Naturwissenschaften (2004) 91:255–276 DOI 10.1007/s00114-004-0515-y REVIEW Ulrich Kutschera · Karl J. Niklas The modern theory of biological evolution: an expanded synthesis Published online: 17 March 2004 Springer-Verlag 2004 Abstract In 1858, two naturalists, Charles Darwin and of the synthetic theory have survived, but in modified Alfred Russel Wallace, independently proposed natural form. These sub-theories require continued elaboration, selection as the basic mechanism responsible for the particularly in light of molecular biology, to answer open- origin of new phenotypic variants and, ultimately, new ended questions concerning the mechanisms of evolution species. A large body of evidence for this hypothesis was in all five kingdoms of life. published in Darwin’s Origin of Species one year later, the appearance of which provoked other leading scientists like August Weismann to adopt and amplify Darwin’s Introduction perspective. Weismann’s neo-Darwinian theory of evolu- tion was further elaborated, most notably in a series of Physicists and chemists investigate the properties and books by Theodosius Dobzhansky, Ernst Mayr, Julian interactions of objects, such as electrons, photons, and Huxley and others. In this article we first summarize the atoms, which are physically uniform and invariant in their history of life on Earth and provide recent evidence characteristic traits and behavior. Accordingly, a single demonstrating that Darwin’s dilemma (the apparent experiment adducing the properties of a single entity (e.g., missing Precambrian record of life) has been resolved. electron or proton) can be used to extrapolate the Next, the historical development and structure of the properties of all comparable entities in the universe. In “modern synthesis” is described within the context of the biology, the “science of the living world,” both past and following topics: paleobiology and rates of evolution, present (Mayr 1997), the situation is very different. The mass extinctions and species selection, macroevolution organisms biologists study, which are typically randomly and punctuated equilibrium, sexual reproduction and drawn from populations, manifest astonishing variation as recombination, sexual selection and altruism, endosym- a consequence of genetic recombination and random biosis and eukaryotic cell evolution, evolutionary devel- genomic changes. Thus, with the exception of identical opmental biology, phenotypic plasticity, epigenetic in- twins or cloned individuals, no two members of the same heritance and molecular evolution, experimental bacterial species look exactly alike (even identical twins may differ evolution, and computer simulations (in silico evolution physically as a result of their individual histories). of digital organisms). In addition, we discuss the expan- Because this general rule of “biological variability” ap- sion of the modern synthesis, embracing all branches of plies not only to plants and animals, but also to microor- scientific disciplines. It is concluded that the basic tenets ganisms that lack the capacity for sexual reproduction, the concept of “types” is radically different in the context of biology versus that of the physical sciences. Dedicated to Prof. Dr. Dr. hc mult. Ernst Mayr on the occasion of However, there are limits to biological variation and his 100th birthday these literally shape evolutionary history. No population U. Kutschera ()) is ever capable of generating all possible theoretical Institut fr Biologie, genomic variants, in part because sexual genetic recom- Universitt Kassel, bination is random and because the existence of any Heinrich-Plett-Strasse 40, 34109 Kassel, Germany particular population is finite. Therefore, biological vari- e-mail: [email protected] Fax: +49-561-8044009 ation, which provides the “raw material” for evolutionary change, is confined by random events. Nevertheless, non- K. J. Niklas random processes also shape evolution. The “struggle for Department of Plant Biology, existence” among the offspring of each generation elim- Cornell University, inates genomic variants that are less adapted to their Ithaca, NY 14853, USA 256 Table 1 List of the principal 1. Supernatural acts of the Creator are incompatible with empirical facts of nature propositions of Darwin’s theo- 2. All life evolved from one or few simple kinds of organisms ry, extracted from the Origin of 3. Species evolve from pre-existing varieties by means of natural selection Species (Darwin 1859, 1872) 4. The birth of a species is gradual and of long duration 5. Higher taxa (genera, families etc.) evolve by the same mechanisms as those responsible for the origin of species 6. The greater the similarities among taxa, the more closely they are related evolutionarily and the shorter their divergence time from a last common ancestor 7. Extinction is primarily the result of interspecific competition 8. The geological record is incomplete: the absence of transitional forms between species and higher taxa is due to gaps in our current knowledge environment. Those that survive pass their genetic infor- their environments can support; (2) intraspecific variabil- mation on to the next generation. In this way, evolution is ity of most characters exists in abundance; (3) competi- the summation of random events (e.g., mutation and tion for limited resources leads to a struggle for life sexual recombination) and natural selection, which is (Darwin) or existence (Wallace); (4) descent with heri- largely non-random. table modification occurs; and (5), as a result, new species This fundamental process – the “principle of natural evolve into being. selection” (Bell 1997) – was conceived independently by Unlike Wallace, Darwin supported his arguments with two nineteenth-century British naturalists, Charles Dar- a large body of facts, drawn mostly from breeding win and Alfred Russel Wallace, and has been substan- experiments and the fossil record (Table 1). He also tially elaborated upon in the early part of the twentieth provided detailed direct observations of organisms exist- century with the rediscovery of Mendelian genetics and ing in their natural habitats (Darwin 1859, 1872). Thirty subsequent advances in population genetics. Importantly, years later, natural selection’s co-discover published a this “modern synthesis” continues to the present day, as series of lectures under the title Darwinism (Wallace insights are gained from diverse fields of study, partic- 1889), which treated the same subjects as Darwin but in ularly molecular biology, which is rapidly detailing the light of facts and data that were unknown to Darwin (who precise mechanisms whereby genomes (and the pheno- died in 1882). A detailed comparative analysis of the types they engender) are altered. Darwin/Wallace publications reveals that Wallace’s con- The aim of this article is to review the historical tributions were more significant than is usually acknowl- development and the progress made in evolutionary edged, so much so that the phrase “the Darwin/Wallace theory from the time of Darwin and Wallace to the mechanism of natural selection” has been proposed to present day. Clearly, no such summary can ever be acknowledge the importance of the “second Darwin” complete, because the literature dealing with evolutionary (Dawkins 2002; Kutschera 2003a). Although Darwin is biology is vast and complex. Here, we only sketch the usually credited as the “principal author” of evolutionary broad outlines of the basic history of evolutionary theory theory, Ernst Mayr (1988, 1991) points out that it is not and enquiry. To do this, we first describe the development correct to refer to “Darwin’s theory of descent with of the idea of evolution and its subsequent establishment modification” (the word “evolution” does not appear in as a documented fact. We then outline the development the original 1858 papers of Darwin and Wallace; only in and expansion of the modern synthetic theory from 1950 later editions of The Origin of Species and in Wallace’s to the present. Although many major questions in evolu- Darwinism). tionary biology remain unanswered, no credible scientist If we equate the word Darwinism with the content of denies evolution as “a fact.” Yet, many scientists continue the book On the Origin of Species, we can distinguish to explore and debate precisely how the mechanisms of between five separate concepts: evolution work. 1. Evolution as such 2. Theory of common descent Charles Darwin and Alfred Russel Wallace 3. Gradualism 4. Multiplication of species In August 1858, two of the most influential publications 5. Natural selection (Mayr 1988, 1991). in the history of biology were published. These concur- rent papers by Darwin and Wallace contained a “very The first two propositions are discussed in the next ingenious theory to account for the appearance and section. Thereafter, the development of Darwin’s original perpetuation of varieties and of specific forms on our theory is described (see Fig. 1). planet” (foreword by C. Lyell and J. Hooker). Therein, Darwin and Wallace (1858) presented for the first time the hypothesis of descent with modification by means of natural selection. This hypothesis makes five fundamental assertions: (1) all organisms produce more offspring than 257 fossil record, was used as a major argument against his proposal 1 (evolution as a fact). This dilemma no longer exists. Scientists have ex- plored the Precambrian in detail (see Schopf 1999; Knoll 2003 for summaries). We now know that life is far more