Evolutionary developmental biology

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Homologous hox genes in such different animals as insects and vertebrates control embryonic development and hence the form of adult bodies. These genes have been highly conserved through hundreds of millions of years of evolution. Genes hox.jpeg
Homologous hox genes in such different animals as insects and vertebrates control embryonic development and hence the form of adult bodies. These genes have been highly conserved through hundreds of millions of years of evolution.

Evolutionary developmental biology (informally, evo-devo) is a field of biological research that compares the developmental processes of different organisms to infer 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 composed of multiple core evolutionary concepts. 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.


Embryology theories of Ernst Haeckel, who argued for recapitulation of evolutionary development in the embryo, and Karl Ernst von Baer's epigenesis Haeckel vs von Baer.svg
Embryology theories of Ernst Haeckel, who argued for recapitulation of evolutionary development in the embryo, and Karl Ernst von Baer's epigenesis


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 recognized 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. [2] [3] [4] [5] [6]

Evolutionary morphology

A. Lancelet (a chordate), B. Larval tunicate, C. Adult tunicate. Kowalevsky saw that the notochord (1) and gill slit (5) are shared by tunicates and vertebrates. Comparison of Three Invertebrate Chordates.svg
A. Lancelet (a chordate), B. Larval tunicate, C. Adult tunicate. Kowalevsky saw that the notochord (1) and gill slit (5) are shared by tunicates and vertebrates.

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. [7] 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. [8] [9] 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. [8] [10]

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 recognized as crustaceans. Müller also recognized 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. [8] 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. [11] [12] [13] 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 a mechanical to evolutionary explanation. [14] [15] But for the next century, without molecular evidence, progress stalled. [8]

The modern synthesis of the early 20th century

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. [8] [16]

The evolutionary embryologist Gavin de Beer anticipated evolutionary developmental biology in his 1930 book Embryos and Ancestors , [17] by showing that evolution could occur by heterochrony, [18] such as in the retention of juvenile features in the adult. [11] 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. [19] 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. [20] [21] [lower-alpha 1]

The lac operon

The lac operon. Top:Repressed, Bottom:Active
1: RNA Polymerase, 2: Repressor, 3: Promoter, 4: Operator, 5: Lactose, 6-8: protein-encoding genes, controlled by the switch, that cause lactose to be digested Lac Operon.svg
The lac operon. Top:Repressed, Bottom:Active
1: RNA Polymerase, 2: Repressor, 3: Promoter, 4: Operator, 5: Lactose, 6–8: protein-encoding genes, controlled by the switch, that cause lactose to be digested

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 organisms as small as a bacterium, are subject to precise control. The implication was that many other genes were also elaborately regulated. [23]

The birth of evo-devo and a second synthesis

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. [8] This led to a second synthesis, [24] [25] at last including embryology as well as molecular genetics, phylogeny, and evolutionary biology to form evo-devo. [26] [27] 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. [28] 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. [29] [30] There were evidently strong similarities in the genes that controlled development across all the eukaryotes. [31] In 1980, Christiane Nüsslein-Volhard and Eric Wieschaus described gap genes which help to create the segmentation pattern in fruit fly embryos; [32] [33] they and Lewis won a Nobel Prize for their work in 1995. [29] [34]

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, [35] 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. [36] [37]

The control of body structure

Deep homology

Roughly spherical eggs of different animals give rise to unique morphologies, 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. [7]

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. [7] 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. [38]

The pax-6 gene controls development of eyes of different types across the animal kingdom. PAX6 Phenotypes Washington etal PLoSBiol e1000247.png
The pax-6 gene controls development of eyes of different types across the animal kingdom.

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. [7] 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". [39] 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. [7] 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. [40] [41] This notion was later extended to the evolution of embryogenesis [42] and has caused a radical revision of the meaning of homology in evolutionary biology. [40] [41] [43]

Gene toolkit

Expression of homeobox (Hox) genes in the fruit fly Hoxgenesoffruitfly.svg
Expression of homeobox (Hox) genes in the fruit fly

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. [43] Hox genes determine where repeating parts, such as the many vertebrae of snakes, will grow in a developing embryo or larva. [7] Pax-6, already mentioned, is a classic toolkit gene. [44] Although other toolkit genes are involved in establishing the plant bodyplan, [45] homeobox genes are also found in plants, implying they are common to all eukaryotes. [46] [47] [48]

The embryo's regulatory networks

A gene regulatory network Gene Regulatory Network.jpg
A gene regulatory network

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. [43] 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. [43] 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. [43] 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. [43]

Gene product distributions along the long axis of the early embryo of a fruit fly Drosophila early embryo protein gradients.svg
Gene product distributions along the long axis of the early embryo of a fruit fly

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. [49] [50]

Gap genes in the fruit fly are switched on by genes such as bicoid, setting up stripes across the embryo which start to pattern the body's segments. Gap gene expression.svg
Gap genes in the fruit fly are switched on by genes such as bicoid , setting up stripes across the embryo which start to pattern the body's segments.

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. [32] 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. [49] [50]

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. [43]

The origins of novelty

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". [51] 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. [43] [52] [53] [54]

Variations in the toolkit

Different species of Heliconius butterfly have independently evolved similar patterns, apparently both facilitated and constrained by the available developmental-genetic toolkit genes controlling wing pattern formation.

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, [55] 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. [56] 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, [57] [58] legs and antennae in the fruit fly, [59] and eyespot pattern in butterfly wings. [60] 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, [61] their wing patterns arose in different evolutionary events, but are controlled by the same genes. [62] Developmental changes can contribute directly to speciation. [63]

Consolidation of epigenetic changes

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, [64] as well as nonprogrammed remoulding of the organism by physical and other environmental effects due to the inherent plasticity of developmental mechanisms. [65] 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. [66]

Developmental bias

Among the centipedes, all members of the Geophilomorpha are constrained by a developmental bias to have an odd number of segments, whether as few as 27 or as many as 191. Chilipoda- Geophilomorpha (3309242471).jpg
Among the centipedes, all members of the Geophilomorpha are constrained by a developmental bias to have an odd number of segments, whether as few as 27 or as many as 191.

Development in specific lineages can be biased either positively, towards a given trajectory or phenotype, [lower-alpha 2] 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 and can also result from developmental constraints that limit diversification. [68] 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. [67] [69] [70]

Ecological evolutionary developmental biology

Ecological evolutionary developmental biology [lower-alpha 3] integrates research from developmental biology and ecology to examine their relationship with evolutionary theory. [71] Researchers study concepts and mechanisms such as developmental plasticity, epigenetic inheritance, genetic assimilation, niche construction and symbiosis. [72] [73]

See also


  1. Though C. H. Waddington had called for embryology to be added to the synthesis in his 1953 paper "Epigenetics and Evolution". [22]
  2. Positive bias is sometimes called developmental drive. [67]
  3. Spanish Wikipedia has an article on the subject: eco-evo-devo.

Related Research Articles

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.

Recapitulation theory Biological hypothesis

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.

Evolutionary biology Study of the processes that produced the diversity of life

Evolutionary biology is the subfield of biology that studies the evolutionary processes that produced the diversity of life on Earth. Simply, it is also defined as the study of the history of life forms on Earth. Evolution is based on the theory that all species are related and they gradually change over time. In a population, the genetic variations affect the physical characteristics i.e. phenotypes of an organism. These changes in the phenotypes will be an advantage to some organisms, which will then be passed onto their offspring. Peppered Moth and Flightless birds are some examples of evolution in species over many generations. In the 1930s, the discipline of evolutionary biology emerged through what Julian Huxley called the modern synthesis of understanding, from previously unrelated fields of biological research, such as genetics and ecology, systematics, and paleontology. A person who studies Evolutionary biology is called an Evolutionary biologist. The importance of studying Evolutionary biology is mainly to understand the principles behind the origin and extinction of species.

Heterochrony Evolutionary change in the rates or durations of developmental events, leading to structural changes

In evolutionary developmental biology, heterochrony is any genetically controlled difference in the timing, rate, 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.

Morphogen Biological substance that guides development by non-uniform distribution

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.

Stuart Alan Newman is a professor of cell biology and anatomy at New York Medical College in Valhalla, NY, United States. His research centers around three program areas: cellular and molecular mechanisms of vertebrate limb development, physical mechanisms of morphogenesis, and mechanisms of morphological evolution. He also writes about social and cultural aspects of biological research and technology.

Body plan Set of morphological features common to members of a phylum of animals

A body plan, Bauplan, or ground plan is a set of morphological features common to many members of a phylum of animals. The vertebrates share one body plan, while invertebrates have many.

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.

Structuralism (biology) Attempt to explain evolution by forces other than natural selection

Biological or process structuralism 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.

Morphogenetic field Developmental biology concept

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.

Deep homology Control of growth and differentiation by deeply conserved genetic mechanisms

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.

<i>Endless Forms Most Beautiful</i> (book) 2005 evo-devo book by Sean B. Carroll

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.

Extended evolutionary synthesis Set of theoretical concepts concerning evolutionary biology

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. Notably, Dr. Müller concluded from this research that Natural Selection has no way of explaining speciation, saying: “selection has no innovative capacity...the generative and the ordering aspects of morphological evolution are thus absent from evolutionary theory.”

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.

von Baers laws (embryology)

Von Baer's laws of embryology are four rules proposed by Karl Ernst von Baer to explain the observed pattern of embryonic development in different species.

Evo-devo gene toolkit

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). Many of them are ancient and highly conserved among animal phyla.

In Embryology a phylotypic stage or phylotypic period is 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.


  1. Richardson and Keuck (2002), "Haeckel's ABC of evolution and development", Biological Reviews of the Cambridge Philosophical Society, 77 (4): 495–528, CiteSeerX , doi:10.1017/s1464793102005948, PMID   12475051, S2CID   23494485 {{citation}}: CS1 maint: uses authors parameter (link) p.516
  2. O'Connell, Lindsey (10 July 2013). "The Meckel-Serres Conception of Recapitulation". The Embryo Project Encyclopedia. Retrieved 10 October 2016.
  3. Desmond, Adrian J. (1989). The politics of evolution: morphology, medicine, and reform in radical London . Chicago: University of Chicago Press. pp.  53–53, 86–88, 337–340, 490–491. ISBN   978-0-226-14374-3.
  4. Secord 2003 , p. 252–253
  5. Bowler, Peter J. (2003). Evolution: the history of an idea. Berkeley: University of California Press. pp.  120–128, 190–191, 208. ISBN   978-0-520-23693-6.
  6. Secord 2003 , p. 424, 512
  7. 1 2 3 4 5 6 Carroll, Sean B. "The Origins of Form". Natural History. Retrieved 9 October 2016. 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.
  8. 1 2 3 4 5 6 Gilbert, Scott F. (2003). "The morphogenesis of evolutionary developmental biology" (PDF). International Journal of Developmental Biology. 47 (7–8): 467–477. PMID   14756322.
  9. Darwin, Charles (1859). On the Origin of Species. London: John Murray. pp. 439–440. ISBN   978-0-8014-1319-3. 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.
  10. Richmond, Marsha (January 2007). "Darwin's Study of the Cirripedia". Darwin Online. Retrieved 9 October 2016.
  11. 1 2 Hall, B. K. (2003). "Evo-Devo: evolutionary developmental mechanisms". International Journal of Developmental Biology. 47 (7–8): 491–495. PMID   14756324.
  12. Ridley, Mark (2003). Evolution. Wiley-Blackwell. ISBN   978-1-4051-0345-9.
  13. Gould 1977, pp. 221–222.
  14. Ball, Philip (7 February 2013). "In retrospect: On Growth and Form". Nature. 494 (32–33): 32–33. Bibcode:2013Natur.494...32B. doi:10.1038/494032a. S2CID   205076253.
  15. Shalizi, Cosma. "Review: The Self-Made Tapestry by Philip Ball". University of Michigan. Retrieved 14 October 2016.
  16. Bock, Walter J. (July 1981). "Reviewed Work: The Evolutionary Synthesis. Perspectives on the Unification of Biology". The Auk . 98 (3): 644–646. ISSN   0004-8038. JSTOR   4086148.
  17. Held, Lewis I. (2014). How the Snake Lost its Legs. Curious Tales from the Frontier of Evo-Devo. Cambridge University Press. p. 67. ISBN   978-1-107-62139-8.
  18. Gould 1977 , pp. 221–222
  19. Ingo Brigandt (2006). "Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899-1972)" (PDF). Journal of Experimental Zoology . 306B (4): 317–328. doi:10.1002/jez.b.21100. PMID   16506229.
  20. Gilbert, S. F.; Opitz, J. M.; Raff, R. A. (1996). "Resynthesizing evolutionary and developmental biology". Developmental Biology. 173 (2): 357–372. doi: 10.1006/dbio.1996.0032 . PMID   8605997.
  21. Adams, M. (1991). Warren, L.; Koprowski, H. (eds.). Through the looking glass: The evolution of Soviet Darwinism. New Perspectives in Evolution. Liss/Wiley. pp. 37–63.
  22. Smocovitis 1996, p. 153
  23. Monod, Jacques; Changeux, J.P.; Jacob, François (1963). "Allosteric proteins and cellular control systems". Journal of Molecular Biology. 6 (4): 306–329. doi:10.1016/S0022-2836(63)80091-1. PMID   13936070.
  24. Gilbert, S.F.; Opitz, J.M.; Raff, R.A. (1996). "Resynthesizing Evolutionary and Developmental Biology". Developmental Biology. 173 (2): 357–372. doi: 10.1006/dbio.1996.0032 . PMID   8605997.
  25. Müller, G. B. (2007). "Evo–devo: extending the evolutionary synthesis". Nature Reviews Genetics. 8 (12): 943–949. doi:10.1038/nrg2219. PMID   17984972. S2CID   19264907.
  26. Goodman, C. S.; Coughlin, B. C. (2000). Goodman, C. S.; Coughlin B. S. (eds.). "Special feature: The evolution of evo-devo biology". Proceedings of the National Academy of Sciences . 97 (9): 4424–4456. Bibcode:2000PNAS...97.4424G. doi: 10.1073/pnas.97.9.4424 . PMC   18255 . PMID   10781035.
  27. Müller GB and Newman SA (Eds.) (2005). "Special issue: Evolutionary Innovation and Morphological Novelty". Journal of Experimental Zoology Part B. 304B (6): 485–631. doi:10.1002/jez.b.21080. PMID   16252267. Archived from the original on 11 December 2012.
  28. Palmer, R.A. (2004). "Symmetry breaking and the evolution of development". Science . 306 (5697): 828–833. Bibcode:2004Sci...306..828P. CiteSeerX . doi:10.1126/science.1103707. PMID   15514148. S2CID   32054147.
  29. 1 2 Winchester, Guil (2004). "Edward B. Lewis 1918-2004" (PDF). Current Biology (published 21 September 2004). 14 (18): R740–742. doi: 10.1016/j.cub.2004.09.007 . PMID   15380080. S2CID   32648995.
  30. Bürglin, Thomas R. "The Homeobox Page". Karolinska Institutet . Retrieved 13 October 2016.
  31. Holland, P.W. (2013). "Evolution of homeobox genes". Wiley Interdiscip Rev Dev Biol. 2 (1): 31–45. doi:10.1002/wdev.78. PMID   23799629. S2CID   44396110. 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.
  32. 1 2 Nüsslein-Volhard, C.; Wieschaus, E. (October 1980). "Mutations affecting segment number and polarity in Drosophila". Nature. 287 (5785): 795–801. Bibcode:1980Natur.287..795N. doi:10.1038/287795a0. PMID   6776413. S2CID   4337658.
  33. Arthur, Wallace (14 February 2002). "The emerging conceptual framework of evolutionary developmental biology". Nature. 415 (6873): 757–764. Bibcode:2002Natur.415..757A. doi:10.1038/415757a. PMID   11845200. S2CID   4432164.
  34. "Eric Wieschaus and Christiane Nüsslein-Volhard: Collaborating to Find Developmental Genes". iBiology. Retrieved 13 October 2016.
  35. Cohen, S. M.; Jurgens, G. (1989). "Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less activity in limb development". EMBO J. 8 (7): 2045–2055. doi:10.1002/j.1460-2075.1989.tb03613.x. PMC   401088 . PMID   16453891.
  36. Carroll, Sean B. (2006) [2005]. Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. Weidenfeld & Nicolson [Norton]. pp. 63–70. ISBN   978-0-297-85094-6.
  37. Panganiban, G.; Irvine, S. M.; Lowe, C.; Roehl, H.; Corley, L. S.; Sherbon, B.; Grenier, J. K.; Fallon, J. F.; Kimble, J.; Walker, M.; Wray, G. A.; Swalla, B. J.; Martindale, M. Q.; Carroll, S. B. (1997). "The origin and evolution of animal appendages". Proceedings of the National Academy of Sciences of the United States of America. 94 (10): 5162–5166. Bibcode:1997PNAS...94.5162P. doi: 10.1073/pnas.94.10.5162 . PMC   24649 . PMID   9144208.
  38. "Fluorescent Probes". ThermoFisher Scientific. 2015. Retrieved 12 October 2016.
  39. Land, M. F.; Fernald, R. D. (1992). "The evolution of eyes". Annual Review of Neuroscience . 15: 1–29. doi:10.1146/annurev.ne.15.030192.000245. PMID   1575438.
  40. 1 2 Tomarev, Stanislav I.; Callaerts, Patrick; Kos, Lidia; Zinovieva, Rina; Halder, Georg; Gehring, Walter; Piatigorsky, Joram (1997). "Squid Pax-6 and eye development". Proceedings of the National Academy of Sciences. 94 (6): 2421–2426. Bibcode:1997PNAS...94.2421T. doi: 10.1073/pnas.94.6.2421 . PMC   20103 . PMID   9122210.
  41. 1 2 Pichaud, Franck; Desplan, Claude (August 2002). "Pax genes and eye organogenesis". Current Opinion in Genetics & Development. 12 (4): 430–434. doi:10.1016/S0959-437X(02)00321-0. PMID   12100888.
  42. Drost, Hajk-Georg; Janitza, Philipp; Grosse, Ivo; Quint, Marcel (2017). "Cross-kingdom comparison of the developmental hourglass". Current Opinion in Genetics & Development. 45: 69–75. doi: 10.1016/j.gde.2017.03.003 . PMID   28347942.
  43. 1 2 3 4 5 6 7 8 Carroll, Sean B. (2008). "Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution". Cell. 134 (1): 25–36. doi: 10.1016/j.cell.2008.06.030 . PMID   18614008. S2CID   2513041.
  44. Xu, P.X.; Woo, I.; Her, H.; Beier, D. R.; Maas, R. L. (1997). "Mouse Eya homologues of the Drosophila eyes absent gene require Pax6 for expression in lens and nasal placode". Development. 124 (1): 219–231. doi:10.1242/dev.124.1.219. PMID   9006082.
  45. Quint, Marcel; Drost, Hajk-Georg; Gabel, Alexander; Ullrich, Kristian Karsten; Bönn, Markus; Grosse, Ivo (4 October 2012). "A transcriptomic hourglass in plant embryogenesis". Nature. 490 (7418): 98–101. Bibcode:2012Natur.490...98Q. doi:10.1038/nature11394. ISSN   0028-0836. PMID   22951968. S2CID   4404460.
  46. Mukherjee, K.; Brocchieri, L.; Bürglin, T.R. (December 2009). "A comprehensive classification and evolutionary analysis of plant homeobox genes". Molecular Biology and Evolution. 26 (12): 2775–94. doi:10.1093/molbev/msp201. PMC   2775110 . PMID   19734295.
  47. Bürglin, T.R. (November 1997). "Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals". Nucleic Acids Research. 25 (21): 4173–80. doi:10.1093/nar/25.21.4173. PMC   147054 . PMID   9336443.{{cite journal}}: CS1 maint: uses authors parameter (link)
  48. Derelle, R.; Lopez, P.; Le Guyader, H.; Manuel, M. (2007). "Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes". Evolution & Development. 9 (3): 212–9. doi:10.1111/j.1525-142X.2007.00153.x. PMID   17501745. S2CID   9530210.
  49. 1 2 Russel, Peter (2010). iGenetics: a molecular approach. Pearson Education. pp. 564–571. ISBN   978-0-321-56976-9.
  50. 1 2 Rivera-Pomar, Rolando; Jackle, Herbert (1996). "From gradients to stripes in Drosophila embryogenesis: Filling in the gaps". Trends in Genetics. 12 (11): 478–483. doi:10.1016/0168-9525(96)10044-5. PMID   8973159.
  51. Gerhart, John; Kirschner, Marc (1997). Cells, Embryos and Evolution. Blackwell Science. ISBN   978-0-86542-574-3.
  52. Carroll, Sean B.; Grenier, Jennifer K.; Weatherbee, Scott D. (2005). From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design — Second Edition. Blackwell Publishing. ISBN   978-1-4051-1950-4.
  53. Carroll, Sean B. (2000). "Endless forms: the evolution of gene regulation and morphological diversity". Cell . 101 (6): 577–80. doi: 10.1016/S0092-8674(00)80868-5 . PMID   10892643. S2CID   12375030.
  54. Moczek, Armin P.; et al. (2015). "The Significance and Scope of Evolutionary Developmental Biology: A Vision for the 21st Century" (PDF). Evolution & Development. 17 (3): 198–219. doi:10.1111/ede.12125. hdl: 2027.42/111768 . PMID   25963198. S2CID   9652129. Archived from the original (PDF) on 17 April 2016. Retrieved 27 November 2015.
  55. Abzhanov, A.; Protas, M.; Grant, B.R.; Grant, P.R.; Tabin, C.J. (2004). "Bmp4 and Morphological Variation of Beaks in Darwin's Finches". Science. 305 (5689): 1462–1465. Bibcode:2004Sci...305.1462A. doi:10.1126/science.1098095. PMID   15353802. S2CID   17226774.
  56. Cohn, M.J.; Tickle, C. (1999). "Developmental basis of limblessness and axial patterning in snakes". Nature. 399 (6735): 474–479. Bibcode:1999Natur.399..474C. doi:10.1038/20944. PMID   10365960. S2CID   4309833.
  57. Beverdam, A.; Merlo, G.R.; Paleari, L.; Mantero, S.; Genova, F.; Barbieri, O.; Janvier, P.; Levi, G. (August 2002). "Jaw Transformation With Gain of Symmetry After DLX5/DLX6 Inactivation: Mirror of the Past?" (PDF). Genesis. 34 (4): 221–227. doi:10.1002/gene.10156. hdl: 2318/87307 . PMID   12434331. S2CID   19592597.
  58. Depew, M.J.; Lufkin, T.; Rubenstein, J.L. (October 2002). "Specification of jaw subdivisions by DLX genes". Science. 298 (5592): 381–385. doi:10.1126/science.1075703. PMID   12193642. S2CID   10274300.
  59. Panganiban, Grace; Rubenstein, John L. R. (2002). "Developmental functions of the Distal-less/Dlx homeobox genes". Development. 129 (19): 4371–4386. doi:10.1242/dev.129.19.4371. PMID   12223397.
  60. Beldade, P.; Brakefield, P.M.; Long, A.D. (2002). "Contribution of Distal-less to quantitative variation in butterfly eyespots". Nature. 415 (6869): 315–318. doi:10.1038/415315a. PMID   11797007. S2CID   4430563.
  61. Gerhart, John; Kirschner, Marc (2007). "The theory of facilitated variation". Proceedings of the National Academy of Sciences. 104 (suppl1): 8582–8589. Bibcode:2007PNAS..104.8582G. doi: 10.1073/pnas.0701035104 . PMC   1876433 . PMID   17494755.
  62. Baxter, S.W.; Papa, R.; Chamberlain, N.; Humphray, S.J.; Joron, M.; Morrison, C.; ffrench-Constant, R.H.; McMillan, W.O.; Jiggins, C.D. (2008). "Convergent Evolution in the Genetic Basis of Mullerian Mimicry in Heliconius Butterflies". Genetics. 180 (3): 1567–1577. doi:10.1534/genetics.107.082982. PMC   2581958 . PMID   18791259.
  63. Pennisi, E. (2002). "Evolutionary Biology:Evo-Devo Enthusiasts Get Down to Details". Science. 298 (5595): 953–955. doi:10.1126/science.298.5595.953. PMID   12411686. S2CID   154023266.
  64. Jablonka, Eva; Lamb, Marion (1995). Epigenetic Inheritance and Evolution: The Lamarckian Dimension. Oxford, New York: Oxford University Press. ISBN   978-0-19-854063-2.
  65. West-Eberhard, Mary Jane (2003). Developmental plasticity and evolution. New York: Oxford University Press. ISBN   978-0-19-512235-0.
  66. Müller, Gerd B.; Newman, Stuart A., eds. (2003). Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology. MIT Press.
  67. 1 2 Arthur, W. (July 2001). "Developmental drive: an important determinant of the direction of phenotypic evolution". Evolution & Development. 3 (4): 271–278. doi:10.1046/j.1525-142x.2001.003004271.x. PMID   11478524. S2CID   41698287.
  68. Drost, Hajk-Georg; Janitza, Philipp; Grosse, Ivo; Quint, Marcel (2017). "Cross-kingdom comparison of the developmental hourglass". Current Opinion in Genetics & Development. 45: 69–75. doi: 10.1016/j.gde.2017.03.003 . PMID   28347942.
  69. Arthur, W. (October 2002). "The interaction between developmental bias and natural selection: from centipede segments to a general hypothesis". Heredity. 89 (4): 239–246. doi: 10.1038/sj.hdy.6800139 . PMID   12242638.
  70. Chipman, Ariel D.; Arthur, Wallace; Akam, Michael (July 2004). "A Double Segment Periodicity Underlies Segment Generation in Centipede Development". Current Biology. 14 (14): 1250–1255. doi: 10.1016/j.cub.2004.07.026 . PMID   15268854. S2CID   2371623.
  71. Abouheif, E.; Favé, M.-J.; Ibarrarán-Viniegra, A. S.; Lesoway, M. P.; Rafiqi, A. M.; Rajakumar, R. (2014). "Eco-Evo-Devo: The Time Has Come". In Landry, C.R.; Aubin-Horth, N. (eds.). Ecological Genomics. Ecological Genomics: Ecology and the Evolution of Genes and Genomes. Advances in Experimental Medicine and Biology. Vol. 781. pp. 107–125. doi:10.1007/978-94-007-7347-9_6. ISBN   978-94-007-7346-2. PMID   24277297.
  72. Schlichting, C.D. (2009). "An Uneven Guide to Eco-Devo". BioScience. 59 (11): 1000–1001. doi:10.1525/bio.2009.59.11.12. S2CID   116886911.
  73. Gilbert, S. F.; Bosch, T. C. G.; Ledón-Rettig, C. (2015). "Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents". Nature Reviews Genetics. 16 (10): 611–622. doi:10.1038/nrg3982. PMID   26370902. S2CID   205486234.