woods Hole and techniques Whitman taught her in Chicago, she looked at head formation in salamanders, sharks, and chicks. Her reason was as much technical as anything else: these creatures have big embryos that develop inside an egg, making them easy to see and manipulate.

With Whitman, she developed a laborious but accurate method to trace cells during development. Her starting point was the three embryonic layers that Pander and von Baer had discovered in the 1820s. By the time of Platt’s work these three layers were taken almost as a biological axiom: cells of the inner layer form guts and associated digestive structures, the middle layer the skeleton and muscles, and the external layer the skin and nervous system. Platt noticed that the cells of the outer and middle layers differed in size and in the number of granules of fat inside. Using this distinction as a marker, she traced small groups of cells from each layer to see where they ended up in the skull. This approach allowed her to see which head structures came from which layer.

According to the dogma of the time, all the bones of the salamander skull should have come from the middle layer. But Platt’s fat granules showed her something else altogether. Some of the bones of the head, even the dentine of the teeth, were coming from the outer later, which supposedly was restricted to becoming skin and nervous tissue. To some, this finding was heresy. Leading researchers set themselves in opposition to her. One prominent scientist wrote, “An examination of a number of series and stages has not enabled me to find the slightest evidence in favor of Miss Platt’s conclusions.” This was just one voice in a chorus of criticism, which, for a young female researcher in the 1800s, could end a career before it started.

Fortunately for Platt, Anton Dohrn (1840–1909), the influential leader of the Stazione Zoologica in Naples, picked up on her research idea. He was originally skeptical of her discovery, but her careful analysis persuaded him to use her markers to study development in sharks. He wrote, “I fully agree with the views that we owe to Miss Platt….It goes without saying that I also make this conversion and now oppose all critical papers and remarks directed against Miss Platt’s findings.”

In Platt’s time, there was little room for women on science faculties, particularly individuals who spouted notions that confronted entrenched orthodoxies. Not being able to find employment in science, she moved to Pacific Grove, California, to set up her own small research group. Still making discoveries, she wrote to David Starr Jordan, president of the newly formed Stanford University. Desperate for a job in science, and knowing she had made fundamental breakthroughs, she ended her letter saying, “Without work, life isn’t worth living. If I cannot obtain the work I wish, then I must take up the next best.”

Unemployed and feeling unemployable in science, Platt left the field. She brought her strong will and fierce independence to new challenges. Within a short time, she was elected the first female mayor of Pacific Grove, where she led an effort to set up a sanctuary saving Monterey Bay from overdevelopment. Residents and visitors to Monterey today can feel the impact of Julia Barlow Platt.

Platt died in 1935 and did not live to witness her vindication almost forty-three years after her first paper on the subject. Following in her footsteps, researchers developed refined methods to mark cells during development. They injected dyes into the cells of embryos and traced where they ended up in later stages. In another technique, researchers took patches of cells from a quail and transplanted them into a chicken embryo at different times of development. Since quail cells can be distinguished easily from those of chicks, the scientists could see which organs emerged from them. Both techniques confirmed that the structures in the head that Platt had studied did not come from von Baer’s middle layer. The cells start off on the developing spinal cord and migrate to the gills to make gill bones.

Julia Platt after her term as mayor of Pacific Grove, California

The discovery that cells migrate between layers is not just a quirky asterisk to the organization of cells in the three-layer embryo—it has deeper implications for our understanding of how new structures arise. Those cells break off from the developing spinal cord to migrate all over the body of the embryo. Once at their new sites, they make tissues. They become pigment cells, myelin sheaths of the nerves, and bones of the head, among many others—all the features that are unique to vertebrates. The big shift in the transformation of Garstang’s ancestral animal to a vertebrate, involving novel tissues across the body, can be traced to the origin of a single type of cell, a new derivative of von Baer and Pander’s outer layer. Platt was right in ways she never could have envisioned. The cells she identified were a precursor to all the tissues that make vertebrates special.

Garstang had shown that a first step in the origin of backboned creatures came from a change in the timing of development, retaining larval sea squirt features into adult descendants. Platt’s discovery helped reveal the next transition, the origin of a new kind of cell. In both cases, complex changes across different organs and tissues can be distilled to simpler shifts in development. Altered timing at one step and the origin of a new type of cell at another can produce a new body plan.

Of course, these observations raise questions: How do changes in development happen? What kinds of biological shifts can cause embryological development itself to evolve?

Living things do not inherit skulls, backbones, or cell layers from their ancestors—they inherit the processes to build them. Much like a family recipe passed along and modified during each generation, the information that builds bodies has continually changed over millions of years as ancestors pass it on to descendants. Unlike a recipe used in a kitchen, the one that builds bodies anew in each generation is written not in words but in DNA. To understand biological recipes, then, we need to learn to read a whole new language and see new kinds of antecedents in the history of life.