Developmental Evolution

Developmental Evolution

Introductory article Article contents

Susan Lindsay, University of Newcastle upon Tyne, Newcastle-upon-Tyne, UK Development and evolution are superficially similar in that both deal with change. In the past, the study of comparative embryology was used as a powerful argument both for and against evolution. More recently, experimental approaches are being used to address questions at a molecular genetic level in both evolutionary and developmental biology studies. The data and ideas generated have led to attempts to synthesize the two disciplines that have been very fruitful, if only partially successful, to date.

Introduction

 Introduction  New Synthesis between Development and Evolution  Future Directions

doi: 10.1038/npg.els.0005112

Differences between developmental and evolutionary research

Historical perspective The idea that organisms carry within them their evolutionary history is not new and, at one level, seems obvious. However, the complexities begin when one thinks about when during an organism’s lifetime one might find such evolutionary traces and, of course, what the mechanisms involved could be. The possibility of major evolutionary change occurring during development has been discussed since Darwin’s time and was famously encapsulated in Haeckel’s ‘biogenetic law’, paraphrased as ‘ontogeny recapitulates phylogeny’. (See Darwin, Charles.) During the nineteenth century, debate raged about evolution, and evidence for and against was sought in comparative studies of the embryology of a wide variety of different species. By the beginning of the twentieth century, the two disciplines of developmental biology and evolutionary biology began to be concerned with different problems and to use different methodologies to address them. Developmental biology moved from being largely based on comparative anatomical studies to an experimental approach, principally under the influence of the pioneering anatomist and physiologist Wilhelm Roux. On the other hand, studies on the genetics of populations and the hypotheses that flowed from these had a considerable impact on evolutionary biology. Darwin and others in the nineteenth century raised the possibility that the mechanisms of inheritance would provide a link between the development of individual organisms and the evolution of species. By the twentieth century, however, it was the genetics of populations that engaged evolutionary biologists, while developmental biologists initially were little concerned with genetics, and when they did become interested, it was in the action of individual genes within cells. (See Homologous, Orthologous and Paralogous Genes; Hox Genes and Body Plan: Evolution.)

There are, of course, fundamental differences between evolution and development. These were summarized by Raff and his colleagues, in an article heralding the publication of a new journal dedicated to the emerging discipline of evolution and development, as follows: Evolution is an unprogrammed, nonrepeating historical process, whereas development is a predictable process repeated in each life-cycle.

At the genetic level, these differences may also be fundamental; for example, are the same genes involved in ‘minor’ phenotypic variation (thought to be the substrate of evolution) as in major developmental events? Moreover, evolutionary biologists focus on studying the diversity of life and attempt to understand how this has arisen. Developmental biologists, on the other hand, search for universal principles underlying developmental processes, a famous example of which (now much modified) is Haeckel’s biogenetic law, discussed in the section Historical perspective. In the 1980s, scientists studying a set of important developmental genes, the homeotic genes, in the fruit fly (Drosophila melanogaster) showed that there were related genes in other species, not only insects and other invertebrates, but also vertebrates. This was an astonishing discovery, because it showed that there had been conservation of genes across a huge period of evolutionary time. This discovery greatly strengthened the hypothesis that there are universal principles in development and, of course, that the underlying mechanisms involve genes. As a side effect, the assumption that universal developmental principles can be established from studying a few ‘model’ organisms also became enshrined. Table 1 highlights the differences between evolutionary and developmental research.

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Developmental Evolution Table 1 Summary of differences in developmental and evolutionary studies Feature

Development

Evolution

Timescale

Individual organism’s life cycle

Usually measured in millions of years

Nature of change

Programmed and reproducible

Unprogrammed and nonreproducible

Genes

Relate to functions within and between cells

Substrate for change

Effect of mutation

Usually deleterious

Basis for change

Species studied

Usually development of only a few ‘model’ organisms has been studied

Many species studied

Approach

Experimental

Descriptive and comparative

Goals

To understand how a complex organism arises from a single cell

To understand how the wide diversity of species has arisen and are related, and the underlying mechanisms of change

Homologies among developmental genes and gene families have now been found in many species, and genetic conservation has been found over and over again. The initial observation in the Hox gene family led to an explosion of research, and many key discoveries have been made, both at the level of understanding basic developmental processes and in identifying and analyzing genes underlying human genetic disorders. (See Hox Genes: Embryonic Development.)

New Synthesis between Development and Evolution Connections and disconnections Development has been studied for centuries, while evolution has a history as a formal subject for study dating back only to the nineteenth century, with the publication by Charles Darwin in 1859 of The Origin of Species by Means of Natural Selection, identified as a convenient starting point. Since the initial period, when the fields of developmental and evolutionary biology overlapped (and generated much fierce debate), and the following decades of the twentieth century, when they went their separate ways, there has again been a great deal of interest in bringing the two fields together. This reawakening of interest began in the 1980s and has been accelerating ever since, to the extent that a new research field has emerged, evolutionary developmental biology or ‘evo-devo’. As the name may suggest, to date there has probably been more interest from the evolutionary side, but this is changing, particularly as information is gained from large-scale gene expression studies (see the section on Gene expression). To bring the fields of developmental and evolutionary biology together needed both the emergence of new ideas as well as of new technologies. Two ideas, in

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particular, were crucial, as were (and still are) the techniques of molecular genetics, which are becoming ever more sophisticated and powerful. The first idea, proposed by Morgan in the early twentieth century, was that evolution can act at any stage in an organism’s life, including its development. Previously, it had been thought that evolution acted only on later developmental stages, as these are most likely to be where species-specific features arise, and on adult characteristics, as these would be most relevant for ecological adaptations and speciation. Studies of marine invertebrates led scientists to realize that larval stages too could be subject to evolutionary pressures and to extend this idea to other developmental stages and species. Developmental biologists had shown that Haeckel’s idea of a strict recapitulation of ancestral evolutionary stages during an organism’s development was incorrect. An earlier proposal by von Baer, however, that during development embryos pass through a stage that is characteristic of the phylum to which they belong, has endured to the present day. This has been designated the phylotypic stage. In vertebrates, a phylotypic stage has been proposed during which vertebrate embryos appear morphologically similar. Although this idea has been much debated, and one modification offered is that of a phylotypic period rather than a phylotypic stage, it is a fruitful area to explore, as one possible implication is that there has been evolutionary pressure to sustain it. Another possibility is that this stage or period might not be amenable to evolutionary change. One of the arguments against evolution, raised by Georges Cuvier, the famous French anatomist, was that of integration of function; that is, since all aspects of an organism’s development are interrelated, altering one part would inevitably have consequences throughout the rest of the body and one or more of these would always be deleterious. The second idea important to the

Developmental Evolution

synthesis of evolution and development directly addressed this problem and proposed that development consisted of modules that could be dissociated, that is, they could evolve independent of each other. This concept of dissociation was first proposed by Joseph Needham in the 1930s. Currently, there is no consensus as to what a module is or what it might do, but modules are perceived as existing at different levels, for example, involving the action of specific genes, or genetic pathways, cell types or tissues. The idea of dissociable modules of development has proved a very powerful one. It encompasses the striking gene sequence homologies between species (e.g. of Hox genes) that have already played such a crucial part in modern molecular developmental biology, as well as providing mechanisms that can explain how the morphology of one species changes into that of another, one of the major goals of evolutionary biologists. Moreover, with new molecular genetic technologies, these mechanisms can be tested. Thus, comparative molecular genetic studies during development and across evolution have become a driving force in improving understanding in the same way that comparative anatomical studies were nearly two centuries ago. (See Hox Genes and Body Plan: Evolution; Hox Genes: Embryonic Development.)

Mechanisms of developmental evolution Three mechanisms of dissociation have been proposed: 1. Heterochrony: Originally this term was applied by Haeckel to developmental features that appeared out of their correct recapitulatory sequence. When the idea of strict recapitulation during development became discredited, the term was redefined by De Beer as ‘a change in developmental timing of an organ or feature relative to the same structure in an ancestor’. 2. Duplication and divergence: In 1970, Susumo Ohno suggested that genes could be duplicated and that the duplicated copy, freed from the constraints of performing the function required of the original gene, is likely to acquire mutations. Although in many cases the mutations will be deleterious, in other cases they may lead to new gene functions. 3. Co-option: The use of preexisting features in new features or structures. (See Gene Families: Formation and Evolution.) Of these, heterochrony has received the most attention, with some authors going so far as to declare that heterochrony is the mechanism underlying all developmental evolution. With the expansion in the number of studies addressing heterochrony, confusion

has crept into the literature about its definition, with some authors applying it to changes in rates of developmental processes rather than alterations in the timing of appearances of developmental features themselves. This can have significant consequences for the interpretation of the underlying mechanisms involved. The new tools of molecular genetics, particularly as they are applied in studies of gene expression patterns, should help to clarify the underlying mechanisms and to make explicit what exactly has altered in the development of one species compared to another. Molecular genetic evidence is also leading to a re-evaluation of the idea that heterochrony is the most prevalent mechanism in developmental evolution.

Gene expression When Jacob and Monod proposed the operon theory, they showed how differential expression of genes could be achieved using the same genomic deoxyribonucleic acid (DNA) as a blueprint. This is crucially important if genes are to have a central role in controlling a program of development. Thus, alterations in the regulation of gene expression could provide a means of setting up heterochronies. But more than that, such alterations could also be important in the other proposed mechanisms of dissociation, that is, duplication and divergence, and co-option. Alterations in the regulation of gene expression could mean that developmental genes are expressed at different times or in different places (e.g. different cell types or tissues) in the embryo. Furthermore, differences in gene regulation could mean that different members of a gene family were involved in a specific function in related species. Clearly, in order to make evolutionary comparisons, data have to be extrapolated from expression patterns in existing species, ideally from as wide a variety of these as possible. More and more data are accumulating on gene expression patterns during development, albeit usually in a few model organisms (e.g. mouse, chick, Xenopus and zebrafish for vertebrates). Some human developmental data are also available for comparison. Clear differences in gene expression patterns have been found; for example, in the highly conserved Wnt gene family of developmental regulators, there are differences in the timing and position of expression for some members, even between two mammalian species (mouse and human). Although there is no clear consensus as to what a module is, in order for there to be dissociability of developmental modules there must be dissociability of the molecular components of these modules. Even the limited comparative gene expression data that are

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Developmental Evolution

available to date provide evidence that this is the case and emphasize the importance of alterations in gene regulation as a mechanism in developmental evolution. (See Promoters: Evolution.)

Advantages of a developmental evolution synthesis Adding an evolutionary perspective should help to counterbalance the prevailing tendency of developmental biologists (and geneticists) to study a few ‘model organisms’ and generalize from there. Evolutionary thinking may encourage a wider variety of species to be studied, at least in sufficient detail, to enable the ‘idiosyncrasies’ of the current chosen model organisms to be identified. Furthermore, such comparative molecular embryology should help to identify processes, pathways or principles that are, indeed, universal (within a phylum or between phyla) and distinguish these from ones that are specific to more closely related species. Evolutionary thinking may also help to challenge prevailing assumptions, for example that, because the same genes are expressed in a given tissue or involved in a specific developmental process, they are performing the same functions in the same pathways. The developmental biologists’ perspective, particularly the search for unifying principles and commonalities among species, challenges the evolutionary biologist in that it suggests that there may be a nonrandom element in the way that developmental systems respond to evolutionary change. The question is whether natural selection can elicit responses in any direction from the mutations that appear in organisms, or if evolution is somehow constrained by existing developmental and genetic systems. Thus, developmental constraints might act to channel change in preferred ways and not act merely as a means of inhibiting advantageous alteration. If this is the case, then a potentially important principle of developmental evolution has emerged. Supporting evidence might come from the fact that there are fewer genes than were expected in the human genome: the number is now estimated to be between 30 000 and 40 000 genes. It appears that humans, at least, use a relatively limited number of genes in a variety of ways (such as alternative splicing, alternative promoter usage, and use of the same genes and pathway elements in different tissues and at different stages) to produce the ordered and highly complex changes required during development. Again, detailed comparative molecular studies during development in a variety of species may tell us whether there is directionality or there are constraints in the way that developmental systems have changed during evolution.

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Future Directions As the Human Genome Project and other genome projects provide detailed sequence information in several species, molecular comparisons at the DNA level have become considerably easier. Many researchers are now addressing the question of the function of genes, both within their species of interest and across different species. The new array technologies that allow many DNA sequences to be analyzed at once hold great promise. Microarray profiling will enable us to assess the changing expression patterns of many genes simultaneously during development. As the technology becomes more accessible, this should facilitate experiments being carried out in a wider range of species, in different developing tissues and at a variety of time points. In this way, we should have the ability to analyze both activities and interactions of many genes and thus build up a picture that much more closely resembles the developmental system under study in vivo. In theory, the increasing ease with which large volumes of data can be gathered should enable evolutionary questions also to be addressed experimentally. The tools, therefore, are now available for an experimental evolutionary developmental biology approach. (See DNA Chip Revolution; DNA Chips and Microarrays.) There are difficulties with trying to synthesize two disparate disciplines, particularly those that have had very different concerns for almost 100 years and use very different vocabularies and underlying modes of thought. However, for both developmental biologists and evolutionary biologists, there is a great deal to be gained from the synthesis, especially at this time when molecular genetic tools of great power and sophistication are available and when, for the foreseeable future, lack of data should not be the problem!

See also Evolution: Views of Evolutionary Thinking in the Medical Sciences

Further Reading Carroll SB, Grenier JK and Weatherbee SD (2001) From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Oxford, UK: Blackwell Publishing. Christen B and Slack JM (1998) All limbs are not the same. Nature 395: 230–231. DuBoule D and Wilkins AS (1998) The evolution of ‘bricolage’. Trends in Genetics 14: 54–59. Fougerousse F, Bullen P, Herasse M, et al. (2000) Human–mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Human Molecular Genetics 9: 165–173.

Developmental Evolution Gould SJ (1992) Ontogeny and phylogeny revisited and reunited. Bioessays 14: 275–279. Gould SJ (2000) Of coiled oysters and big brains: how to rescue the terminology of heterochrony, now gone astray. Evolution and Development 2: 241–248. Raff RA (1996) The Shape of Life: Genes, Development and the Evolution of Animal Form. Chicago, IL: University of Chicago Press.

Raff RA, Arthur W, Carroll SB, Coates MI and Wray G (1999) Chronicling the birth of a discipline. Evolution and Development 1: 1–2. Raff EC and Raff RA (2000) Dissociability, modularity and evolution. Evolution and Development 2: 235–237. Richardson MK (1995) Heterochrony and the phylotypic period. Developmental Biology 172: 412–421.

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