Estimates of hybrid fitness have been used as either a platform for testing the potential role of natural hybridization in the evolution of species and species complexes or, alternatively, as a rationale for dismissing hybridization events as being of any evolutionary significance. From the time of Darwin's publication of The Origin, through the neo-Darwinian synthesis, to the present day, the observation of variability in hybrid fitness has remained a challenge for some models of speciation. Yet, Darwin and others have reported the elevated fitness of hybrid genotypes under certain environmental conditions. In modern scientific terminology, this observation reflects the fact that hybrid genotypes can demonstrate genotype × environment interactions. In the current review, we illustrate the development of one plant species complex, namely the Louisiana Irises, into a ‘model system' for investigating hybrid fitness and the role of genetic exchange in adaptive evolution and diversification. In particular, we will argue that a multitude of approaches, involving both experimental and natural environments, and incorporating both manipulative analyses and surveys of natural populations, are necessary to adequately test for the evolutionary significance of introgressive hybridization. An appreciation of the variability of hybrid fitness leads to the conclusion that certain genetic signatures reflect adaptive evolution. Furthermore, tests of the frequency of allopatric versus sympatric/parapatric divergence (that is, divergence with ongoing gene flow) support hybrid genotypes as a mechanism of evolutionary diversification in numerous species complexes.
natural hybridization; habitat selection; hybrid fitness
The scientific contribution of Darwin, still agonized in many religious circles, has now been recognized and celebrated by scientists from various disciplines. However, in recent years, several evolutionists have criticized Darwin as outdated, arguing that “Darwinism,” assimilated to the “tree of life,” cannot explain microbial evolution, or else was not operating in early life evolution. These critics either confuse “Darwinism” and old versions of “neo-Darwinism” or misunderstand the role of gene transfers in evolution. The core of Darwin explanation of evolution (variation/selection) remains necessary and sufficient to decipher the history of life. The enormous diversity of mechanisms underlying variations has been successfully interpreted by evolutionists in this framework and has considerably enriched the corpus of evolutionary biology without the necessity to kill the father. However, it remains for evolutionists to acknowledge interactions between cells and viruses (unknown for Darwin) as a major driving force in life evolution.
evolutionary synthesis; variation; natural selection; lateral gene transfer; Darwinian threshold; viruses
Comparative genomics and systems biology offer unprecedented opportunities for testing central tenets of evolutionary biology formulated by Darwin in the Origin of Species in 1859 and expanded in the Modern Synthesis 100 years later. Evolutionary-genomic studies show that natural selection is only one of the forces that shape genome evolution and is not quantitatively dominant, whereas non-adaptive processes are much more prominent than previously suspected. Major contributions of horizontal gene transfer and diverse selfish genetic elements to genome evolution undermine the Tree of Life concept. An adequate depiction of evolution requires the more complex concept of a network or ‘forest’ of life. There is no consistent tendency of evolution towards increased genomic complexity, and when complexity increases, this appears to be a non-adaptive consequence of evolution under weak purifying selection rather than an adaptation. Several universals of genome evolution were discovered including the invariant distributions of evolutionary rates among orthologous genes from diverse genomes and of paralogous gene family sizes, and the negative correlation between gene expression level and sequence evolution rate. Simple, non-adaptive models of evolution explain some of these universals, suggesting that a new synthesis of evolutionary biology might become feasible in a not so remote future.
The 200th anniversary of Darwin and the 150th jubilee of the Origin of Species prompt a new look at evolutionary biology. The 1959 Origin centennial was marked by the consolidation of the Modern Synthesis. The edifice of the Modern Synthesis has crumbled, apparently, beyond repair. The hallmark of the Darwinian discourse of 2009 is the plurality of evolutionary processes and patterns. Nevertheless, glimpses of a new synthesis might be discernible in emerging universals of evolution.
Small incremental biological change, winnowed by natural selection over geological time scales to produce large consequences, was Darwin's singular insight that revolutionized the life sciences. His publications after 1859, including the ‘earthworm book’, were all written to amplify and support the evolutionary theory presented in the Origin. Darwin was unable to provide a physical basis for the inheritance of favoured traits because of the absence of genetic knowledge that much later led to the ‘modern synthesis’. Mistaken though he was in advocating systemic ‘gemmules’ as agents of inheritance, Darwin was perceptive in seeking to underpin his core vision with concrete factors that both determine the nature of a trait in one generation and convey it to subsequent generations. This brief review evaluates the molecular genetic literature on earthworms published during the last decade, and casts light on the specific aspects of earthworm evolutionary biology that more or less engaged Darwin: (i) biogeography, (ii) species diversity, (iii) local adaptations and (iv) sensitivity. We predict that the current understanding will deepen with the announcement of a draft earthworm genome in Darwin's bicentenary year, 2009. Subsequently, the earthworm may be elevated from the status of a soil sentinel to that elusive entity, an ecologically relevant genetic model organism.
Darwin; earthworms; evolution; genotypes; biogeography; transcriptomics
Analysis of DNA sequences now plays a key role in evolutionary biology research. If Darwin were to come back today, I think he would be absolutely delighted with molecular evolutionary genetics, for three reasons. First, it solved one of the greatest problems for his theory of evolution by natural selection. Second, it gives us a tool that can be used to investigate many of the questions he found the most fascinating. And third, DNA data confirm Darwin's grand view of evolution.
molecular evolution; heredity; macroevolution; pangenesis; gemmule; central dogma
The framework for modern studies of speciation was established as part of the Neo-Darwinian synthesis of the early twentieth century. Here we evaluate this framework in the light of recent empirical and theoretical studies. Evidence from experimental studies of selection, quantitative genetic studies of species’ differences, and the molecular evolution of ‘isolation’ genes, all agree that directional selection is the primary cause of speciation, as initially proposed by Darwin. Likewise, as suggested by Dobzhansky and Mayr, gene flow does hold species together, but probably more by facilitating the spread of beneficial mutants and associated hitchhiking events than by homogenizing neutral loci. Reproductive barriers are important as well in that they preserve adaptations, but as has been stressed by botanists for close to a century, they rarely protect the entire genome from gene flow in recently diverged species. Contrary to early views, it is now clear that speciation can occur in the presence of gene flow. However, recent theory does support the long-held view that population structure and small population size may increase speciation rates, but only under special conditions and not because of the increased efficacy of drift as suggested by earlier authors. Rather, low levels of migration among small populations facilitates the rapid accumulation of beneficial mutations that indirectly cause hybrid incompatibilities.
gene flow; introgression; population size; population subdivision; reproductive isolation; selection; selective sweep; speciation
Biological evolution represents one of the most successful, but also controversial scientific concepts. Ever since Charles Darwin formulated his version of evolution via natural selection, biological sciences experienced explosive development and progress. First of all, although Darwin could not explain how traits of organisms, selected via natural selection, are inherited and passed down along generations; his theory stimulated research in this respect and resulted in the establishment of genetics and still later in the discovery of DNA and genome sequencing some hundred years after his evolutionary theory. Nevertheless, there are several weaknesses in classical Darwinian as well as Neodarwinian gene-centric views of biological evolution. The most serious drawback is its narrow focus: the modern evolutionary synthesis, as formulated in the 20th Century, is based on the concept of gene and on the mathematical/statistical analysis of populations. While Neodarwinism is still generally considered a valid theory of biological evolution, its narrow focus and incompatibility with several new findings and discoveries calls for its update and/or transformation. Either it will be replaced with an updated version or, if not flexible enough, it will be replaced by a new theory. In his book “Evolution — A New View from the 21st Century,”1 James A. Shapiro discusses these problems as well as newly emerging results which are changing our understanding of biological evolution. This new book joins a row of several other recent books highlighting the same issues.2–13
150 years ago, Heinrich Bronn provided in the first German translation of Charles Darwin's Origin of Species a rather liberal interpretation, even adding his own view of Darwin's ideas in an additional 15th chapter. Ernst Haeckel widely popularized his view of Darwinian evolution based on his reading of this translation. This was long seen - probably incorrectly - as the intellectual root of social Darwinism in Germany.
As Dobzhansky wrote, nothing in biology makes sense outside the context of the evolutionary theory, and this truth has not been sufficiently explored yet by medicine. We comment on Shanks and Pyles' recently published paper, Evolution and medicine: the long reach of "Dr. Darwin", and discuss some recent advancements in the application of evolutionary theory to carcinogenesis. However, we disagree with Shanks and Pyles about the usefulness of animal experiments in predicting human hazards. Based on the darwinian observation of inter-species and inter-individual variation in all biological functions, Shanks and Pyles suggest that animal experiments cannot be used to identify hazards to human health. We claim that while the activity of enzymes may vary among individuals and among species, this does not indicate that critical events in disease processes occurring after exposure to hazardous agents differ qualitatively between animal models and humans. In addition, the goal is to avoid human disease whenever possible and with the means that are available at a given point in time. Epidemics of cancer could have been prevented if experimental data had been used to reduce human exposures or ban carcinogenic chemicals. We discuss examples.
In spite of its success, Neo-Darwinism is faced with major conceptual barriers to further progress, deriving directly from its metaphysical foundations. Most importantly, neo-Darwinism fails to recognize a fundamental cause of evolutionary change, “niche construction”. This failure restricts the generality of evolutionary theory, and introduces inaccuracies. It also hinders the integration of evolutionary biology with neighbouring disciplines, including ecosystem ecology, developmental biology, and the human sciences. Ecology is forced to become a divided discipline, developmental biology is stubbornly difficult to reconcile with evolutionary theory, and the majority of biologists and social scientists are still unhappy with evolutionary accounts of human behaviour. The incorporation of niche construction as both a cause and a product of evolution removes these disciplinary boundaries while greatly generalizing the explanatory power of evolutionary theory.
niche construction; evolutionary biology; ecological inheritance; ecosystem ecology; developmental biology
Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwin's insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwin's seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwin's efforts towards integration.
adaptation; Charles Darwin; flowers; pollination; mating
Darwin proposed an explicitly aesthetic theory of sexual selection in which he described mate preferences as a ‘taste for the beautiful’, an ‘aesthetic capacity’, etc. These statements were not merely colourful Victorian mannerisms, but explicit expressions of Darwin's hypothesis that mate preferences can evolve for arbitrarily attractive traits that do not provide any additional benefits to mate choice. In his critique of Darwin, A. R. Wallace proposed an entirely modern mechanism of mate preference evolution through the correlation of display traits with male vigour or viability, but he called this mechanism natural selection. Wallace's honest advertisement proposal was stridently anti-Darwinian and anti-aesthetic. Most modern sexual selection research relies on essentially the same Neo-Wallacean theory renamed as sexual selection. I define the process of aesthetic evolution as the evolution of a communication signal through sensory/cognitive evaluation, which is most elaborated through coevolution of the signal and its evaluation. Sensory evaluation includes the possibility that display traits do not encode information that is being assessed, but are merely preferred. A genuinely Darwinian, aesthetic theory of sexual selection requires the incorporation of the Lande–Kirkpatrick null model into sexual selection research, but also encompasses the possibility of sensory bias, good genes and direct benefits mechanisms.
sexual selection; natural selection; aesthetics; beauty; adaptation
When Charles Darwin formulated the central principles of evolutionary biology in the Origin of Species in 1859 and the architects of the Modern Synthesis integrated these principles with population genetics almost a century later, the principal if not the sole objects of evolutionary biology were multicellular eukaryotes, primarily animals and plants. Before the advent of efficient gene sequencing, all attempts to extend evolutionary studies to bacteria have been futile. Sequencing of the rRNA genes in thousands of microbes allowed the construction of the three- domain “ribosomal Tree of Life” that was widely thought to have resolved the evolutionary relationships between the cellular life forms. However, subsequent massive sequencing of numerous, complete microbial genomes revealed novel evolutionary phenomena, the most fundamental of these being: (1) pervasive horizontal gene transfer (HGT), in large part mediated by viruses and plasmids, that shapes the genomes of archaea and bacteria and call for a radical revision (if not abandonment) of the Tree of Life concept, (2) Lamarckian-type inheritance that appears to be critical for antivirus defense and other forms of adaptation in prokaryotes, and (3) evolution of evolvability, i.e., dedicated mechanisms for evolution such as vehicles for HGT and stress-induced mutagenesis systems. In the non-cellular part of the microbial world, phylogenomics and metagenomics of viruses and related selfish genetic elements revealed enormous genetic and molecular diversity and extremely high abundance of viruses that come across as the dominant biological entities on earth. Furthermore, the perennial arms race between viruses and their hosts is one of the defining factors of evolution. Thus, microbial phylogenomics adds new dimensions to the fundamental picture of evolution even as the principle of descent with modification discovered by Darwin and the laws of population genetics remain at the core of evolutionary biology.
Darwin; modern synthesis; comparative genomics; tree of life; horizontal gene transfer
To Darwin, parasites were fascinating examples of adaptation but their significance as selective factors for a wide range of phenomena has only been studied in depth over the last few decades. This work has had its roots in behavioural/evolutionary ecology on the one hand, and in population biology/ecology on the other, thus shaping a new comprehensive field of ‘evolutionary parasitology’. Taking parasites into account has been a success story and has shed new light on several old questions such as sexual selection, the evolution of sex and recombination, changes in behaviour, adaptive life histories, and so forth. In the process, the topic of ecological immunology has emerged, which analyses immune defences in a framework of costs and benefits. Throughout, a recurrent theme is how to appropriately integrate the underlying mechanisms as evolved boundary conditions into a framework of studying the adaptive value of traits. On the conceptual side, major questions remain and await further study.
parasitism; evolution; virulence; ecological immunology
Species are generally viewed by evolutionists as ‘real’ distinct entities in nature, making speciation appear difficult. Charles Darwin had originally promoted a very different uniformitarian view that biological species were continuous with ‘varieties’ below the level of species and became distinguishable from them only when divergent natural selection led to gaps in the distribution of morphology. This Darwinian view on species came under immediate attack, and the consensus among evolutionary biologists today appears to side more with the ideas of Ernst Mayr and Theodosius Dobzhansky, who argued 70 years ago that Darwin was wrong about species. Here, I show how recent genetic studies of supposedly well-behaved animals, such as insects and vertebrates, including our own species, have supported the existence of the Darwinian continuum between varieties and species. Below the level of species, there are well-defined ecological races, while above the level of species, hybridization still occurs, and may often lead to introgression and, sometimes, hybrid speciation. This continuum is evident, not only across vast geographical regions, but also locally in sympatry. The existence of this continuum provides good evidence for gradual evolution of species from ecological races and biotypes, to hybridizing species and, ultimately, to species that no longer cross. Continuity between varieties and species not only provides an excellent argument against creationism, but also gives insight into the process of speciation. The lack of a hiatus between species and ecological races suggests that speciation may occur, perhaps frequently, in sympatry, and the abundant intermediate stages suggest that it is happening all around us. Speciation is easy!
hybridization; speciation; species concepts
Celebrating 300 years since the birth of Carl Linnaeus (1707–1778), a meeting was held in June 2007 to review recent progress made in understanding the origins and evolutionary radiation of the animals. The year 2008 celebrates the 250th anniversary of the publication of the 10th edition of Linnaeus' Systema Naturae, generally considered to be the starting point of zoological nomenclature. With subsequent advances in comparative taxonomic and systematic studies, Darwin's discovery of evolution by natural selection, the birth of phylogenetic systematics, and the wider interest in biodiversity, it is salutary to consider that many of the major advances in our understanding of animal evolution have been made in recent years. Phylogenetic systematics, drawing from evidence provided by genotype, phenotype and an understanding of the link between them through comparative embryological and evolutionary developmental studies, has provided a wide consensus of the major branching patterns of the tree of life. More importantly, the integrated approaches discussed in the 16 contributions to this volume highlight the identity and nature of problematic taxa, the missing data, errors in existing analytical procedures and the promise of a wealth of additional characters from genomes that need to be accumulated and assessed in providing a definitive Systema Naturae.
Linnaeus; animal evolution; evo–devo; phylogenetics
This year celebrates the 200th aniversary of the birth of Charles Darwin, best known for his theory of evolution summarized in On the Origin of Species. Less well known is that, in the second half of his life, Darwin’s major scientific focus turned towards plants. He wrote several books on plants, the next-to-last of which, The Power of Movement of Plants, published together with his son Francis, opened plants to a new view. Here we amplify the final sentence of this book in which the Darwins proposed that: “It is hardly an exaggeration to say that the tip of the radicle thus endowed [with sensitivity] and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements.” This sentence conveys two important messages: first, that the root apex may be considered to be a ‘brain-like’ organ endowed with a sensitivity which controls its navigation through soil; second, that the root apex represents the anterior end of the plant body. In this article, we discuss both these statements.
auxin; cognition; plant neurobiology; plant tropisms; roots; sensory biology; signaling
Constructive neutral evolution (CNE) suggests that neutral evolution may follow a stepwise path to extravagance. Whether or not CNE is common, the mere possibility raises provocative questions about causation: in classical neo-Darwinian thinking, selection is the sole source of creativity and direction, the only force that can cause trends or build complex features. However, much of contemporary evolutionary genetics departs from the conception of evolution underlying neo-Darwinism, resulting in a widening gap between what formal models allow, and what the prevailing view of the causes of evolution suggests. In particular, a mutationist conception of evolution as a 2-step origin-fixation process has been a source of theoretical innovation for 40 years, appearing not only in the Neutral Theory, but also in recent breakthroughs in modeling adaptation (the “mutational landscape” model), and in practical software for sequence analysis. In this conception, mutation is not a source of raw materials, but an agent that introduces novelty, while selection is not an agent that shapes features, but a stochastic sieve. This view, which now lays claim to important theoretical, experimental, and practical results, demands our attention. CNE provides a way to explore its most significant implications about the role of variation in evolution.
Alex Kondrashov, Eugene Koonin and Johann Peter Gogarten reviewed this article.
Evolutionary theory; Constructive neutral evolution; Neo-Darwinism; Mutation; Evolutionary genetics; Mutation bias; Modern Synthesis
One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin's finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galápagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin's finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin's finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin's finches or whose studies were inspired by research on Darwin's finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.
Darwin's finches; evolution; speciation; adaptive radiation
Evolutionary theory has never had a stronger scientific foundation than it does today. In a short review I hope to portray the deep commitment of today's biologists to Darwinian natural selection and to discoveries made since Darwin's time. In spite of the scientific advances in the century and a half since the publication of On the Origin of Species, Darwin still remains the principal author of modern evolutionary theory. He is one of the greatest contributors of all time to our understanding of nature.
There is increasing evidence that Darwin's theory of evolution by natural selection provides insights into the etiology and treatment of cancer. On a microscopic scale, neoplastic cells meet the conditions for evolution by Darwinian selection: cell reproduction with heritable variability that affects cell survival and replication. This suggests that, like other areas of biological and biomedical research, Darwinian theory can provide a general framework for understanding many aspects of cancer, including problems of great clinical importance. With the availability of raw molecular data increasing rapidly, this theory may provide guidance in translating data into understanding and progress. Several conceptual and analytical tools from evolutionary biology can be applied to cancer biology. Two clinical problems may benefit most from the application of Darwinian theory: neoplastic progression and acquired therapeutic resistance. The Darwinian theory of cancer has especially profound implications for drug development, both in terms of explaining past difficulties, and pointing the way toward new approaches. Because cancer involves complex evolutionary processes, research should incorporate both tractable (simplified) experimental systems, and also longitudinal observational studies of the evolutionary dynamics of cancer in laboratory animals and in human patients. Cancer biology will require new tools to control the evolution of neoplastic cells.
acquired drug resistance; cancer progression; drug development; natural selection; neoplasms; somatic evolution; stem cells; transdisciplinary research
The idea of an evolutionary sequence for humans is quite recent. Over the last 150 years, we have discovered unexpected ancestors, numerous close relatives and our deep evolutionary roots in Africa. In the last decade, three Late Miocene hominids have been described, two about 6 Ma (Ardipithecus and Orrorin) in East Africa and the third dated to about 7 Ma (Sahelanthropus) in Central Africa. The specimens are too few to propose definite relationship to other species, but clearly these belong to a new evolutive grade distinct from Australopithecus and Homo. Moreover, all of them were probably habitual bipeds and lived in woodlands, thus falsifying the savannah hypothesis of human origins. In light of all this recent knowledge, Charles Darwin predicted correctly in 1871 that Africa is the birthplace of humans, chimpanzees and our close relatives.
earliest hominids; central Africa; evolutionary grade; woodland origin
In recognition of the 200th anniversary of Charles Darwin's birth, this short article on flooding stress acknowledges not only Darwin's great contribution to the concept of evolution but also to the study of plant physiology. In modern biology, Darwin-inspired reductionist physiology continues to shed light on mechanisms that confer competitive advantage in many varied and challenging environments, including those where flooding is prevalent.
Mild flooding is experienced by most land plants but as its severity increases, fewer species are able to grow and survive. At the extreme, a highly exclusive aquatic lifestyle appears to have evolved numerous times over the past 120 million years. Although only 1–2% of angiosperms are aquatics, some of their adaptive characteristics are also seen in those adopting an amphibious lifestyle where flooding is less frequent. Lowland rice, the staple cereal for much of tropical Asia falls into this category. But, even amongst dry-land dwellers, or certain of their sub-populations, modest tolerance to occasional flooding is to be found, for example in wheat. The collection of papers summarized in this article describes advances to the understanding of mechanisms that explain flooding tolerance in aquatic, amphibious and dry-land plants. Work to develop more tolerant crops or manage flood-prone environments more effectively is also included. The experimental approaches range from molecular analyses, through biochemistry and metabolomics to whole-plant physiology, plant breeding and ecology.
Abiotic stress; adaptation; anoxia; Charles Darwin; environmental stress; evolution; flooding; hypoxia; rice; submergence; wetlands
In the Origin of Species Darwin hypothesized that the “manufactory” of species operates at different rates in different lineages and that the richness of taxonomic units is autocorrelated across levels of the taxonomic hierarchy. We confirm the manufactory hypothesis using a database of all the world's extant avian subspecies, species and genera. The hypothesis is confirmed both in correlations across all genera and in paired comparisons controlling for phylogeny. We also find that the modern risk of extinction, as measured by “Red List” classifications, differs across the different categories of genera identified by Darwin. Specifically, species in “manufactory” genera are less likely to be threatened, endangered or recently extinct than are “weak manufactory” genera. Therefore, although Darwin used his hypothesis to investigate past evolutionary processes, we find that the hypothesis also foreshadows future changes to the evolutionary tree.