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Introduction: Taking a Fresh Look at the Basics of Evolution in the New Century

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James A. Shapiro introduces his book, which is dedicated to considering the many ways that living organisms actively change themselves.
This chapter is from the book

How does novelty arise in evolution? Innovation, not selection, is the critical issue in evolutionary change. Without variation and novelty, selection has nothing to act upon. So this book is dedicated to considering the many ways that living organisms actively change themselves. Uncovering the molecular mechanisms by which living organisms modify their genomes is a major accomplishment of late 20th Century molecular biology.

Conventional evolutionary theory made the simplifying assumption that inherited novelty was the result of chance or accident. Darwin theorized that adaptive change resulted from natural selection applied to countless random small changes over long periods of time. In Chapter 6 of Origin of Species, he wrote: "If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down. But I can find out no such case" [1]. His neo-Darwinist followers took the same kind of black-box approach in the pre-DNA era by declaring all genetic change to be accidental and random with respect to biological function or need. With the discovery of DNA as a hereditary storage medium in the 1940s and early 1950s, the accidental view of change received a molecular interpretation as arising from inevitable errors in the replication process. As many professional and popular press articles attest, the accidental, stochastic nature of mutations is still the prevailing and widely accepted wisdom on the subject [2, 3].

In the context of earlier ideological debates about evolution, this insistence on randomness and accident is not surprising. It springs from a determination in the 19th and 20th Centuries by biologists to reject the role of a supernatural agent in religious accounts of how diverse living organisms originated. While that determination fits with the naturalistic boundaries of science, the continued insistence on the random nature of genetic change by evolutionists should be surprising for one simple reason: empirical studies of the mutational process have inevitably discovered patterns, environmental influences, and specific biological activities at the roots of novel genetic structures and altered DNA sequences. The perceived need to reject supernatural intervention unfortunately led the pioneers of evolutionary theory to erect an a priori philosophical distinction between the "blind" processes of hereditary variation and all other adaptive functions. But the capacity to change is itself adaptive. Over time, conditions inevitably change, and the organisms that can best acquire novel inherited functions have the greatest potential to survive. The capacity of living organisms to alter their own heredity is undeniable. Our current ideas about evolution have to incorporate this basic fact of life.

The recognition of organically generated heritable change has its origins in classical cytogenetics, especially in the revolutionary studies of Barbara McClintock on chromosome repair and restructuring during the 1930s through the 1960s [4]. Cytogenetics is the combination of microscopic examination of chromosomes in cells with Mendelian genetic analysis. Before we knew about DNA, it was the one direct way to observe the behavior of the hereditary apparatus. The advent of molecular genetic studies, starting with bacteria in the 1950s and then expanding to all life forms with recombinant DNA technology in the 1970s, extended McClintock's insights into a universal property of microbes, plants, and animals [5] [6, 7]. Molecular analysis provided mechanistic insight into the myriad distinct ways that living cells can engineer their DNA [8]. Genome sequencing at the end of the 20th Century and the start of this one confirmed major roles played by "natural genetic engineering" in the course of evolutionary change. As we will discuss in detail in Part II, natural genetic engineering represents the ability of living cells to manipulate and restructure the DNA molecules that make up their genomes.

The contemporary concept of life forms as self-modifying beings coincides with the shift in biology from a mechanistic to informatic view of living organisms. One of the great scientific ironies of the last century is the fact that molecular biology, which its pioneers expected to provide a firm chemical and physical basis for understanding life, instead uncovered powerful sensory and communication networks essential to all vital processes, such as metabolism, growth, the cell cycle, cellular differentiation, and multicellular morphogenesis. Whenever these processes have been subjected to the most advanced types of biological analysis, the number of regulatory interactions and control molecules inevitably has grown to rival (and frequently outnumber) the molecules dedicated to executing the basic biochemical and biomechanical events [30]. Paralleling the contemporaneous transformation from a largely mechanical-industrial society to a densely interconnected information-driven society, the life sciences have converged with other disciplines to focus on questions of acquiring, processing, and transmitting information to ensure the correct operation of complex vital systems.

The conceptual universe of biology inevitably underwent a radical transformation from the days of classic thinking about evolution and heredity in the 19th and 20th Centuries. That is the way of science [31]. Instead of cell and organismal properties hardwired by an all-determining genome, we now understand how cells regulate the expression, reproduction, transmission, and restructuring of their DNA molecules. The key evolutionary questions no longer center on whether we can establish relationships between different organisms. Through genome sequences, we can do that across the largest taxonomic distances, finding molecular features that connect the smallest microbes with the largest plants and animals. Today, instead, we endeavor to understand how complex new vital capacities arose in the course of evolution and contributed to the ability of myriad organisms to survive, proliferate, diversify, and reorganize their environment in the course of at least 3.5 billion tumultuous years of Earth history. How did evolutionary inventions help shape the biosphere and influence the nature of the organisms that inhabit it today?

We have learned enough about the diversity of existing life forms and the course of geobiological evolution to recognize that we currently see only the tip of the iceberg. At least 99% of all life forms are still without scientific description, and knowledge of the most diverse forms of life, microorganisms, is expanding daily as we discover unknown kinds in every new ecological niche we explore (including those within and upon our own bodies). But even our incomplete knowledge of the evolutionary iceberg's tip contains clues to exciting processes that were long thought (and long taught) to be impossible. The goal of this book is to acquaint you with previously "inconceivable" but currently well-documented aspects of cell biology and genomics so that you will be ready for the inevitable surprises in evolutionary science as this new century runs its course.

We will focus on how the cell rewrites its genome because that is what we know best about the sources of organic novelty. We can observe genome reorganization in real time and relate what cells do now to what the DNA record tells us has happened over the course of evolution. At both the cellular and genomic levels, the evolutionary process has clearly been one of combinatorial innovation to produce functional systems, followed by the amplification of these systems and their adaptation to novel uses.

Genomic innovations occur at many different levels of complexity. These levels cover the entire range of DNA modifications: from single nucleotide substitutions, to short strings of nucleotides comprising regulatory signals, to longer polynucleotide strings encoding functional regions ("domains") of protein molecules, through larger DNA segments encoding entire RNA or protein molecules, and finally extending to complexes of multiple coding segments and their attendant control regions. In a surprisingly large number of cases, genome analysis tells us that reorganization events have comprised whole genomes.

Because genome evolution is multilevel, amplifying, and combinatorial in nature, the end results are complex hierarchical structures with characteristic system architectures [32, 33]. Genomes are sophisticated data storage organelles integrated into the cellular and multicellular life cycles of each distinct organism. Thinking about genomes from an informatic perspective, it is apparent that systems engineering is a better metaphor for the evolutionary process than the conventional view of evolution as a selection-biased random walk through the limitless space of possible DNA configurations.

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