The ID Report

Robert Deyes
ARN Correspondent

Writing in The Origin Of Species, Charles Darwin expressed his believe that many anatomical structures seen in nature were simply modifications of progenitor structures that had existed in common ancestors some time in the past. He referred to such structures as homologous and considered them to be powerful indicators of common ancestry. Indeed he saw homology as representing the "very soul" of natural history (Ref 1). He was especially intrigued by the "extraordinary type" of the mammalian forelimbs that, in several species, had the same overall structure even though they served quite dissimilar needs:

"What can be more curious than that the hand of man, formed for grasping, that of a mole for digging, the leg of the horse, the paddle of the porpoise, and the wing of the bat, should all be constructed on the same pattern, and should include similar bones, in the same relative positions? How curious it is, to give a subordinate though striking instance, that the hind-feet of the kangaroo, which are so well fitted for bounding over the open plains- those of the climbing, leaf koala, equally fitted for grasping the branches of trees, those of the ground dwelling, insect or root-eating bandicoots and those of some other Australian marsupials should all be constructed on the same extraordinary type, namely with the bones of the second and third digits extremely slender and enveloped within the same skin....is this not powerfully suggestive of true relationship, of inheritance from a common ancestor" (Ref 1, pp.579-580)

Modern genetics has made major strides in recent years and contributed hugely in our search for relationships between genes and their phenotypes. The most astonishing revelation has been that not only are different genes involved in the formation of apparently homologous structures but supposedly related genes also code for structures that would not be categorized as homologous under the Darwinian definition. One article that appeared in Nature described a stunning example of how genes- once thought to be predictable 'operators' of structural homology- are proving to be just the opposite. Molecular biologists Ying Litingtung and Randall Dahn described the involvement of two genes- sonic hedgehog (shh) and Gli3- in the development of the digit pattern of the vertebrate pentadactyl limb (Ref 2). It turns out that Shh is part of a much larger group of highly conserved genes called the hedgehog family that not only exist in vertebrates but also in a number of invertebrate species including leeches, sea urchins, amphioxus and fruit flies (Ref 2). As biologists Philip Ingham and Andrew McMahon wrote, the extreme conservation of the hedgehog family across such a diverse set of species is, from a homology standpoint, a highly unexpected find:

"parallel studies in invertebrate and vertebrate systems have shown that although the final outcome might look quite different (eg: a fly vs a mouse), there is a striking conservation in the deployment of members of the same signaling families to regulate development of these seemingly quite different organisms" (Ref 3)

In evolutionary terms, Shh and Gli are described as orthologous genes on the basis that they have, "evolved by vertical descent from a common ancestor and are presumed to have the same function" (Ref 4). It is therefore paradoxical to find that these genes should be responsible for such a wide variety of different phenotypic outcomes. Of course this is not the only example of such an incongruency. Another set of genes called the Hox family also play a role in development in several distinct animal phyla (Ref 5). University of Wisconsin biologist Sean Carroll has written on this rather troubling state of affairs:

"The first and perhaps most important lesson from [the study of evolutionary development] is that looks can be quite deceiving. Virtually no biologist expected to find what turned out to be the case: most of the genes first identified as body-building and organ-forming genes in the fruit fly have exact counterparts, performing similar jobs, in most mammals, including humans. The very first shots fired in the [evolutionary development] revolution revealed that despite their great differences in appearance, almost all animals share a common "tool kit" of body-building genes. That discovery - actually a series of discoveries - vaporized many previous ideas about how animals differ from one another...The architects of the modern synthesis expected the genomes of vastly different species to differ vastly. They had no idea that such different forms could be built with similar sets of genes" (Ref 6).

And of course the list goes on. A group headed by Walter Gehring from the University of Basel in Switzerland wrote of the involvement of a gene called Pax-6 in eye development in a number of distinct animal taxa including mammals, amphibians, fish and insects (Ref 7). Possibly the most important finding about Pax-6 is that not only are the mouse and human forms of the Pax-6 protein identical in their amino acid sequence but they also share between 90 and 94% sequence similarity with the fruit fly sequence (Ref 7) The challenge that such a finding poses to the traditional Darwinian view of homology is clear. As Gehring and his colleagues wrote

"This was [an unexpected result] because of the long-standing dogma.. that the insect compound eye was non-homologous to the vertebrate camera eye, and that the two types of eye had evolved independently" (Ref 7)

As paleontologist Simon Conway Morris has pointed out, such findings are puzzling when one considers how different the vertebrate and insect eyes really are (Ref 8, p.8). More generally, Darwin was well aware of the enormous difficulties that an organ as apparently near-perfect as the eye presented to his theory of natural selection. He wrote:

"To suppose that the eye with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest degree."(Ref 1, p.227)

However, he was certain that if a gradual sequence of light perceiving organs could be drawn up spanning the unimaginable distance between the simplest 'imperfect eye' and its more complex derivative, the threat to his theory would not be so great (Ref 1, p.228). Such a sequence is precisely what Darwin failed to find and what Gehring and his colleagues subsequently used in defense of a common origin to the diversity of eye-like organs in nature (Ref 7). Gehring and Ikeo postulated that the evolution of the eye was "intimately connected to the evolution of the visual pigment rhodopsin". Thus the seemingly ubiquitous presence of both the rhodopsin and the Pax-6 proteins could only be considered as evidence that all eyes in higher organisms had evolved from a single prototype and were therefore, according to Gehring and Ikeo, evolutionarily related (Ref 7). This was a massive shift in thinking given the commonly held view of non-homology between eye-like organs of organisms as disparate as insects and vertebrates.

In their own depiction of a, "hypothetical scheme of evolution of various eye-types from a common ancestral prototype" Gehring and Ikeo were unable to fill in the tremendous jumps that would have to have been made to obtain the diversity of eye-like organs from their hypothetical prototype. Such omissions are of utmost importance if we are to have a serious discussion on the step-by step evolution of the eye. It can always be argued, and Sean Carroll does, that the fact that there are common genes involved in the development of most organisms is evidence itself for evolutionary relatedness and that structural differences arise because significant differences in the patterns of expression of these genes have evolved through time.

Nevertheless, when we begin to investigate gene expression patterns in different organisms we find that they are very tightly regulated with little scope for change. In fact ever-so-slight changes in these expression patterns can have extremely deleterious consequences for the organisms involved. Indeed fruit fly biologist Peter Lawrence has shed light on how the patterning of body plans during embryonic development is dependent on what he calls 'positional information'- the program through which cells recognize their position relative to other cells and develop into specialized tissues accordingly (Ref 9, pp. 146-148). As Lawrence so eloquently describes, individual cells recognize their relative positions or coordinates through the activities of proteins called morphogens that form highly specified concentration gradients across the embryo (Ref 9, p. 27; pp. 57-59). In all there are four systems of concentration gradients that define amongst other things the overall patterning of the developing embryo (Ref 9, p.50). These gradients determine the fate of cells by generating molecular 'triggers' that will lead to further specialization into tissues and organs (Ref 9, p.51). Strikingly, these gradients also exhibit a high degree of specification with particular genes being turned on at determined concentrations within the gradients. Too high or too low a concentration and the genes so necessary for the correct specialization of cells into tissues in a given region of the embryo will not be turned on. Indeed dramatic experiments on flies lacking one morphogen called 'bicoid' have shown just how disastrous variations in its concentration can be on subsequent development (Ref 9, pp. 28-30).

How does one explain the origin of structural differences between organisms from some limited number of ancestral forms if the gene expression patterns that define structural differences are so tightly regulated? As we can glean from Lawrence's review, there is very little room for these expression patterns to evolve through slight successive changes because of the critical roles that they play in defining overall body plans in different organisms (Ref 9). As we have seen, orthologous genes which seemingly bear the hallmarks of common ancestral relationships, generate outward phenotypes that show everything besides the conserved structural forms that a Darwinian and neo-Darwinian assessment of homology would predict. In conclusion, Darwin's 'Soul of Natural History' is today being put to the test by the very unit of hereditary that should have solidified the case for natural selection. This unit is none other than the gene itself.

References
1. Charles Darwin (1859), The Origin of Species By Means of Natural Selection Or The Preservation of Favored Races In the Struggle For Survival Modern Library Paperbacks Edition (1998), New York

2. Ying Litingtung, Randall Dahn, Yina Li, John F. Fallon and Chin Chiang (2002) Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity, Nature Volume 418 pp 979-983

3. Philip W. Ingham and Andrew P. McMahon (2001), Hedgehog signaling in animal development: paradigms and principles, Genes and Development Volume 15 pp3059-3087

4. Arcady R. Mushergian, James Garey, Jason Martin, Leo X. Liu (1998), Large-Scale Taxonomic Profiling of Eukaryotic Model Organisms: A Comparison of Orthologous Proteins Encoded by the Human Fly, Nematode And Yeast Genomes, Genome Research Volume 8 pp590-598

5. Patrick Callaerts, Patricia N. Lee, Britta Hartmann, Claudia Farfan, Darrett W.Y. Choy, Kazuho Ikeo, Karl-Friederich Fischbach, Walter J. Gehring and H Gert de Couet (2001), HOX genes in the sepiolid squid Euprymna scolopes: Implications for the evolution of complex body plans
PNAS Vol 99 pp 2088-2093

6. Sean Carroll (2005), The Origins of Form, Natural History Magazine, November 2005. Article can be found at http://www.naturalhistorymag.com/

7. Walter J. Gehring and Kazuho Ikeo (1999), Pax 6: mastering eye morphogenesis and eye evolution, Trends in Genetics, Volume 15 pp.371-377

8. Simon Conway Morris (1998), The Crucible of Creation; The Burgess Shale And the Rise of Animals, 1st Ed, Oxford University Press

9. Peter Lawrence (1992), The Making Of A Fly- The Genetics Of Animal Design, Blackwell Scientific Publications, Oxford, UK