Evolutionary developmental biology


Evolutionary developmental biology

Evolutionary developmental biology (evolution of development or informally, evo-devo) is a field of biology that compares the developmental processes of different animals and plants in an attempt to determine the ancestral relationship between organisms and how developmental processes evolved. It addresses the origin and evolution of embryonic development; how modifications of development and developmental processes lead to the production of novel features; the role of developmental plasticity in evolution; how ecology impacts in development and evolutionary change; and the developmental basis of homoplasy and homology.Hall 2000]

Although interest in the relationship between ontogeny and phylogeny extends back to the nineteenth century, the contemporary field of evo-devo has gained impetus from the discovery of genes regulating embryonic development in model organisms. General hypotheses remain hard to test because organisms differ so much in shape and form. Nevertheless, it now appears that just as evolution tends to create new genes from parts of old genes (molecular economy), evo-devo demonstrates that evolution alters developmental processes (genes and gene networks) to create new and novel structures from the old gene networks (such as bone structures of the jaw deviating to the ossicles of the middle ear) or will conserve (molecular economy) a similar program in a host of organisms such as eye development genes in molluscs, insects, and vertebrates [Squid Pax-6 and eye development.Stanislav I. Tomarev,*† Patrick Callaerts,‡ Lidia Kos,§ Rina Zinovieva,¶ Georg Halder,‡ Walter Gehring,‡ and Joram Piatigorsky*. 1997, PNAS.] [Pax genes and eye organogenesis. Franck Pichaud and Claude Desplan. 2002, Science Direct] . Initially the major interest has been in the macroevolutionary evidence of homology in the cellular and molecular mechanisms that regulate body plan and organ development. However more modern approaches include microevolution and developmental changes associated in speciation. [cite journal | author = Pennisi, E | title = EVOLUTIONARY BIOLOGY:Evo-Devo Enthusiasts Get Down to Details| journal = Science | volume = 298 | issue = 5595 | pages = 953–955. | year =2002 | doi = 10.1126/science.298.5595.953 | pmid = 12411686 ]

Introduction

Charles Darwin's theory of evolution is based on three principles: natural selection, heredity, and variation. At the time that Darwin wrote, the principles underlying heredity and variation were poorly understood. In the 1940s, however, biologists incorporated Gregor Mendel's principles of genetics to explain both, resulting in the modern synthesis. It was not until the 1980s and 1990s, however, when more comparative molecular sequence data between different kinds of organisms was amassed and detailed, that an understanding of the molecular basis of the developmental mechanisms has arisen. Currently, it is well understood how genetic mutation occurs. However, developmental mechanisms are not understood sufficiently to explain which kinds of phenotypic variation can arise in each generation from variation at the genetic level. Evolutionary developmental biology studies how the dynamics of development determine the phenotypic variation arising from genetic variation and how that affects phenotypic evolution (specially its direction). At the same time evolutionary developmental biology also studies how development itself evolves. Thus, the origins of evolutionary developmental biology come from both an improvement in molecular biology techniques as applied to development, and the full appreciation of the limitations of classic neo-Darwinism as applied to phenotypic evolution. Some evo-devo researchers see themselves as extending and enhancing the modern synthesis by incorporating into it findings of molecular genetics and developmental biology. Others, drawing on findings of discordances between genotype and phenotype and epigenetic mechanisms of development, are mounting an explicit challenge to neo-Darwinism.

Evolutionary developmental biology is not yet a unified discipline, but can be distinguished from earlier approaches to evolutionary theory by its focus on a few crucial ideas. One of these is modularity: as has been long recognized, plants and animal bodies are modular: they are organized into developmentally and anatomically distinct parts. Often these parts are repeated, such as fingers, ribs, and body segments. Evo-devo seeks the genetic and evolutionary basis for the division of the embryo into distinct modules, and for the partly independent development of such modules.

Another central idea is that some gene products function as switches whereas others act as diffusible signals. Genes specify proteins, some of which act as structural components of cells and others as enzymes that regulate various biochemical pathways within an organism. Most biologists working within the modern synthesis assumed that an organism is a straightforward reflection of its component genes. The modification of existing, or evolution of new, biochemical pathways (and, ultimately, the evolution of new species of organisms) depended on specific genetic mutations. In 1961, however, Jacques Monod, Jean-Pierre Changeux and François Jacob discovered within the bacterium Escherichia coli a gene that functioned only when "switched on" by an environmental stimulus.Monod et al. 1961] Later, scientists discovered specific genes in animals, including a subgroup of the genes which contain the homeobox DNA motif, called Hox genes, that act as switches for other genes, and could be induced by other gene products, morphogens, that act analogously to the external stimuli in bacteria. These discoveries drew biologists' attention to the fact that genes can be selectively turned on and off, rather than being always active, and that highly disparate organisms (for example, fruit flies and human beings) may use the same genes for embryogenesis (e.g., the genes of the "developmental-genetic toolkit", see below), just regulating them differently.

Similarly, organismal form can be influenced by mutations in promoter regions of genes, those DNA sequences at which the products of some genes bind to and control the activity of the same or other genes, not only protein-specifying sequences. In addition to providing new support for Darwin's assertion that all organisms are descended from a common ancestor, this finding suggested that the crucial distinction between different species (even different orders or phyla) may be due less to differences in their content of gene products than to differences in spatial and temporal "expression" of conserved genes. The implication that large evolutionary changes in body morphology are associated with changes in gene regulation, rather than the evolution of new genes, suggested that the action of natural selection on promoters responsive to Hox and other "switch" genes may play a major role in evolution.

Another focus of evo-devo is developmental plasticity, the basis of the recognition that organismal phenotypes are not uniquely determined by their genotypes. If generation of phenotypes is conditional, and dependent on external or environmental inputs, evolution can proceed by a "phenotype-first" route,Palmer 2004] with genetic change following, rather than initiating, the formation of morphological and other phenotypic novelties.

History

In "The Origin of Species" (1859), Charles Darwin proposed evolution through natural selection, a theory central to modern biology. Darwin recognised the importance of embryonic development in the understanding of evolution: cquote|We can see why characters derived from the embryo should be of equal importance with those derived from the adult, for a natural classification of course includes all ages.
Ernst Haeckel (1866), in response to Darwin's theory, proposed that "ontogeny recapitulates phylogeny," that is, the development of the embryo of every species (ontogeny) fully repeats the evolutionary development of that species (phylogeny). Haeckel's concept explained, for example, why humans, and indeed all vertebrates, have gill slits and tails early in embryonic development. While true in general, his theory has been discredited in its absolute form. However, it served as a backdrop for a renewed interest in the evolution of development after the modern evolutionary synthesis was established (roughly 1936 to 1947).

Stephen Jay Gould called this approach to explaining evolution as "terminal addition"; as if every evolutionary advance was added as new stage by reducing the duration of the older stages. The idea was based on observations of neoteny. [Ridley, Mark (2003) Evolution. Third Edition. [http://www.blackwellpublishing.com/ridley/] ] This was extended by the more general idea of heterochrony (changes in timing of development) as a mechanism for evolutionary change;Gould 1977]

D'Arcy Thompson postulated that differential growth rates could produce variations in form in his 1917 book "On Growth and Form". He showed the underlying similarities in "body plans" and how geometric "transformations" could be used to explain the variations.

Edward B. Lewis discovered homeotic genes, rooting the emerging discipline of evo-devo in molecular genetics. In 2000, a special section of the Proceedings of the National Academy of Sciences (PNAS) was devoted to "evo-devo",Goodman and Coughlin 2000] and an entire 2005 issue of the Journal of Experimental Zoology Part B: Molecular and Developmental Evolution was devoted to the key evo-devo topics of evolutionary innovation and morphological novelty.Müller and Newman 2005]

The developmental-genetic toolkit

The developmental-genetic toolkit consists of genes whose products control the development of a multicellular organism. Differences in deployment of toolkit genes affect the body plan and the number, identity, and pattern of body parts. The toolkit is highly conserved across animal phyla. Only a small fraction of the genes in the genome are involved in development. The majority of toolkit genes are components of signaling pathways, and encode for the production of transcription factors, cell adhesion proteins, cell surface receptor proteins, and secreted morphogens. Their function is highly correlated with their spatial and temporal expression patterns. One of the major goals of evo-devo is to catalogue all genes (their identity, product, function, and interaction) in the toolkit.

Among the most important of the toolkit genes are those of the Hox gene cluster, or complex. Hox genes, transcription factors containing the more broadly distributed homeobox protein-binding DNA motif, function in patterning the body axis. Thus, by combinatorially specifying the identity of particular body regions, Hox genes determine where limbs and other body segments will grow in a developing embryo or larva.
Mutations in any one of these genes can lead to the growth of extra, typically non-functional body parts in invertebrates, for example aristapedia complex in "Drosophila," which results in a leg growing from the head in place of an antenna and is due to a defect in a single gene (this mutation is also known as Antennapedia).

Development and the origin 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 Gerhart and Kirschner have noted, there is an apparent paradox: "where we most expect to find variation, we find conservation, a lack of change".Gerhart and Kirschner 1997]

Even within a species, the occurrence of novel forms within a population does not generally correlate with levels of genetic variation sufficient to account for all morphological diversity. For example, there is significant variation in limb morphologies amongst salamanders and in differences in segment number in centipedes, even when the respective genetic variation is low.

A major question then, for evo-devo studies, is: If the morphological novelty we observe at the level of different clades is not always reflected in the genome, where does it come from? Apart from neo-Darwinian mechanisms such as mutation, translocation and duplication of genes, novelty may also arise by mutation-driven changes in gene regulation. The finding that much biodiversity is not due to differences in genes, but rather to alterations in gene regulation, has introduced an important new element into evolutionary theory.Carroll et al., 2005 ] Diverse organisms may have highly conserved developmental genes, but highly divergent regulatory mechanisms for these genes. Changes in gene regulation are "second-order" effects of genes, resulting from the interaction and timing of activity of gene networks, as distinct from the functioning of the individual genes in the network.

The discovery of the homeotic Hox gene family in vertebrates in the 1980s allowed researchers in developmental biology to empirically assess the relative roles of gene duplication and gene regulation with respect to their importance in the evolution of morphological diversity. Several biologists, including Sean B. Carroll of the University of Wisconsin-Madison suggest that "changes in the cis-regulatory systems of genes" are more significant than "changes in gene number or protein function".Carroll 2000] These researchers argue that the combinatorial nature of transcriptional regulation allows a rich substrate for morphological diversity, since variations in the level, pattern, or timing of gene expression may provide more variation for natural selection to act upon than changes in the gene product alone.

Epigenetic alterations of gene regulation or phenotype generation that are subsequently consolidated by changes at the gene level constitute another class of mechanisms for evolutionary innovation. Epigenetic changes include modification of the genetic material due to methylation and other reversible chemical alteration Jablonka and Lamb 1995] , as well as nonprogrammed remolding of the organism by physical and other environmental effects due to the inherent plasticity of developmental mechanisms.West-Eberhard 2003] 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.Müller and Newman 2003]

ee also

* Developmental biology
* Animal evolution
* Plant Evolutionary Developmental Biology
* Baldwin effect
* Developmental systems theory
* Evolution of multicellularity
* Genetic assimilation
* Ontogeny
* Ontogeny recapitulates phylogeny
* List of gene families
* Important publications in evolutionary developmental biology
* Evolution and Development Leading journal
* Body plan
* Cell signaling
* Signal transduction
* Cell signaling networks
* Transcription factor
* Enhancer
* Enhanceosome
* Promoter
* Gene regulatory network

Notes

References

*cite journal | author=Carroll SB | title=Endless forms: the evolution of gene regulation and morphological diversity | journal=Cell | year=2000 | pages=577–80 | volume=101 | doi=10.1016/S0092-8674(00)80868-5
*cite book | author=Carroll SB | year=2005 |title=Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom | publisher=Norton
*cite book | author=Carroll SB Jennifer K. Grenier, Scott D. Weatherbee | year=2004 | title=From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design | edition=2nd ed. | publisher=Norton
*cite book | author=Gerhart J and Kirschner M | year=1997 | title= Cells, Embryos and Evolution| publisher=Blackwell Science
*cite journal | author=Goodman CS and Coughlin BS (Eds). |title=Special feature: The evolution of evo-devo biology | journal=Proceedings of the National Academy of Sciences | year=2000 | volume=97 | pages=4424–4456|url=http://www.pnas.org/cgi/content/full/97/9/4424 |doi=10.1073/pnas.97.9.4424 |pmid=10781035
*cite book | author=Gould SJ | year=1977| title=Ontogeny and Phylogeny| publisher=Harvard University Press
*cite journal | author=Hall BK | title=Evo-devo or devo-evo--does it matter | journal=Evolution & Development | year=2000 | pages=177–178 | volume=2 | doi=10.1046/j.1525-142x.2000.00003e.x
*cite book | author=Kirschner M and Gerhart J| year=2005 | title= The Plausibility of Life: Resolving Darwin's Dilemma| publisher=Yale University Press
*cite journal | author=Monod J, Changeux JP, Jacob F | year=1963 | title=Allosteric proteins and cellular control systems |journal=Journal of Molecular Biology | volume=6 | pages=306–329
*cite book | author= Müller GB and Newman SA (Eds.) | year=2003 | title= | publisher=MIT Press
*cite journal | author=Müller GB and Newman SA (Eds.) |title=Special issue: Evolutionary Innovation and Morphological Novelty | journal=Journal of Exp. Zool. Part B: Molecular and Developmental Evolution | year=2005 | volume=304B | pages=485–631|url=http://www3.interscience.wiley.com/cgi-bin/jissue/112149101
*cite journal | author=Palmer RA | title=Symmetry breaking and the evolution of development | journal=Science | year=2004 | pages=828–833 | volume=306 | doi=10.1126/science.1103707 | pmid=15514148
*cite book| author=West-Eberhard MJ |year=2003 | title=Developmental Plasticity and Evolution | publisher=Oxford University Press

Further reading

*cite book | author=Leo W. Buss | year=1987 | title=The Evolution of Individuality | publisher=Princeton University Press
*cite book| author=Brian Goodwin | year=1994 | title=How the Leopard Changed its Spots | publisher=Phoenix Giants
*cite book | author=Stephen Jay Gould | year=1977 | title=Ontogeny and Phylogeny | publisher=Harvard University Press
*cite book |author=Manfred D. Laubichler and Jane Maienschein, eds. | title=From Embryology to Evo-Devo: A History of Developmental Evolution | year=2007 | publisher=The MIT Press | id=ISBN 978-0-262-12283-2
*cite book | author=Alessandro Minelli | year=2003 | title=The Development of Animal Form: Ontogeny, Morphology, and Evolution | publisher=Cambridge University Press
* H. Allen Orr, [http://www.newyorker.com/critics/books/articles/051024crbo_books1 "Turned on: A revolution in the field of evolution?"] , The New Yorker, 10/24/2005. Discussion of Carroll, Endless Forms Most Beautiful
*cite book | author=Rudolf A. Raff | year=1996 | title=The Shape of Life: Genes, Development, and the Evolution of Animal Form | publisher=The University of Chicago Press

External links

* Scott F. Gilbert, [http://www.ijdb.ehu.es/fullaccess/fulltext.03078/ft467.pdf The morphogenesis of evolutionary developmental biology]


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