The Evolution Of Regulatory Dna And Morphological Diversity

In this chapter, we have examined the evolution of regulatory DNA from three perspectives —theoretical considerations of cis-regulatory element function, comparative analyses of known czs-regulatory elements, and a handful of genetic investigations into the nature of morphological variation. All of these approaches support the claim that regulatory DNA is the source of genetic diversity that underlies morphological diversity. The greater role of regulatory DNA in morphological evolution (as compared to coding DNA) is enabled by three critical factors:

• The degree of freedom in cz's-regulatory sequences

• The modularity of cz's-regulatory elements

• The combinatorial action of the transcription factor repertoire in cells

The degree of freedom in regulatory DNA is important because it imparts a greater tolerance of regulatory DNA to all types of mutational change. Regulatory DNA does not need to maintain any reading frame, and it can function at widely varying distances from or orientation to the transcription units it controls.

The modularity of the elements that make up the cz's-regulatory systems of genes facilitates evolution because individual elements can evolve independently. The ability of regulatory DNA to readily evolve creates a rich source of genetic variation and, therefore, potential morphological variation.

The importance of the combinatorial nature of transcription regulation cannot be overemphasized. The transcription factor repertoire is sufficiently diverse and the stringency of DNA binding sufficiently relaxed such that sites for most transcription factors can evolve at a significant frequency in animal genomes. As new combinations of sites arise in existing functional elements, and potentially within nonfunctional DNA as well, variations in the timing, level, and spatial domains of gene expression may evolve and generate phenotypic variations, which serve as the raw material for selection and morphological change. The very structure of the cz's-regulatory regions of toolkit genes—that is, its composition from multiple, independently regulated cz's-elements—is the product of these evolutionary processes. It constitutes persuasive evidence that the diversification of regulatory DNA, while generally maintaining coding function, is the most available and most frequently exploited mode of genetic diversification in animal evolution.

Extrapolating from bristles to body plans

This book has explored and sought to explain the genetic basis of the morphological diversity of animals. Three kinds of assumptions are implicit to our approach and the conclusions we have drawn.

First, we assume that we can extrapolate from the present to the past. Ayshaiea (see Fig. 1.1a) and Acanthostega (see Fig. 1.5e) are no longer walking the Earth, but we assume that we can extrapolate from genetic and developmental knowledge of their modern descendants and thereby infer processes that occurred in the Cambrian or the Devonian periods.

Second, we assume that we can extrapolate from the particular to the general. Very few genetic regulatory circuits or networks are known in great detail, a modest number of czs-regulatory elements have been thoroughly dissected at the DNA sequence and transcription factor level and compared between relevant taxa. Nevertheless, we assert that the specific knowledge we do have is likely to apply to the general case.

Our third, and perhaps most controversial, assumption is that we may extrapolate from the observable small genetic changes underlying fine-scale morphological variation to the largest changes that have happened in animal history. Jacques Monod once asserted that what was true of the bacterium Escherichia coli was true of elephants. Analogously, we suggest that what is true of bristles is true of body plans. If dozens of regulatory changes and gene interactions underlie the difference of just a few bristles between fruit fly populations, then the number of genetic regulatory differences underlying the full range of morphological differences between a fly and a butterfly, or between a mouse and a human, must be staggeringly immense. But, do we need to invoke any additional or special genetic or evolutionary mechanisms beyond those illustrated for bristle variation to explain morphological diversity at higher levels?

Is there any role, for example, for the sorts of dramatic variants described by Bateson in the evolution of large differences between taxa? The emerging evidence suggests not. Although, in theory, any morphological or genetic variation may potentially be selected for, Bateson's monsters (for example, homeotic mutants) are generally less fit than other individuals and would be selected against in interbreeding populations. Furthermore, the case studies and mechanisms described in this book suggest that not only are such large steps improbable, but unnecessary. We have described many examples of morphological evolution that involved homeotic genes, but not homeotic mutations. Dramatic morphological changes, such as the fin-to-limb transition in vertebrates or the evolution of the insect haltere, involved many regulatory, developmental, and anatomical modifications that could not and did not evolve instantaneously. Instead, these structures were sculpted by regulatory evolution over millions of years.

Does variation exist in animal forms that might provide the basis for large-scale morphological evolution? Indeed, variants are found with significant frequency within and between natural populations for characters that are more significant to the evolution of body plans and body parts than just bristle number. For example, detailed analysis of a single population of newts has revealed a surprising array of variation in limb skeleton morphologies in approximately 30% of individuals examined (Fig. 8.6). Most interestingly, these variant patterns often resembled the standard limb skeletal morphologies found in other species. Some of these patterns were similar to more "ancient" patterns; others reflected more derived conditions. These observations suggest that within this single population of animals, many potential limb morphologies are expressed that represent both potential novelties and atavisms (return to an ancestral state). As the evolution of limb skeletal morphology is important to the functional adaptation of these and other tetrapods, the variation documented in this population suggests that the evolution of new forms or the reversion to "old" forms can arise through readily available genetic variation in the genes that affect limb morphology. Little, if any, morphological variation in this population is likely to be due to intraspecific variation in protein function.

Other well-documented examples of striking intraspecific morphological variation have been described in centipedes and certain fishes. Among geophilomorph centipede species, the number of leg-bearing segments varies from 29 to 191; in other centipede orders, this number remains relatively constant. Within geophilomorph species, there may be a range of variance of 12-14 segments. Given the considerable range in segment number observed in fossil and extant arthropods, the mechanisms underlying variation in such a central feature of the arthropod body plan are of immense interest.

Figure 8.6

Intraspecific variation in limb morphology in salamanders

Figure 8.6

Intraspecific variation in limb morphology in salamanders

A single population of salamanders displays considerable variations in limb morphology. (a, top and bottom) The standard bone patterns of the forelimb and hindlimb, respectively, of Taricha granulosa. ( b) Variations of the standard patterns. (top) A forelimb bone pattern in which fewer distinct carpal elements form. (bottom) Four variants in hindlimb patterns in which the number and pattern of carpal structures differ.

Source: Shubin N, Wake DB, Crawford AJ. Morphological variation in the limbs of Taricha granulosa (Caudata: Salamandridae): evolutionary and phylogenetic implications. Evolution 1995; 49: 874-884.

Remarkable body pattern variation is also observed between populations of the three-spine stickleback fish. This group of species has experienced repeated postglacial episodes of colonization of freshwater lakes and streams. Skull, body, and appendage shapes differ extensively between populations (Fig. 8.7) that have become isolated relatively recently (for example, circa 13,000 years ago). It appears that, in the stickleback, colonization and ecological diversification have led to a radiation of morphologically diverse, but closely related species.

These surveys of natural populations offer striking support for the idea that the morphological variation required for the evolution of new body patterns is available, at least in some groups. When this information is coupled with new insights into the scope of genetic variation that can lurk beneath the surface of phenotypic stability, it appears that the developmental,

Figure 8.7

Variation in stickleback fish body patterns

General body form, fin morphology, dorsal spine number, coloration, and several other morphological features differ considerably between populations of the three-spine stickleback Gasterosteus aculeatus species complex. Lake and river populations from various North American populations are depicted around the periphery of a representative marine form. The striking variation of recently isolated species in this complex illustrates the potential for rapid morphological diversification of major body characters. Source: Bell MA, Foster SA. In: Bell MA, Foster SA, eds. The evolutionary biology of the threespine stickleback. Oxford, UK: Oxford University Press, 1994: 1-27.

Figure 8.7

Variation in stickleback fish body patterns

General body form, fin morphology, dorsal spine number, coloration, and several other morphological features differ considerably between populations of the three-spine stickleback Gasterosteus aculeatus species complex. Lake and river populations from various North American populations are depicted around the periphery of a representative marine form. The striking variation of recently isolated species in this complex illustrates the potential for rapid morphological diversification of major body characters. Source: Bell MA, Foster SA. In: Bell MA, Foster SA, eds. The evolutionary biology of the threespine stickleback. Oxford, UK: Oxford University Press, 1994: 1-27.

genetic, and potential morphological diversity of any large interbreeding group is much greater than has been realized by biologists, or is realized in the course of evolution. This potential is generated from the creative power of regulatory change and interaction; and it is realized through ecological interactions at many levels.

We arrive at a view—while perhaps made more sophisticated by virtue of modern embryology, genetics, and molecular biology—that does not stray far from the spirit, if not the heart, of Darwin's original ideas. Darwin chose to open The Origin of Species with a discussion of domesticated species, arguing persuasively about the power of selection upon variation, on a scale and landscape familiar to his readers. Then, in closing his great work, he urged his audience to extrapolate from dog and pigeon breeding to the larger landscape of life's history:

"we are always slow in admitting great changes of which we do not see the steps. . . . The mind cannot possibly grasp the full meaning of the term of even a million years; it cannot add up and perceive the full effects of many slight variations, accumulated during an almost infinite number of generations."

Today, we are beginning to identify the genetic steps underlying the evolution of specific traits, and to conceive and reconstruct some of the innumerable steps underlying the great changes in animal designs that have unfolded from our Precambrian ancestors. We have been able to elucidate some of the general mechanisms that have been at work throughout animal history. Armed with increasingly more powerful tools for analyzing variation and comparing genomes and gene expression, the relationship between the evolution of DNA and animal diversity is drawing increasingly within our grasp.

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