The understanding of the genetic bases of development has increased dramatically during the past 30 years. Interest in development had not always come, as in the case of the constraint school, from the perception that there is a conflict between our current understanding of morphological variation and development and the conceptual framework of the Modern Synthesis. The aim of the developmental genetics school of evo-devo is often perceived as the identification of the genetic bases underlying morphological differences in evolution (Wilkins 2001). Here I argue that most studies in evo-devo are not designed to address question 1.
Many researchers in developmental genetics have become interested in evolutionary issues after the discovery that many important genes in development are conserved across animals. Often, the same genes, gene interactions and similar patterns of gene expression are involved in the development of similar morphological structures in different species. Many research papers in evo-devo consist of standard research in developmental genetics with some comparative discussions at the end. By comparing developmental genetics between different species, essential data about variation in development are acquired. These studies identify differences in the patterns of expression of homologous genes (Patel 1994, Abzhanov and Kaufman 1999), differences in the target genes of homologous transcriptional or signalling pathways (Akam 1998), or even differences in the cis-regulatory elements of homologous genes (Carroll 2000), that correlate with morphological differences between species. These studies show correlations between genetic differences and morphological differences between species but do not show which were the original genetic changes that gave rise to these differences. This is not even the case when experimental mutations in one species produce morphologies reminiscent of the other species (Solé et al. 1999, Nijhout 2002). Even between closely related species the genetic structure of development may have changed since the time the morphological differences under study appeared. Then the genetic differences currently found may differ from the ones originally involved in the formation of a morphological structure. It has even been suggested that in many cases (Salazar-Ciudad et al. 2001a,b, Newman and Müller 2000) the developmental mechanisms underlying a specific morphology can change during evolution.
Although identifying these genetic differences may be a first necessary step, it does not in itself explain which patterns of morphological variation are produced by development or how development evolves. A gene difference, a difference of gene expression or a difference in a target gene does not explain a morphological difference unless the network of genetic, cellular and epigenetic interactions in which it is acting is causally understood. In other words, single genes or even small groups of gene interactions do not constitute mechanisms to explain morphological variation.
In fact, the problem of morphological variation can be seen, by using adequate definitions, to be the same as the problem of pattern formation: that is, how relatively simple spatial distributions of cell types and extracellular components (hereafter called a pattern or previous pattern) are transformed, during development time, into different (normally more complex) spatial distributions of cell types and extracellular components (hereafter called a final pattern). From these definitions development can be seen as a sequence of these transformations between patterns; morphology and its variation as these patterns and their variation. Causal explanations of development require a description of (1) the network of gene interactions involved in a specific pattern transformation, (2) how these affect basic cell behaviours (e.g. proliferation, apoptosis, adhesion, signal secretion and reception, etc.), (3) how these networks and cell behaviours interact with the epigenetic information existing in the previous pattern and in other parts of the embryo (i.e. the spatial distributions of extracellular signals and components, and the spatial distribution and mechanical properties of cells) and (4) how the patterns produced will change when (1), (2) or (3) change. These networks of interactions are herein called developmental mechanisms (Salazar-Ciudad et al. 2003) while the pattern variations they can produce are called the variational properties of a developmental mechanism. Without an understanding of how pattern formation takes place in a morphological structure, the identification of a genetic difference underlying a morphological difference between species cannot be meaningfully interpreted. However, hypotheses about pattern formation that are based on partially known gene networks and previous patterns can be used to give tentative explanations about the morphological differences between species. These hypotheses can be refuted or refined by comparing their predictions with morphological variation between mutants and between species. This approach, here called 'variational', has been used in some previous studies (Goodwin 1994, Holloway and Harrison 1999, Salazar-Ciudad and Jernvall 2002, Harris et al. 2005, Jaeger et al. 2004, Newman and Müller 2005) and has the advantage of explaining which morphological variation is possible by development, rather than only which are the genetic changes underlying particular morphological variants.
Even if pattern formation is one of the more apparent and important phenomena in development, explicit hypotheses about the mechanisms for specific pattern transformations are rare. Even more rarely is it demonstrated how proposed hypotheses can explain the production of a pattern and its variation from previous patterns and networks of genetic and cellular interactions. For complex pattern transformations, verbal arguments are unlikely to be able to describe precisely how the patterns will change according to a given hypothesis when mutations or previous pattern changes occur. In fact, the most explicitly formulated hypotheses that exist include mathematical models that give precise morphological quantitative descriptions about the patterns produced (Holloway and Harrison 1999, Salazar-Ciudad and Jernvall 2002, Harris et al. 2005, Newman and Müller 2005). Research with explicit pattern formation hypotheses based on networks of gene, cell and epigenetic context interactions are relatively rare. Most of the research is more focused on identifying genes, and gene or tissue interactions (and their timing), that are required for the development of some morphological structure. Even when the focus is on pattern formation, it is rarely stated from which previous pattern a pattern appears. Moreover, the reasons for the formation of a pattern are sometimes indicated as being due to the existence of a previous pattern. Although most pattern transformations occur from spatially heterogeneous patterns, the question of pattern formation cannot be passed back to previous patterns in some kind of preformationist chain (Horder 1993). In each developmental stage some spatial information (in the form of spatial distributions of cells) is produced from the previous one. How that happens is the question of pattern formation. Inevitably the explanation of the transformation between a previous pattern and a later pattern requires a precise description of both patterns. Accurate descriptions of both final morphology and intermediate embryonic morphologies are, however, relatively rare (see for exceptions Jernvall et al. 2000, Streicher and Müller 2001, Kuszak et al. 2004). The same occurs for patterns of gene expression, even though it is well known that they change in complex ways in space and time. Somehow, in the same way that some researchers (Dobzhansky 1937) tried to reduce evolution to changes in gene frequencies, some developmental biologists see development as reducible to gene interactions, or even cis-regulatory regions (Carroll 2000), both at the causal level and at the level of explanation.
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