Evolutionary developmental biology, informally known asevo-devo, is a field ofbiological research that compares thedevelopmental processes of differentorganisms to infer how developmental processesevolved.
The field grew from 19th-century beginnings, whereembryology faced a mystery:zoologists did not know howembryonic 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 withmolecular genetics. A key early discovery was that ofhomeotic genes that regulate development in a wide range ofeukaryotes.
The field is composed of multiple core evolutionary concepts. One isdeep homology, the finding that dissimilar organs such as the eyes ofinsects,vertebrates andcephalopod molluscs, long thought to have evolved separately, are controlled by similar genes such aspax-6, from theevo-devo gene toolkit. These genes are ancient, beinghighly conserved amongphyla; they generate the patterns in time and space which shape the embryo, and ultimately form thebody plan of the organism. Another is that species do not differ much in their structural genes, such as those coding forenzymes; what does differ is the way thatgene expression is regulated by thetoolkit 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 multiplepleiotropic reuse explains why these genes are highly conserved, as any change would have many adverse consequences whichnatural selection would oppose.
Newmorphological 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 theneo-Lamarckian theory thatepigenetic changes are laterconsolidated at gene level, something that may have been important early in the history of multicellular life.
Philosophers began to think about how animals acquired form in thewomb inclassical antiquity.Aristotle asserts in hisPhysics treatise that according toEmpedocles, order "spontaneously" appears in the developing embryo. In hisThe Parts of Animals treatise, he argues that Empedocles' theory was wrong. In Aristotle's account, Empedocles stated that thevertebral column is divided into vertebrae because, as it happens, the embryo twists about and snaps the column into pieces. Aristotle argues instead that the process has a predefined goal: that the "seed" that develops into the embryo began with an inbuilt "potential" to become specific body parts, such as vertebrae. Further, each sort of animal gives rise to animals of its own kind: humans only have human babies.[2]
Arecapitulation theory of evolutionary development was proposed byÉtienne Serres in 1824–26, echoing the 1808 ideas ofJohann 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 thegreat chain of being. For example, the brain of a human embryo looked first like that of afish, then in turn like that of areptile,bird, andmammal before becoming clearlyhuman. The embryologistKarl Ernst von Baer opposed this, arguing in 1828 that there was no linear sequence as in the great chain of being, based on a singlebody plan, but a process ofepigenesis in which structures differentiate. Von Baer instead recognized four distinct animalbody plans: radiate, likestarfish; molluscan, likeclams; articulate, likelobsters; and vertebrate, like fish. Zoologists then largely abandoned recapitulation, thoughErnst Haeckel revived it in 1866.[4][5][6][7][8]
From the early 19th century through most of the 20th century,embryology faced a mystery. Animals were seen to develop into adults of widely differingbody plan, often through similar stages, from the egg, but zoologists knew almost nothing about howembryonic development was controlled at themolecular level, and therefore equally little about howdevelopmental processes had evolved.[9]Charles Darwin argued that a shared embryonic structure implied a common ancestor. For example, Darwin cited in his 1859 bookOn the Origin of Species theshrimp-likelarva of thebarnacle, whosesessile adults looked nothing like otherarthropods;Linnaeus andCuvier had classified them asmolluscs.[10][11] Darwin also notedAlexander Kowalevsky's finding that thetunicate, too, was not a mollusc, but in its larval stage had anotochord and pharyngeal slits which developed from the same germ layers as the equivalent structures invertebrates, and should therefore be grouped with them aschordates.[10][12]
19th century zoology thus convertedembryology into an evolutionary science, connectingphylogeny withhomologies between the germ layers of embryos. Zoologists includingFritz Müller proposed the use of embryology to discoverphylogenetic relationships between taxa. Müller demonstrated thatcrustaceans shared theNauplius larva, identifying several parasitic species that had not been recognized as crustaceans. Müller also recognized thatnatural 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.[10] 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.[13][14][15]
In 1917,D'Arcy Thompson wrotea book on the shapes of animals, showing with simplemathematics how small changes toparameters, such as the angles of agastropod's spiral shell, can radically alteran animal's form, though he preferred a mechanical to evolutionary explanation.[17][18] But without molecular evidence, progress stalled.[10]
In 1952,Alan Turing published his paper "The Chemical Basis of Morphogenesis", on the development of patterns in animals' bodies. He suggested thatmorphogenesis could be explained by areaction–diffusion system, a system of reacting chemicals able to diffuse through the body.[16] He modelled catalysed chemical reactions usingpartial differential equations, showing that patterns emerged when the chemical reaction produced both acatalyst (A) and aninhibitor (B) that slowed down production of A. If A and B then diffused at different rates, A dominated in some places, and B in others. The Russian biochemistBoris Belousov had run experiments with similar results, but was unable to publish them because scientists thought at that time that creating visible order violated thesecond law of thermodynamics.[19]
In the so-calledmodern synthesis of the early 20th century, between 1918 and 1930Ronald Fisher brought together Darwin's theory ofevolution, with its insistence on natural selection,heredity, andvariation, andGregor Mendel'slaws of genetics into a coherent structure forevolutionary 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 throughmutations in these genes. It was a simple, clear and nearly comprehensive picture: but it did not explain embryology.[10][20]Sean B. Carroll has commented that had evo-devo's insights been available, embryology would certainly have played a central role in the synthesis.[1]
The evolutionary embryologistGavin de Beer anticipated evolutionary developmental biology in his 1930 bookEmbryos and Ancestors,[21] by showing that evolution could occur byheterochrony,[22] such as inthe retention of juvenile features in the adult.[13] This, de Beer argued, could cause apparently sudden changes in thefossil 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.[23] 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.[24][25][a]
In 1961,Jacques Monod,Jean-Pierre Changeux andFrançois Jacob discovered thelac operon in thebacteriumEscherichia coli. It was a cluster ofgenes, arranged in a feedbackcontrol loop so that its products would only be made when "switched on" by an environmental stimulus. One of these products wasan enzyme that splits a sugar, lactose; andlactose 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.[27]
In 1977, a revolution in thinking about evolution and developmental biology began, with the arrival ofrecombinant DNA technology ingenetics, the bookOntogeny and Phylogeny byStephen J. Gould and the paper"Evolution and Tinkering"[28] byFrançois Jacob. Gould laid to rest Haeckel's interpretation of evolutionary embryology, while Jacob set out an alternative theory.[10] This led toa second synthesis,[29][30] at last including embryology as well asmolecular genetics, phylogeny, and evolutionary biology to form evo-devo.[31][32] In 1978,Edward B. Lewis discoveredhomeotic genes that regulate embryonic development inDrosophila fruit flies, which like all insects arearthropods, one of the majorphyla of invertebrate animals.[33]Bill McGinnis quickly discovered homeotic gene sequences,homeoboxes, in animals in other phyla, invertebrates such asfrogs,birds, andmammals; they were later also found infungi such asyeasts, and inplants.[34][35] There were evidently strong similarities in the genes that controlled development across all theeukaryotes.[36]In 1980,Christiane Nüsslein-Volhard andEric Wieschaus describedgap genes which help to create the segmentation pattern infruit fly embryos;[37][38] they and Lewis won aNobel Prize for their work in 1995.[34][39]
Later, more specific similarities were discovered: for example, thedistal-less gene was found in 1989 to be involved in the development of appendages or limbs in fruit flies,[40] the fins of fish, the wings of chickens, theparapodia of marineannelid worms, the ampullae and siphons of tunicates, and thetube feet ofsea urchins. It was evident that the gene must be ancient, dating back to thelast common ancestor of bilateral animals (before theEdiacaran Period, which began some 635 million years ago). Evo-devo had started to uncover the ways that all animal bodies were built during development.[41][42]
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. Thegiraffe does not have a gene for a long neck, any more than theelephant 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.[9]
The puzzle of how embryonic development was controlled began to be solved using the fruit flyDrosophila melanogaster as amodel organism. The step-by-step control ofits embryogenesis was visualized by attachingfluorescent dyes of different colours to specific types of protein made by genes expressed in the embryo.[9] A dye such asgreen fluorescent protein, originally froma jellyfish, was typically attached to anantibody specific to a fruit fly protein, forming a precise indicator of where and when that protein appeared in the living embryo.[43]
Using such a technique, in 1994Walter Gehring found that thepax-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 assquid, acephalopodmollusc. Biologists includingErnst 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.[9] For example, the fruit fly'scompound eye is made of hundreds of small lensed structures (ommatidia); thehuman eye has ablind spot where theoptic nerve enters the eye, and the nerve fibres run over the surface of theretina, 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".[44] The evidence ofpax-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.[9]Ancient genes had beenconserved through millions of years of evolution to create dissimilar structures for similar functions, demonstratingdeep homology between structures once thought to be purely analogous.[45][46] This notion was later extended to the evolution ofembryogenesis[47] and has caused a radical revision of the meaning of homology in evolutionary biology.[45][46][1]
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 amongphyla, 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 ofsignalling pathways: they encodetranscription factors,cell adhesion proteins, cell surfacereceptor proteins and signallingligands that bind to them, and secretedmorphogens 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 thebody plan of the organism. Among the most important toolkit genes are theHox genes. These transcription factors contain thehomeobox protein-binding DNA motif, also found in other toolkit genes, and create the basic pattern of the body along its front-to-back axis.[1]Hox genes determine where repeating parts, such as the manyvertebrae ofsnakes, will grow in a developing embryo or larva.[9]Pax-6, already mentioned, is a classic toolkit gene.[48] Although other toolkit genes are involved in establishing the plantbodyplan,[49]homeobox genes are also found in plants, implying they are common to alleukaryotes.[50][51][52]
The protein products of the regulatory toolkit are reused not by duplication and modification, but by a complex mosaic ofpleiotropy, being applied unchanged in many independent developmental processes, giving pattern to many dissimilar body structures.[1] The loci of these pleiotropic toolkit genes have large, complicated and modularcis-regulatory elements. For example, while a non-pleiotropicrhodopsin gene in the fruit fly has a cis-regulatory element just a few hundredbase pairs long, the pleiotropiceyeless cis-regulatory region contains 6 cis-regulatory elements in over 7000 base pairs.[1] Theregulatory 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.[1] 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.[1]
Such a cascading regulatory network has been studied in detail in thedevelopment of the fruit fly embryo. The young embryo is oval in shape, like arugby ball. A small number of genes producemessenger RNAs that set up concentration gradients along the long axis of the embryo. In the early embryo, thebicoid andhunchback genes are at high concentration near the anterior end, and give pattern to the future head and thorax; thecaudal andnanos 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 ofcaudal'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.[53][54]
The Bicoid, Hunchback and Caudal proteins in turn regulate the transcription ofgap genes such asgiant,knirps,Krüppel, andtailless in a striped pattern, creating the first level of structures that will become segments.[37] The proteins from these in turn control thepair-rule genes, which in the next stage set up 7 bands across the embryo's long axis. Finally, the segment polarity genes such asengrailed split each of the 7 bands into two, creating 14 future segments.[53][54]
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.[1]
The mechanism that sets up everyanimal's front-back axis is the same, implying a common ancestor. There is a similar mechanism for the back-belly axis forbilaterian animals, but it is reversed betweenarthropods andvertebrates.[55] Another process,gastrulation of the embryo, is driven byMyosin II molecular motors, which are not conserved across species. The process may have been started by movements of sea water in the environment, later replaced by the evolution of tissue movements in the embryo.[56][57]
Among the more surprising and, perhaps, counterintuitive (from aneo-Darwinian viewpoint) results of recent research in evolutionary developmental biology is that the diversity ofbody plans andmorphology in organisms across manyphyla 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".[58] So, if the observed morphological novelty between differentclades does not come from changes in gene sequences (such as bymutation), where does it come from? Novelty may arise by mutation-driven changes ingene regulation.[1][59][60][61]
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'slarge ground-finch was enlarged by theBMP gene,[62] or when snakes lost their legs asdistal-less became under-expressed or not expressed at all in the places where other reptiles continued to form their limbs.[63] 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,[64][65] legs and antennae in the fruit fly,[66] andeyespot pattern inbutterflywings.[67] Given that small changes in toolbox genes can cause significant changes in body structures, they have often enabled the same functionconvergently orin parallel.distal-less generates wing patterns in the butterfliesHeliconius erato andHeliconius melpomene, which areMüllerian mimics. In so-calledfacilitated variation,[68] their wing patterns arose in different evolutionary events, but are controlled by the same genes.[69] Developmental changes can contribute directly tospeciation.[70]
Evolutionary innovation may sometimes beginin Lamarckian style withepigenetic alterations of gene regulation orphenotype generation, subsequentlyconsolidated by changes at the gene level. Epigenetic changes include modification of DNA by reversible methylation,[71] as well as nonprogrammed remoulding of the organism by physical and other environmental effects due to the inherentplasticity of developmental mechanisms.[72] The biologistsStuart A. Newman andGerd 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 earlymacroevolutionary changes.[73]
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Development in specific lineages can be biased either positively, towards a given trajectory or phenotype,[b] 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.[47] For example, in thegastropods, 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 thecentipedes, theLithobiomorpha always have 15 trunk segments as adults, probably the result of a developmental bias towards an odd number of trunk segments. Another centipede order, theGeophilomorpha, 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.[74][75][76]
Ecological evolutionary developmental biology, informally known as eco-evo-devo, integrates research from developmental biology andecology to examine their relationship with evolutionary theory.[77] Researchers study concepts and mechanisms such asdevelopmental plasticity,epigenetic inheritance,genetic assimilation,niche construction andsymbiosis.[78][79]
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.
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