The practice of classification and the theory of evolution,and what the demise of Charles Darwin's tree of life hypothesis means for both of them

Debates over the status of the tree of life (TOL) often proceed without agreement as to what it is supposed to be: a hierarchical classification scheme, a tracing of genomic and organismal history or a hypothesis about evolutionary processes and the patterns they can generate. I will argue that for Darwin it was a hypothesis, which lateral gene transfer in prokaryotes now shows to be false. I will propose a more general and relaxed evolutionary theory and point out why anti-evolutionists should take no comfort from disproof of the TOL hypothesis.     

Revisiting the concept of lineage in prokaryotes: a phylogenetic perspective

Mutation and lateral transfer are two categories of processes generating genetic diversity in prokaryotic genomes. Their relative importance varies between lineages, yet both are complementary rather than independent, separable evolutionary forces. The replication process inevitably merges together their effects on the genome. We develop the concept of “open lineages” to characterize evolutionary lineages that over time accumulate more changes in their genomes by lateral transfer than by mutation. They contrast with “closed lineages,” in which most of the changes are caused by mutation. Open and closed lineages are interspersed along the branches of any tree of prokaryotes. This patchy distribution conflicts with the basic assumptions of traditional phylogenetic approaches. As a result, a tree representation including both open and closed lineages is a misrepresentation. The evolution of all prokaryotic lineages cannot be studied under a single model unless new phylogenetic approaches that are more pluralistic about lineage evolution are designed.     

The naturalist in a world of genomics

Functional genomics provides new opportunities to address issues of fundamental interest in evolutionary biology and suggests many new research directions that are ripe for evolutionary investigation. New types of data, and the ability to study biological processes from a whole genome perspective, are likely to have a profound impact on evolutionary biology and ecology. To illustrate, we discuss how genomewide gene expression studies can be used to reformulate questions about trade-offs and pleiotropy. We then touch on some of the new research opportunities that the application of functional genomics affords to evolutionary biologists. We end with some brief notes about how evolutionary biology and comparative approaches will probably have an impact on functional genomics.     

A Resurgence in Field Research is Essential to Better Understand the Diversity,Ecology, and Evolution of Microbial Eukaryotes

The discovery and characterization of protist communities from diverse environments are crucial for understanding the overall evolutionary history of life on earth. However, major questions about the diversity, ecology, and evolutionary history of protists remain unanswered, notably because data obtained from natural protist communities, especially of heterotrophic species, remain limited. In this review, we discuss the challenges associated with “field protistology”, defined here as the exploration, characterization, and interpretation of microbial eukaryotic diversity within the context of natural environments or field experiments, and provide suggestions to help fill this important gap in knowledge. We also argue that increased efforts in field studies that combine molecular and microscopical methods offer the most promising path toward (1) the discovery of new lineages that expand the tree of eukaryotes; (2) the recognition of novel evolutionary patterns and processes; (3) the untangling of ecological interactions and functions, and their roles in larger ecosystem processes; and (4) the evaluation of protist adaptations to a changing climate.     

The tree of one percent

Two significant evolutionary processes are fundamentally not tree-like in nature - lateral gene transfer among prokaryotes and endosymbiotic gene transfer (from organelles) among eukaryotes. To incorporate such processes into the bigger picture of early evolution, biologists need to depart from the preconceived notion that all genomes are related by a single bifurcating tree.     

The Singular Quest for a Universal Tree of Life

Carl Woese developed a unique research program, based on rRNA, for discerning bacterial relationships and constructing a universal tree of life. Woese''s interest in the evolution of the genetic code led to him to investigate the deep roots of evolution, develop the concept of the progenote, and conceive of the Archaea. In so doing, he and his colleagues at the University of Illinois in Urbana revolutionized microbiology and brought the classification of microbes into an evolutionary framework. Woese also provided definitive evidence for the role of symbiosis in the evolution of the eukaryotic cell while underscoring the importance of lateral gene transfer in microbial evolution. Woese and colleagues'' proposal of three fundamental domains of life was brought forward in direct conflict with the prokaryote-eukaryote dichotomy. Together with several colleagues and associates, he brought together diverse evidence to support the rRNA evidence for the fundamentally tripartite nature of life. This paper aims to provide insight into his accomplishments, how he achieved them, and his place in the history of biology.     

Explosive radiation of a bacterial species group

The current diversity of life on earth is the product of macroevolutionary processes that have shaped the dynamics of diversification. Although the tempo of diversification has been studied extensively in macroorganisms, much less is known about the rates of diversification in the exceedingly diverse and species-rich microbiota. Decreases in diversification rates over time, a signature of explosive radiations, are commonly observed in plant and animal lineages. However, the few existing analyses of microbial lineages suggest that the tempo of diversification in prokaryotes may be fundamentally different. Here, we use multilocus and genomic sequence data to test hypotheses about the rate of diversification in a well-studied pathogenic bacterial lineage, Borrelia burgdorferi sensu lato (sl). Our analyses support the hypothesis that an explosive radiation of lineages occurred near the origin of the clade, followed by a sharp decay in diversification rates. These results suggest that explosive radiations may be a general feature of evolutionary history across the tree of life.     

Two faces of the prokaryote concept.

Bacteria had remained undefined when, in 1962, Roger Y. Stanier and C.B. van Niel published their famed paper 'The concept of a bacterium.' The articulation of the prokaryote-eukaryote dichotomy was a vital moment in the history of biology. This article provides a brief overview of the context in which the prokaryote concept was successfully launched in the 1960s, and what it was meant to connote. Two concepts were initially distinguished within the prokaryote-eukaryote dichotomy at that time. One was organizational and referred to comparative cell structure; the other was phylogenetic and referred to a 'natural' classification. Here, I examine how the two concepts became inseparable; how the prokaryotes came to signify a monophyletic group that preceded the eukaryotes, and how this view remained unquestioned for 15 years, until the birth of molecular evolutionary biology and coherent methods for bacteria phylogenetics based on 16S rRNA. Today, while microbial phylogeneticists generally agree that the prokaryote is a polyphyletic group, there is no agreement on whether the term should be maintained in an organizational sense.     

Teaching Evolution with Historical Narratives

This paper focuses on evolution as a unifying theme in biology education. Our aim is to argue that the different topics taught in secondary school biology classes should be enriched with and linked together by means of accounts of the history of life. We named this approach a “natural history perspective” on biology education. An essential aspect of the natural history perspective is the claim that evolutionary history forms the context for the development of an understanding of evolutionary processes. While there are some indications that a natural history perspective can function as a context for understanding micro-evolutionary processes, more research is called for.

Causal mechanisms of evolution and the capacity for niche construction

Ernst Mayr proposed a distinction between “proximate”, mechanistic, and “ultimate”, evolutionary, causes of biological phenomena. This dichotomy has influenced the thinking of many biologists, but it is increasingly perceived as impeding modern studies of evolutionary processes, including study of “niche construction” in which organisms alter their environments in ways supportive of their evolutionary success. Some still find value for this dichotomy in its separation of answers to “how?” versus “why?”questions about evolution. But “why is A?” questions about evolution necessarily take the form “how does A occur?”, so this separation is illusory. Moreover, the dichotomy distorts our view of evolutionary causality, in that, contra Mayr, the action of natural selection, driven by genotype-phenotype-environment interactions which constitute adaptations, is no less “proximate” than the biological mechanisms which are altered by naturally selected genetic variants. Mayr’s dichotomy thus needs replacement by more realistic, mechanistic views of evolution. From a mechanistic viewpoint, there is a continuum of adaptations from those evolving as responses to unchanging environmental pressures to those evolving as the capacity for niche construction, and intermediate stages of this can be identified. Some biologists postulate an association of “phenotypic plasticity” (phenotype-environment covariation with genotype held constant) with capacity for niche construction. Both “plasticity” and niche construction comprise wide ranges of adaptive mechanisms, often fully heritable and resulting from case-specific evolution. Association of “plasticity” with niche construction is most likely to arise in systems wherein capacity for complex learning and behavioral flexibility have already evolved.     

Charles Darwin's views of classification in theory and practice

It has long been argued that Charles Darwin was the founder of the school of "evolutionary taxonomy" of the Modern Synthesis and, accordingly, that he recognized genealogy and similarity as dual, synergistic criteria for classification. This view is based on three questionable interpretations: first, of isolated passages in the 13th chapter of the Origin of Species; second, of one phrase in a letter that Darwin wrote about the work of an author he had partly misunderstood; and third, of his taxonomic practice in the barnacle monographs, which only implicitly embody his philosophy of classification, if at all. These works, seen in fuller context and with the perspective of extensive correspondence, are consistent with the view that Darwin advocated only genealogy as the basis of classification, and that similarity was merely a tool for discovering evolutionary relationships. Darwin was neither a Mayrian taxonomist nor a cladist, and he did not approach systematic issues in the same terms that we do in the late 20th century.     

The fundamental units,processes and patterns of evolution,and the Tree of Life conundrum

Background

The elucidation of the dominant role of horizontal gene transfer (HGT) in the evolution of prokaryotes led to a severe crisis of the Tree of Life (TOL) concept and intense debates on this subject.

Concept

Prompted by the crisis of the TOL, we attempt to define the primary units and the fundamental patterns and processes of evolution. We posit that replication of the genetic material is the singular fundamental biological process and that replication with an error rate below a certain threshold both enables and necessitates evolution by drift and selection. Starting from this proposition, we outline a general concept of evolution that consists of three major precepts.1. The primary agency of evolution consists of Fundamental Units of Evolution (FUEs), that is, units of genetic material that possess a substantial degree of evolutionary independence. The FUEs include both bona fide selfish elements such as viruses, viroids, transposons, and plasmids, which encode some of the information required for their own replication, and regular genes that possess quasi-independence owing to their distinct selective value that provides for their transfer between ensembles of FUEs (genomes) and preferential replication along with the rest of the recipient genome.2. The history of replication of a genetic element without recombination is isomorphously represented by a directed tree graph (an arborescence, in the graph theory language). Recombination within a FUE is common between very closely related sequences where homologous recombination is feasible but becomes negligible for longer evolutionary distances. In contrast, shuffling of FUEs occurs at all evolutionary distances. Thus, a tree is a natural representation of the evolution of an individual FUE on the macro scale, but not of an ensemble of FUEs such as a genome.3. The history of life is properly represented by the "forest" of evolutionary trees for individual FUEs (Forest of Life, or FOL). Search for trends and patterns in the FOL is a productive direction of study that leads to the delineation of ensembles of FUEs that evolve coherently for a certain time span owing to a shared history of vertical inheritance or horizontal gene transfer; these ensembles are commonly known as genomes, taxa, or clades, depending on the level of analysis. A small set of genes (the universal genetic core of life) might show a (mostly) coherent evolutionary trend that transcends the entire history of cellular life forms. However, it might not be useful to denote this trend "the tree of life", or organismal, or species tree because neither organisms nor species are fundamental units of life.

Conclusion

A logical analysis of the units and processes of biological evolution suggests that the natural fundamental unit of evolution is a FUE, that is, a genetic element with an independent evolutionary history. Evolution of a FUE on the macro scale is naturally represented by a tree. Only the full compendium of trees for individual FUEs (the FOL) is an adequate depiction of the evolution of life. Coherent evolution of FUEs over extended evolutionary intervals is a crucial aspect of the history of life but a "species" or "organismal" tree is not a fundamental concept.

Reviewers

This articles was reviewed by Valerian Dolja, W. Ford Doolittle, Nicholas Galtier, and William Martin

     

生物进化研究的回顾与展望

生物进化是自然科学的永恒之迷。随着历史的发展和科学的进步,生物进化思想从早期的萌芽,到自然选择学说、新达尔文主义,从现代综合理论,到分子进化的中性学说。再到新灾变论和点断平衡论等。当前,由于生物学各分支学科的飞速发展．它们就各自的研究对象在宏观和微观上不断地拓展和深入,并在不同的层次上形成了广泛的交叉、渗透和融合,现代的进化生物学研究从宏观的表型到微观的分子,从群体遗传改变的微进化到成种事件以及地史上生物类群谱系演化的宏进化,从直接的化石证据到基于形态性状、分子证据和环境变迁的综合推理,从基于遗传基础的比较基因组学到演化机理的进化发育生物学等。可以预见,在新的世纪里,在哲学和具体方法论(如系统论、控制论和信息论)的指导下,在生命科学、其他自然科学乃至社会科学工作者的通力合作下,综合遗传、发育和进化等研究领域的各种理论成果,生物进化理论即将出现也一定会出现的一个新的大综合和新的大统一。     

In What Sense Does ‘Nothing Make Sense Except in the Light of Evolution’?

Dobzhansky argued that biology only makes sense if life on earth has a shared history. But his dictum is often reinterpreted to mean that biology only makes sense in the light of adaptation. Some philosophers of science have argued in this spirit that all work in 'proximal' biosciences such as anatomy, physiology and molecular biology must be framed, at least implicitly, by the selection histories of the organisms under study. Others have denied this and have proposed non-evolutionary ways in which biologists can frame these investigations. This paper argues that an evolutionary perspective is indeed necessary, but that it must be a forward-looking perspective informed by a general understanding of the evolutionary process, not a backward-looking perspective informed by the specific evolutionary history of the species being studied. Interestingly, it turns out that there are aspects of proximal biology that even a creationist cannot study except in the light of a theory of their effect on future evolution.     

Fungal evolution: cellular,genomic and metabolic complexity

The question of how phenotypic and genomic complexity are inter‐related and how they are shaped through evolution is a central question in biology that historically has been approached from the perspective of animals and plants. In recent years, however, fungi have emerged as a promising alternative system to address such questions. Key to their ecological success, fungi present a broad and diverse range of phenotypic traits. Fungal cells can adopt many different shapes, often within a single species, providing them with great adaptive potential. Fungal cellular organizations span from unicellular forms to complex, macroscopic multicellularity, with multiple transitions to higher or lower levels of cellular complexity occurring throughout the evolutionary history of fungi. Similarly, fungal genomes are very diverse in their architecture. Deep changes in genome organization can occur very quickly, and these phenomena are known to mediate rapid adaptations to environmental changes. Finally, the biochemical complexity of fungi is huge, particularly with regard to their secondary metabolites, chemical products that mediate many aspects of fungal biology, including ecological interactions. Herein, we explore how the interplay of these cellular, genomic and metabolic traits mediates the emergence of complex phenotypes, and how this complexity is shaped throughout the evolutionary history of Fungi.     

Phylogenomics and the reconstruction of the tree of life

As more complete genomes are sequenced, phylogenetic analysis is entering a new era - that of phylogenomics. One branch of this expanding field aims to reconstruct the evolutionary history of organisms on the basis of the analysis of their genomes. Recent studies have demonstrated the power of this approach, which has the potential to provide answers to several fundamental evolutionary questions. However, challenges for the future have also been revealed. The very nature of the evolutionary history of organisms and the limitations of current phylogenetic reconstruction methods mean that part of the tree of life might prove difficult, if not impossible, to resolve with confidence.     

Prokaryotic biosphere

The life philosophy aspects of natural sciences are discussed. The key role of prokaryotes in the origin, development, and existence of the biosphere is considered. It helps to understand how the penetration in the world of prokaryotes changes our notions of the place of biology in natural sciences.     

Understanding Evolutionary Trees

Charles Darwin sketched his first evolutionary tree in 1837, and trees have remained a central metaphor in evolutionary biology up to the present. Today, phylogenetics—the science of constructing and evaluating hypotheses about historical patterns of descent in the form of evolutionary trees—has become pervasive within and increasingly outside evolutionary biology. Fostering skills in “tree thinking” is therefore a critical component of biological education. Conversely, misconceptions about evolutionary trees can be very detrimental to one’s understanding of the patterns and processes that have occurred in the history of life. This paper provides a basic introduction to evolutionary trees, including some guidelines for how and how not to read them. Ten of the most common misconceptions about evolutionary trees and their implications for understanding evolution are addressed.

The evolution of cooperative breeding in birds: kinship,dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.     

Brain reorganization,not relative brain size,primarily characterizes anthropoid brain evolution

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.