Evolutionary developmental biology (informally, evo-devo) is a field of biological research that compares the developmental processes of different organisms to infer the ancestral relationships between them and how developmental processes evolved.
The field grew from 19th-century beginnings, where embryology faced a mystery: zoologists did not know how embryonic development was controlled at the molecular level. Charles Darwin noted that having similar embryos implied common ancestry, but little progress was made until the 1970s. Then, recombinant DNA technology at last brought embryology together with molecular genetics. A key early discovery was of homeotic genes that regulate development in a wide range of eukaryotes.
The field is characterised by some key concepts which took evolutionary biologists by surprise. One is deep homology, the finding that dissimilar organs such as the eyes of insects, vertebrates and cephalopod molluscs, long thought to have evolved separately, are controlled by similar genes such as pax-6 , from the evo-devo gene toolkit. These genes are ancient, being highly conserved among phyla; they generate the patterns in time and space which shape the embryo, and ultimately form the body plan of the organism. Another is that species do not differ much in their structural genes, such as those coding for enzymes; what does differ is the way that gene expression is regulated by the toolkit genes. These genes are reused, unchanged, many times in different parts of the embryo and at different stages of development, forming a complex cascade of control, switching other regulatory genes as well as structural genes on and off in a precise pattern. This multiple pleiotropic reuse explains why these genes are highly conserved, as any change would have many adverse consequences which natural selection would oppose.
New morphological features and ultimately new species are produced by variations in the toolkit, either when genes are expressed in a new pattern, or when toolkit genes acquire additional functions. Another possibility is the Neo-Lamarckian theory that epigenetic changes are later consolidated at gene level, something that may have been important early in the history of multicellular life.
A recapitulation theory of evolutionary development was proposed by Étienne Serres in 1824–26, echoing the 1808 ideas of Johann Friedrich Meckel. They argued that the embryos of 'higher' animals went through or recapitulated a series of stages, each of which resembled an animal lower down the great chain of being. For example, the brain of a human embryo looked first like that of a fish, then in turn like that of a reptile, bird, and mammal before becoming clearly human. The embryologist Karl Ernst von Baer opposed this, arguing in 1828 that there was no linear sequence as in the great chain of being, based on a single body plan, but a process of epigenesis in which structures differentiate. Von Baer instead recognised four distinct animal body plans: radiate, like starfish; molluscan, like clams; articulate, like lobsters; and vertebrate, like fish. Zoologists then largely abandoned recapitulation, though Ernst Haeckel revived it in 1866.
From the early 19th century through most of the 20th century, embryology faced a mystery. Animals were seen to develop into adults of widely differing body plan, often through similar stages, from the egg, but zoologists knew almost nothing about how embryonic development was controlled at the molecular level, and therefore equally little about how developmental processes had evolved.Charles Darwin argued that a shared embryonic structure implied a common ancestor. As an example of this, Darwin cited in his 1859 book On the Origin of Species the shrimp-like larva of the barnacle, whose sessile adults looked nothing like other arthropods; Linnaeus and Cuvier had classified them as molluscs. Darwin also noted Alexander Kowalevsky's finding that the tunicate, too, was not a mollusc, but in its larval stage had a notochord and pharyngeal slits which developed from the same germ layers as the equivalent structures in vertebrates, and should therefore be grouped with them as chordates. 19th century zoology thus converted embryology into an evolutionary science, connecting phylogeny with homologies between the germ layers of embryos. Zoologists including Fritz Müller proposed the use of embryology to discover phylogenetic relationships between taxa. Müller demonstrated that crustaceans shared the Nauplius larva, identifying several parasitic species that had not been recognised as crustaceans. Müller also recognised that natural selection must act on larvae, just as it does on adults, giving the lie to recapitulation, which would require larval forms to be shielded from natural selection. Two of Haeckel's other ideas about the evolution of development have fared better than recapitulation: he argued in the 1870s that changes in the timing (heterochrony) and changes in the positioning within the body (heterotopy) of aspects of embryonic development would drive evolution by changing the shape of a descendant's body compared to an ancestor's. It took a century before these ideas were shown to be correct. In 1917, D'Arcy Thompson wrote a book on the shapes of animals, showing with simple mathematics how small changes to parameters, such as the angles of a gastropod's spiral shell, can radically alter an animal's form, though he preferred mechanical to evolutionary explanation. But for the next century, without molecular evidence, progress stalled.
In the so-called modern synthesis of the early 20th century, Ronald Fisher brought together Darwin's theory of evolution, with its insistence on natural selection, heredity, and variation, and Gregor Mendel's laws of genetics into a coherent structure for evolutionary biology. Biologists assumed that an organism was a straightforward reflection of its component genes: the genes coded for proteins, which built the organism's body. Biochemical pathways (and, they supposed, new species) evolved through mutations in these genes. It was a simple, clear and nearly comprehensive picture: but it did not explain embryology.
The evolutionary embryologist Gavin de Beer anticipated evolutionary developmental biology in his 1930 book Embryos and Ancestors ,by showing that evolution could occur by heterochrony, such as in the retention of juvenile features in the adult. This, de Beer argued, could cause apparently sudden changes in the fossil record, since embryos fossilise poorly. As the gaps in the fossil record had been used as an argument against Darwin's gradualist evolution, de Beer's explanation supported the Darwinian position. However, despite de Beer, the modern synthesis largely ignored embryonic development to explain the form of organisms, since population genetics appeared to be an adequate explanation of how forms evolved.
In 1961, Jacques Monod, Jean-Pierre Changeux and François Jacob discovered the lac operon in the bacterium Escherichia coli . It was a cluster of genes, arranged in a feedback control loop so that its products would only be made when "switched on" by an environmental stimulus. One of these products was an enzyme that splits a sugar, lactose; and lactose itself was the stimulus that switched the genes on. This was a revelation, as it showed for the first time that genes, even in an organism as small as a bacterium, were subject to fine-grained control. The implication was that many other genes were also elaborately regulated.
In 1977, a revolution in thinking about evolution and developmental biology began, with the arrival of recombinant DNA technology in genetics, and the works Ontogeny and Phylogeny by Stephen J. Gould and Evolution by Tinkering by François Jacob. Gould laid to rest Haeckel's interpretation of evolutionary embryology, while Jacob set out an alternative theory.This led to a second synthesis, at last including embryology as well as molecular genetics, phylogeny, and evolutionary biology to form evo-devo. In 1978, Edward B. Lewis discovered homeotic genes that regulate embryonic development in Drosophila fruit flies, which like all insects are arthropods, one of the major phyla of invertebrate animals. Bill McGinnis quickly discovered homeotic gene sequences, homeoboxes, in animals in other phyla, in vertebrates such as frogs, birds, and mammals; they were later also found in fungi such as yeasts, and in plants. There were evidently strong similarities in the genes that controlled development across all the eukaryotes. In 1980, Christiane Nüsslein-Volhard and Eric Wieschaus described gap genes which help to create the segmentation pattern in fruit fly embryos; they and Lewis won a Nobel Prize for their work in 1995.
Later, more specific similarities were discovered: for example, the Distal-less gene was found in 1989 to be involved in the development of appendages or limbs in fruit flies,the fins of fish, the wings of chickens, the parapodia of marine annelid worms, the ampullae and siphons of tunicates, and the tube feet of sea urchins. It was evident that the gene must be ancient, dating back to the last common ancestor of bilateral animals (before the Ediacaran Period, which began some 635 million years ago). Evo-devo had started to uncover the ways that all animal bodies were built during development.
Roughly spherical eggs of different animals give rise to extremely different bodies, from jellyfish to lobsters, butterflies to elephants. Many of these organisms share the same structural genes for body-building proteins like collagen and enzymes, but biologists had expected that each group of animals would have its own rules of development. The surprise of evo-devo is that the shaping of bodies is controlled by a rather small percentage of genes, and that these regulatory genes are ancient, shared by all animals. The giraffe does not have a gene for a long neck, any more than the elephant has a gene for a big body. Their bodies are patterned by a system of switching which causes development of different features to begin earlier or later, to occur in this or that part of the embryo, and to continue for more or less time.
The puzzle of how embryonic development was controlled began to be solved using the fruit fly Drosophila melanogaster as a model organism. The step-by-step control of its embryogenesis was visualized by attaching fluorescent dyes of different colours to specific types of protein made by genes expressed in the embryo.A dye such as green fluorescent protein, originally from a jellyfish, was typically attached to an antibody specific to a fruit fly protein, forming a precise indicator of where and when that protein appeared in the living embryo.
Using such a technique, in 1994 Walter Gehring found that the pax-6 gene, vital for forming the eyes of fruit flies, exactly matches an eye-forming gene in mice and humans. The same gene was quickly found in many other groups of animals, such as squid, a cephalopod mollusc. Biologists including Ernst Mayr had believed that eyes had arisen in the animal kingdom at least 40 times, as the anatomy of different types of eye varies widely.For example, the fruit fly's compound eye is made of hundreds of small lensed structures (ommatidia); the human eye has a blind spot where the optic nerve enters the eye, and the nerve fibres run over the surface of the retina, so light has to pass through a layer of nerve fibres before reaching the detector cells in the retina, so the structure is effectively "upside-down"; in contrast, the cephalopod eye has the retina, then a layer of nerve fibres, then the wall of the eye "the right way around". The evidence of pax-6, however, was that the same genes controlled the development of the eyes of all these animals, suggesting that they all evolved from a common ancestor. Ancient genes had been conserved through millions of years of evolution to create dissimilar structures for similar functions, demonstrating deep homology between structures once thought to be purely analogous. This has caused a radical revision of the meaning of homology in evolutionary biology.
A small fraction of the genes in an organism's genome control the organism's development. These genes are called the developmental-genetic toolkit. They are highly conserved among phyla, meaning that they are ancient and very similar in widely separated groups of animals. Differences in deployment of toolkit genes affect the body plan and the number, identity, and pattern of body parts. Most toolkit genes are parts of signalling pathways: they encode transcription factors, cell adhesion proteins, cell surface receptor proteins and signalling ligands that bind to them, and secreted morphogens that diffuse through the embryo. All of these help to define the fate of undifferentiated cells in the embryo. Together, they generate the patterns in time and space which shape the embryo, and ultimately form the body plan of the organism. Among the most important toolkit genes are the Hox genes. These transcription factors contain the homeobox protein-binding DNA motif, also found in other toolkit genes, and create the basic pattern of the body along its front-to-back axis.Hox genes determine where repeating parts, such as the many vertebrae of snakes, will grow in a developing embryo or larva. Pax-6, already mentioned, is a classic toolkit gene. Homeobox genes are also found in plants, implying they are common to all eukaryotes.
The protein products of the regulatory toolkit are reused not by duplication and modification, but by a complex mosaic of pleiotropy, being applied unchanged in many independent developmental processes, giving pattern to many dissimilar body structures.The loci of these pleiotropic toolkit genes have large, complicated and modular cis-regulatory elements. For example, while a non-pleiotropic rhodopsin gene in the fruit fly has a cis-regulatory element just a few hundred base pairs long, the pleiotropic eyeless cis-regulatory region contains 6 cis-regulatory elements in over 7000 base pairs. The regulatory networks involved are often very large. Each regulatory protein controls "scores to hundreds" of cis-regulatory elements. For instance, 67 fruit fly transcription factors controlled on average 124 target genes each. All this complexity enables genes involved in the development of the embryo to be switched on and off at exactly the right times and in exactly the right places. Some of these genes are structural, directly forming enzymes, tissues and organs of the embryo. But many others are themselves regulatory genes, so what is switched on is often a precisely-timed cascade of switching, involving turning on one developmental process after another in the developing embryo.
Such a cascading regulatory network has been studied in detail in the development of the fruit fly embryo. The young embryo is oval in shape, like a rugby ball. A small number of genes produce messenger RNAs that set up concentration gradients along the long axis of the embryo. In the early embryo, the bicoid and hunchback genes are at high concentration near the anterior end, and give pattern to the future head and thorax; the caudal and nanos genes are at high concentration near the posterior end, and give pattern to the hindmost abdominal segments. The effects of these genes interact; for instance, the Bicoid protein blocks the translation of caudal's messenger RNA, so the Caudal protein concentration becomes low at the anterior end. Caudal later switches on genes which create the fly's hindmost segments, but only at the posterior end where it is most concentrated.
The Bicoid, Hunchback and Caudal proteins in turn regulate the transcription of gap genes such as giant, knirps, Krüppel, and tailless in a striped pattern, creating the first level of structures that will become segments.The proteins from these in turn control the pair-rule genes, which in the next stage set up 7 bands across the embryo's long axis. Finally, the segment polarity genes such as engrailed split each of the 7 bands into two, creating 14 future segments.
This process explains the accurate conservation of toolkit gene sequences, which has resulted in deep homology and functional equivalence of toolkit proteins in dissimilar animals (seen, for example, when a mouse protein controls fruit fly development). The interactions of transcription factors and cis-regulatory elements, or of signalling proteins and receptors, become locked in through multiple usages, making almost any mutation deleterious and hence eliminated by natural selection.
Among the more surprising and, perhaps, counterintuitive (from a neo-Darwinian viewpoint) results of recent research in evolutionary developmental biology is that the diversity of body plans and morphology in organisms across many phyla are not necessarily reflected in diversity at the level of the sequences of genes, including those of the developmental genetic toolkit and other genes involved in development. Indeed, as John Gerhart and Marc Kirschner have noted, there is an apparent paradox: "where we most expect to find variation, we find conservation, a lack of change".So, if the observed morphological novelty between different clades does not come from changes in gene sequences (such as by mutation), where does it come from? Novelty may arise by mutation-driven changes in gene regulation.
Variations in the toolkit may have produced a large part of the morphological evolution of animals. The toolkit can drive evolution in two ways. A toolkit gene can be expressed in a different pattern, as when the beak of Darwin's large ground-finch was enlarged by the BMP gene,or when snakes lost their legs as distal-less became under-expressed or not expressed at all in the places where other reptiles continued to form their limbs. Or, a toolkit gene can acquire a new function, as seen in the many functions of that same gene, distal-less, which controls such diverse structures as the mandible in vertebrates, legs and antennae in the fruit fly, and eyespot pattern in butterfly wings. Given that small changes in toolbox genes can cause significant changes in body structures, they have often enabled the same function convergently or in parallel. distal-less generates wing patterns in the butterflies Heliconius erato and Heliconius melpomene , which are Müllerian mimics. In so-called facilitated variation, their wing patterns arose in different evolutionary events, but are controlled by the same genes. Developmental changes can contribute directly to speciation.
Evolutionary innovation may sometimes begin in Lamarckian style with epigenetic alterations of gene regulation or phenotype generation, subsequently consolidated by changes at the gene level. Epigenetic changes include modification of DNA by reversible methylation,as well as nonprogrammed remoulding of the organism by physical and other environmental effects due to the inherent plasticity of developmental mechanisms. The biologists Stuart A. Newman and Gerd B. Müller have suggested that organisms early in the history of multicellular life were more susceptible to this second category of epigenetic determination than are modern organisms, providing a basis for early macroevolutionary changes.
Development in specific lineages can be biased either positively, towards a given trajectory or phenotype,or negatively, away from producing certain types of change; either may be absolute (the change is always or never produced) or relative. Evidence for any such direction in evolution is however hard to acquire. For example, in the gastropods, the snail-type shell is always built as a tube that grows both in length and in diameter; selection has created a wide variety of shell shapes such as flat spirals, cowries and tall turret spirals within these constraints. Among the centipedes, the Lithobiomorpha always have 15 trunk segments as adults, probably the result of a developmental bias towards an odd number of trunk segments. Another centipede order, the Geophilomorpha, the number of segments varies in different species between 27 and 191, but the number is always odd, making this an absolute constraint; almost all the odd numbers in that range are occupied by one or another species.
Ecological evolutionary developmental biology (eco-evo-devo) integrates research from developmental biology and ecology to examine their relationship with evolutionary theory.Researchers study concepts and mechanisms such as developmental plasticity, epigenetic inheritance, genetic assimilation, niche construction and symbiosis.
Developmental biology is the study of the process by which animals and plants grow and develop. Developmental biology also encompasses the biology of regeneration, asexual reproduction, metamorphosis, and the growth and differentiation of stem cells in the adult organism.
The theory of recapitulation, also called the biogenetic law or embryological parallelism—often expressed using Ernst Haeckel's phrase "ontogeny recapitulates phylogeny"—is a historical hypothesis that the development of the embryo of an animal, from fertilization to gestation or hatching (ontogeny), goes through stages resembling or representing successive adult stages in the evolution of the animal's remote ancestors (phylogeny). It was formulated in the 1820s by Étienne Serres based on the work of Johann Friedrich Meckel, after whom it is also known as Meckel–Serres law.
Embryology is the branch of biology that studies the prenatal development of gametes, fertilization, and development of embryos and fetuses. Additionally, embryology encompasses the study of congenital disorders that occur before birth, known as teratology.
In evolutionary developmental biology, heterochrony is any genetically controlled difference in the timing or duration of a developmental process in an organism compared to its ancestors or other organisms. This leads to changes in the size, shape, characteristics and even presence of certain organs and features. It is contrasted with heterotopy, a change in spatial positioning of some process in the embryo, which can also create morphological innovation. Heterochrony can be divided into intraspecific heterochrony, variation within a species, and interspecific heterochrony, phylogenetic variation, i.e. variation of a descendant species with respect to an ancestral species.
A morphogen is a substance whose non-uniform distribution governs the pattern of tissue development in the process of morphogenesis or pattern formation, one of the core processes of developmental biology, establishing positions of the various specialized cell types within a tissue. More specifically, a morphogen is a signaling molecule that acts directly on cells to produce specific cellular responses depending on its local concentration.
Hox genes, a subset of homeobox genes, are a group of related genes that specify regions of the body plan of an embryo along the head-tail axis of animals. Hox proteins encode and specify the characteristics of 'position', ensuring that the correct structures form in the correct places of the body. For example, Hox genes in insects specify which appendages form on a segment, and Hox genes in vertebrates specify the types and shape of vertebrae that will form. In segmented animals, Hox proteins thus confer segmental or positional identity, but do not form the actual segments themselves.
The theory of facilitated variation demonstrates how seemingly complex biological systems can arise through a limited number of regulatory genetic changes, through the differential re-use of pre-existing developmental components. The theory was presented in 2005 by Marc W. Kirschner and John C. Gerhart.
A body plan, Bauplan, or ground plan is a set of morphological features common to many members of a phylum of animals. The vertebrate body plan is one of many: invertebrates consist of many phyla.
Genetic assimilation is a process described by Conrad H. Waddington by which a phenotype originally produced in response to an environmental condition, such as exposure to a teratogen, later becomes genetically encoded via artificial selection or natural selection. Despite superficial appearances, this does not require the (Lamarckian) inheritance of acquired characters, although epigenetic inheritance could potentially influence the result. Waddington stated that genetic assimilation overcomes the barrier to selection imposed by what he called canalization of developmental pathways; he supposed that the organism's genetics evolved to ensure that development proceeded in a certain way regardless of normal environmental variations.
Biological or process structuralism, also known as formalism, is a school of biological thought that objects to an exclusively Darwinian or adaptationist explanation of natural selection such as is described in the 20th century's modern synthesis. It proposes instead that evolution is guided differently, basically by more or less physical forces which shape the development of an animal's body, and sometimes implies that these forces supersede selection altogether.
In the developmental biology of the early twentieth century, a morphogenetic field is a group of cells able to respond to discrete, localized biochemical signals leading to the development of specific morphological structures or organs. The spatial and temporal extents of the embryonic field are dynamic, and within the field is a collection of interacting cells out of which a particular organ is formed. As a group, the cells within a given morphogenetic field are constrained: thus, cells in a limb field will become a limb tissue, those in a cardiac field will become heart tissue. However, specific cellular programming of individual cells in a field is flexible: an individual cell in a cardiac field can be redirected via cell-to-cell signaling to replace specific damaged or missing cells. Imaginal discs in insect larvae are examples of morphogenetic fields.
Evolutionary developmental biology (evo-devo) is the study of developmental programs and patterns from an evolutionary perspective. It seeks to understand the various influences shaping the form and nature of life on the planet. Evo-devo arose as a separate branch of science rather recently. An early sign of this occurred in 1999.
In evolutionary developmental biology, the concept of deep homology is used to describe cases where growth and differentiation processes are governed by genetic mechanisms that are homologous and deeply conserved across a wide range of species.
Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom is a 2005 book by the molecular biologist Sean B. Carroll. It presents a summary of the emerging field of evolutionary developmental biology and the role of toolkit genes. It has won numerous awards for science communication.
Michael Levine is an American developmental and cell biologist at Princeton University, where he is the Director of the Lewis-Sigler Institute for Integrative Genomics and a Professor of Molecular Biology.
Alessandro Minelli is an Italian biologist and a professor emeritus of Zoology in the Faculty of Mathematical, Physical and Natural Sciences of the University of Padova mainly working on evo-devo subjects.
The extended evolutionary synthesis consists of a set of theoretical concepts argued to be more comprehensive than the earlier modern synthesis of evolutionary biology that took place between 1918 and 1942. The extended evolutionary synthesis was called for in the 1950s by C. H. Waddington, argued for on the basis of punctuated equilibrium by Stephen Jay Gould and Niles Eldredge in the 1980s, and was reconceptualized in 2007 by Massimo Pigliucci and Gerd B. Müller.
Heterotopy is an evolutionary change in the spatial arrangement of an animal's embryonic development, complementary to heterochrony, a change to the rate or timing of a development process. It was first identified by Ernst Haeckel in 1866 and has remained less well studied than heterochrony.
The evo-devo gene toolkit is the small subset of genes in an organism's genome whose products control the organism's embryonic development. Toolkit genes are central to the synthesis of molecular genetics, palaeontology, evolution and developmental biology in the science of evolutionary developmental biology (evo-devo).
In Embryology the notion of a phylotypic stage or phylotypic period refers to a particular developmental stage or developmental period during mid-embryogenesis where embryos of related species within a phylum express the highest degree of morphological and molecular resemblance. Recent molecular studies in various plant and animal species were able to quantify the expression of genes covering crucial stages of embryo development and found that during the morphologically defined phylotypic period the evolutionary oldest genes, genes with similar temporal expression patterns, and genes under strongest purifying selection are most active throughout the phylotypic period.
Biologists could say, with confidence, that forms change, and that natural selection is an important force for change. Yet they could say nothing about how that change is accomplished. How bodies or body parts change, or how new structures arise, remained complete mysteries.
Cirripedes afford a good instance of this: even the illustrious Cuvier did not perceive that a barnacle was, as it certainly is, a crustacean; but a glance at the larva shows this to be the case in an unmistakeable manner.
Homeobox genes are found in almost all eukaryotes, and have diversified into 11 gene classes and over 100 gene families in animal evolution, and 10 to 14 gene classes in plants.