Embryos and Evolution
The first approach naturalists took to dealing with the great variety of animals was to sort them into groups, such as vertebrates (including fish, amphibians, reptiles, birds, and mammals) and arthropods (insects, crustaceans, arachnids, and more), but between and within these groups there are many differences. What makes a fish different from a salamander? Or an insect from a spider? On a finer scale, clearly a leopard is a cat, but what makes it different from a domestic tabby? And closer to home, what makes us different from our chimpanzee cousins?
The key to answering such questions is to realize that every animal form is the product of two processes—development from an egg and evolution from its ancestors. To understand the origins of the multitude of animal forms, we must understand these two processes and their intimate relationship to each other. Simply put, development is the process that transforms an egg into a growing embryo and eventually an adult form. The evolution of form occurs through changes in development.
Both processes are breathtaking. Consider that the development of an entire complex creature begins with a single cell—the fertilized egg. In a matter of just a day (a fly maggot), a few weeks (a mouse), or several months (ourselves), an egg grows into millions, billions, or, in the case of humans, perhaps 10 trillion cells formed into organs, tissues, and parts of the body. There are few, if any, phenomena in nature that inspire our wonder and awe as much as the transformation from egg to embryo to the complete animal. One of the great figures in all of biology, Darwin’s close ally Thomas H. Huxley, remarked:
The student of Nature wonders the more and is astonished the less, the more conversant he becomes with her operations; but of all the perennial miracles she offers to his inspection, perhaps the most worthy of admiration is the development of a plant or of an animal from its embryo.—Aphorisms and Reflections (1907)
The intimate connection between development and evolution has long been appreciated in biology. Both Darwin, in The Origin of Species (1859) and The Descent of Man (1871), and Huxley in his short masterpiece, Evidence as to Man’s Place in Nature (1863), leaned heavily on the facts of embryology (as they were in the mid-nineteenth century) to connect man to the animal kingdom and for indisputable evidence of evolution. Darwin asked his reader to consider how slight changes, introduced at different points in the process and in different parts of the body, over the course of many thousands or a million generations, spanning perhaps tens of thousands to a few million years, can produce different forms that are adapted to different circumstances and that possess unique capabilities. That is evolution in a nutshell.
For Huxley, the nub of the argument was simple: we may marvel at the process of an egg becoming an adult, but we accept it as an everyday fact. It is merely then a lack of imagination to fail to grasp how changes in this process that are assimilated over long periods of time, far longer than the span of human experience, shape life’s diversity. Evolution is as natural as development. [SNIP]
While Darwin and Huxley were right about development as key to evolution, for more than one hundred years after their chief works, virtually no progress was made in understanding the mysteries of development. The puzzle of how a simple egg gives rise to a complete individual stood as one of the most elusive questions in all of biology. Many thought that development was hopelessly complex and would involve entirely different explanations for different types of animals. So frustrating was the enterprise that the study of embryology, heredity, and evolution, once intertwined at the core of biological thought a century ago, fractured into separate fields as each sought to define its own principles.
Because embryology was stalled for so long, it played no part in the so-called Modern Synthesis of evolutionary thought that emerged in the 1930s and 1940s. In the decades after Darwin, biologists struggled to understand the mechanisms of evolution. At the time of The Origin of Species, the mechanism for the inheritance of traits was not known. Gregor Mendel’s work was rediscovered decades later and genetics did not prosper until well into the 1900s. Different kinds of biologists were approaching evolution at dramatically different scales. Paleontology focused on the largest time scales, the fossil record, and the evolution of higher taxa. Systematists were concerned with the nature of species and the process of speciation. Geneticists generally studied variation in traits in just a few species. These disciplines were disconnected and sometimes hostile over which offered the most worthwhile insights into evolutionary biology. Harmony was gradually approached through an integration of evolutionary viewpoints at different levels. Julian Huxley’s book Evolution: The Modern Synthesis (1942) signaled this union and the general acceptance of two main ideas. First, that gradual evolution can be explained by small genetic changes that produce variation which is acted upon by natural selection. Second, that evolution at higher taxonomic levels and of greater magnitude can be explained by these same gradual evolutionary processes sustained over longer periods.
The Modern Synthesis established much of the foundation for how evolutionary biology has been discussed and taught for the past sixty years. However, despite the monikers of “Modern” and “Synthesis,” it was incomplete. At the time of its formulation and until recently, we could say that forms do change, and that natural selection is a force, but we could say nothing about how forms change, about the visible drama of evolution as depicted, for example, in the fossil record. The Synthesis treated embryology as a “black box” that somehow transformed genetic information into three-dimensional, functional animals.
The stalemate continued for several decades. Embryology was preoccupied with phenomena that could be studied by manipulating the eggs and embryos of a few species, and the evolutionary framework faded from embryology’s view. Evolutionary biology was studying genetic variation in populations, ignorant of the relationship between genes and form. Perhaps even worse, the perception of evolutionary biology in some circles was that it had become relegated to dusty museums.
Such was the setting in the 1970s when voices for the reunion of embryology and evolutionary biology made themselves heard. Most notable was that of Stephen Jay Gould, whose book Ontogeny and Phylogeny revived discussion of the ways in which the modification of development may influence evolution. Gould had also stirred up evolutionary biology when, with Niles Eldredge, he took a fresh look at the patterns of the fossil record and forwarded the idea of punctuated equilibria—that evolution was marked by long periods of stasis (equilibria) interrupted by brief intervals of rapid change (punctuation). Gould’s book and his many subsequent writings reexamined the “big picture” in evolutionary biology and underscored the major questions that remained unsolved. He planted seeds in more than a few impressionable young scientists, myself included.
To me, and others who had been weaned on the emerging successes of molecular biology in explaining how genes work, the situations in embryology and in evolutionary biology were both unsatisfying, but they presented enormous potential opportunities. Our lack of embryological knowledge seemed to turn much of the discussion in evolutionary biology about the evolution of form into futile exercises in speculation. How could we make progress on questions involving the evolution of form without a scientific understanding of how form is generated in the first place? Population genetics had succeeded in establishing the principle that evolution is due to changes in genes, but this was a principle without an example. No gene that affected the form and evolution of any animal had been characterized. New insights in evolution would require breakthroughs in embryology.
The Tools for Making the Kingdom are Ancient
The first and still perhaps the most stunning discovery of Evo Devo is the ancient origin of the genes for building all sorts of animals (chapters 3 and 6). The fact that such different forms of animals are shaped by very similar sets of tool kit proteins was entirely unanticipated. The ramifications of these revolutionary findings are powerful and manifold.First of all, this is entirely new and profound evidence for one of Darwin’s most important ideas—the descent of all forms from one (or a few) common ancestor. The shared genetic tool kit for development reveals deep connections between animal groups that were not at all appreciated from their dramatically different morphologies.Second, the discovery that organs and structures that were long viewed as independent analogous inventions of different animals, such as eyes, hearts, and limbs, have common genetic ingredients controlling their formation has forced a complete change in our picture of how complex structures arise. Rather than being invented repeatedly from scratch, each eye, limb, or heart has evolved by modification of some ancient regulatory networks under the command of the same master gene or genes (chapter 3). Parts of these networks trace back to the last common ancestor of bilaterians (Urbilateria), and earlier forms (chapter 6).Third, the deep history of the tool kit reveals that the invention of these genes was not the trigger of evolution. The bilaterian tool kit predated the Cambrian (chapter 6), the mammalian tool kit predated the rapid diversification of mammals in the Tertiary period, and the human tool kit long predated apes and other primates (chapter 10). It is clear that genes per se were not “drivers” of evolution. The genetic tool kit represents possibility—realization of its potential is ecologically driven.
Existing Genes and Structures Provide the Means for Innovation
We have seen that insects, pterosaurs, birds, or bats did not invent “wing” genes (chapter 7), butterflies a “spot” gene (chapter 8), or humans a “bipedalism” or “speech” gene (chapter 10). Rather, innovation in all of these groups has been a matter of modifying existing structures and of teaching old genes new tricks.
The key to innovation at the genetic level is the multifunctionality of tool kit genes. The multifunctionality of tool kit genes stems from their deployment at different times and places through batteries of genetic switches. In this manner, a protein such as Distal-less can act at one time to promote limb formation, and at another to promote eyespot development. The protein made each time is identical, so the difference in function is due to its action on different switches in these different contexts.
At an anatomical level, multifunctionality and redundancy are keys to understanding the evolutionary transitions in structures. We saw this especially in arthropods, where the shifting of a function such as feeding to one of a battery of appendages freed other appendages to become specialized for walking, swimming, or other activities. In a similar fashion, the gill branches in aquatic arthropod ancestors became modified into book gills, book lungs, tubular tracheae, spinnerets, and wings.
Evo Devo has revealed the continuity among forms that was masked or about which there were uncertainties based on appearance alone. By revealing the developmental similarities among structures, Evo Devo presents a wholly new kind of evidence that is far more objective than morphology alone. These insights into the evolution of novelty strengthen aspects of Darwin’s original ideas that some have found most difficult to grasp.
The history of these structures also illustrates how “endless forms” evolve through cycles of invention and expansion. New structures open up new ways of living. The insect wing led to the evolution of dragonflies and mayflies, butterflies and beetles, fleas and flies, and more. The expansion of these groups was catalyzed in turn by a cycle of innovation and expansion by making modifications to the wings or body plan—scale coloration systems in moths and butterflies, a hard covering in beetles, a sophisticated balancing hindwing in flies.
Why are existing body parts and genes the more frequent pathway to innovation? This is a matter of probability. Variation in existing structures and genes is more likely to arise than are new structures or genes, and this variation is therefore more abundant for selection to act upon. As François Jacob explained so eloquently, Nature works as a tinkerer with available materials, not as an engineer does by design. The invention of wings never occurred from scratch, but by modifying a gill branch (insects) or forelimbs (three times). Trends in evolution reflect the paths that are most available and therefore those taken most frequently.
Evo Devo has revealed that evolution can and does repeat itself at the levels of structures and patterns, as well as of individual genes. If evolution takes the most probable path, via existing structures and genes, then when confronted with similar selection pressures, different species may follow the same path to adaptation. We saw this in the evolution of feeding appendages in crustacea (chapter 6), pelvic spine reduction in sticklebacks (chapter 7), and other cases of limb reduction in vertebrates. We also saw that melanic fur or plumage patterns can arise through mutations in the very same gene in different species, and even the very same position in this gene (chapter 9).
These instances of evolution repeating itself directly address difficulties some have had in grasping the role of random mutation in the evolutionary process. Some people have found it hard to imagine how novelty and complexity arise from “a random process.” The key distinction is that while the generation of genetic variation by mutation is a completely random process, the sorting of these variations as to which will persist and which will be discarded is determined by a powerful, selective nonrandom process. Of the hundreds of millions or billions of individual base pairs in an animal genome, all are equally susceptible to random copying errors or physical damage that cause mutations. But only a tiny fraction of all possible mutations can alter a mammal’s coat in a viable manner, or reduce a stickleback’s spines without causing catastrophic collateral damage. In large populations of animals, over eons of time, such mutations will arise simply as a matter of probability. When they do occur, positive selection upon the trait they affect will cause them to spread in populations over time.
Jacques Monod captured this interplay of randomness and selection in evolution most eloquently in the title of his landmark book, Chance and Necessity (a reference to the Greek philosopher Democritus who said, “Everything existing in the Universe is the fruit of chance and necessity”). Evolution is indeed a matter of chance, but in the random lottery of mutations, some numbers and combinations better meet the imperatives of ecological necessity, and they arise and are selected for repeatedly.
We also saw in rock pocket mice that the same species can use different paths to a similar solution. And, while pterosaurs, birds, and bats evolved wings out of their forelimbs, they did so in fundamentally different ways. Similar ecological demands and opportunities have selected for similar adaptations, but the developmental solutions will sometimes differ in detail.
By revealing the genetic and developmental mechanisms underlying change, Evo Devo allows us to compare and contrast the evolutionary paths of different groups. Long-standing mysteries such as Batesian mimicry in butterflies, melanism in moths, and even the evolution of finch beak size and shape now lie within our grasp. We shall soon have detailed pictures of many of the classic examples of natural selection and understand in depth how variation arises and is selected for.
