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1.  Trees and networks before and after Darwin 
Biology Direct  2009;4:43.
It is well-known that Charles Darwin sketched abstract trees of relationship in his 1837 notebook, and depicted a tree in the Origin of Species (1859). Here I attempt to place Darwin's trees in historical context. By the mid-Eighteenth century the Great Chain of Being was increasingly seen to be an inadequate description of order in nature, and by about 1780 it had been largely abandoned without a satisfactory alternative having been agreed upon. In 1750 Donati described aquatic and terrestrial organisms as forming a network, and a few years later Buffon depicted a network of genealogical relationships among breeds of dogs. In 1764 Bonnet asked whether the Chain might actually branch at certain points, and in 1766 Pallas proposed that the gradations among organisms resemble a tree with a compound trunk, perhaps not unlike the tree of animal life later depicted by Eichwald. Other trees were presented by Augier in 1801 and by Lamarck in 1809 and 1815, the latter two assuming a transmutation of species over time. Elaborate networks of affinities among plants and among animals were depicted in the late Eighteenth and very early Nineteenth centuries. In the two decades immediately prior to 1837, so-called affinities and/or analogies among organisms were represented by diverse geometric figures. Series of plant and animal fossils in successive geological strata were represented as trees in a popular textbook from 1840, while in 1858 Bronn presented a system of animals, as evidenced by the fossil record, in a form of a tree. Darwin's 1859 tree and its subsequent elaborations by Haeckel came to be accepted in many but not all areas of biological sciences, while network diagrams were used in others. Beginning in the early 1960s trees were inferred from protein and nucleic acid sequences, but networks were re-introduced in the mid-1990s to represent lateral genetic transfer, increasingly regarded as a fundamental mode of evolution at least for bacteria and archaea. In historical context, then, the Network of Life preceded the Tree of Life and might again supersede it.
Reviewers
This article was reviewed by Eric Bapteste, Patrick Forterre and Dan Graur.
doi:10.1186/1745-6150-4-43
PMCID: PMC2793248  PMID: 19917100
2.  From documents to datasets: A MediaWiki-based method of annotating and extracting species observations in century-old field notebooks 
ZooKeys  2012;235-253.
Part diary, part scientific record, biological field notebooks often contain details necessary to understanding the location and environmental conditions existent during collecting events. Despite their clear value for (and recent use in) global change studies, the text-mining outputs from field notebooks have been idiosyncratic to specific research projects, and impossible to discover or re-use. Best practices and workflows for digitization, transcription, extraction, and integration with other sources are nascent or non-existent. In this paper, we demonstrate a workflow to generate structured outputs while also maintaining links to the original texts. The first step in this workflow was to place already digitized and transcribed field notebooks from the University of Colorado Museum of Natural History founder, Junius Henderson, on Wikisource, an open text transcription platform. Next, we created Wikisource templates to document places, dates, and taxa to facilitate annotation and wiki-linking. We then requested help from the public, through social media tools, to take advantage of volunteer efforts and energy. After three notebooks were fully annotated, content was converted into XML and annotations were extracted and cross-walked into Darwin Core compliant record sets. Finally, these recordsets were vetted, to provide valid taxon names, via a process we call “taxonomic referencing.” The result is identification and mobilization of 1,068 observations from three of Henderson’s thirteen notebooks and a publishable Darwin Core record set for use in other analyses. Although challenges remain, this work demonstrates a feasible approach to unlock observations from field notebooks that enhances their discovery and interoperability without losing the narrative context from which those observations are drawn.
“Compose your notes as if you were writing a letter to someone a century in the future.”
Perrine and Patton (2011)
doi:10.3897/zookeys.209.3247
PMCID: PMC3406479  PMID: 22859891
Field notes; notebooks; crowd sourcing; digitization; biodiversity; transcription; text-mining; Darwin Core; Junius Henderson; annotation; taxonomic referencing; natural history; Wikisource; Colorado; species occurrence records
3.  Epigenetics and the Evolution of Darwin’s Finches 
Genome Biology and Evolution  2014;6(8):1972-1989.
The prevailing theory for the molecular basis of evolution involves genetic mutations that ultimately generate the heritable phenotypic variation on which natural selection acts. However, epigenetic transgenerational inheritance of phenotypic variation may also play an important role in evolutionary change. A growing number of studies have demonstrated the presence of epigenetic inheritance in a variety of different organisms that can persist for hundreds of generations. The possibility that epigenetic changes can accumulate over longer periods of evolutionary time has seldom been tested empirically. This study was designed to compare epigenetic changes among several closely related species of Darwin’s finches, a well-known example of adaptive radiation. Erythrocyte DNA was obtained from five species of sympatric Darwin’s finches that vary in phylogenetic relatedness. Genome-wide alterations in genetic mutations using copy number variation (CNV) were compared with epigenetic alterations associated with differential DNA methylation regions (epimutations). Epimutations were more common than genetic CNV mutations among the five species; furthermore, the number of epimutations increased monotonically with phylogenetic distance. Interestingly, the number of genetic CNV mutations did not consistently increase with phylogenetic distance. The number, chromosomal locations, regional clustering, and lack of overlap of epimutations and genetic mutations suggest that epigenetic changes are distinct and that they correlate with the evolutionary history of Darwin’s finches. The potential functional significance of the epimutations was explored by comparing their locations on the genome to the location of evolutionarily important genes and cellular pathways in birds. Specific epimutations were associated with genes related to the bone morphogenic protein, toll receptor, and melanogenesis signaling pathways. Species-specific epimutations were significantly overrepresented in these pathways. As environmental factors are known to result in heritable changes in the epigenome, it is possible that epigenetic changes contribute to the molecular basis of the evolution of Darwin’s finches.
doi:10.1093/gbe/evu158
PMCID: PMC4159007  PMID: 25062919
epimutations; DNA methylation; copy number variation; phylogeny; adaptive radiation; BMP; toll; melanogenesis
4.  Charles Darwin and the Origin of Life 
When Charles Darwin published The Origin of Species 150 years ago he consciously avoided discussing the origin of life. However, analysis of some other texts written by Darwin, and of the correspondence he exchanged with friends and colleagues demonstrates that he took for granted the possibility of a natural emergence of the first life forms. As shown by notes from the pages he excised from his private notebooks, as early as 1837 Darwin was convinced that “the intimate relation of Life with laws of chemical combination, & the universality of latter render spontaneous generation not improbable”. Like many of his contemporaries, Darwin rejected the idea that putrefaction of preexisting organic compounds could lead to the appearance of organisms. Although he favored the possibility that life could appear by natural processes from simple inorganic compounds, his reluctance to discuss the issue resulted from his recognition that at the time it was possible to undertake the experimental study of the emergence of life.
doi:10.1007/s11084-009-9172-7
PMCID: PMC2745620  PMID: 19633921
Darwin; Warm little pond; Origin of life; Spontaneous generation
5.  A review of the diversity and evolution of photonic structures in butterflies, incorporating the work of John Huxley (The Natural History Museum, London from 1961 to 1990) 
The photonic structures of butterfly wings are among the most anatomically diverse of all those in nature, giving rise to an unrivalled display of structural colours. These have recently become the focus of research by workers in a variety of disciplines, stimulated by their potential applications to technology (‘biomimetics’). This interest, together with the discovery of unpublished electron micrographs taken by the late Dr John Huxley (Natural History Museum, London), prompted this review of butterfly photonics in general. The current work provides a synopsis of the literature to date, covering the diversity and evolution of these optical structures and incorporating Huxley's work, which represents an important biomimetic and evolutionary database on its own. This review deals with butterfly photonic devices according to the parts of the butterfly scales on which they occur. In this way, the information is ripe for evolutionary study.
doi:10.1098/rstb.2007.2258
PMCID: PMC2606806  PMID: 18331987
photonic; interference; structural colour; butterfly; diversity; evolution
6.  Genetic Tests for Ecological and Allopatric Speciation in Anoles on an Island Archipelago 
PLoS Genetics  2010;6(4):e1000929.
From Darwin's study of the Galapagos and Wallace's study of Indonesia, islands have played an important role in evolutionary investigations, and radiations within archipelagos are readily interpreted as supporting the conventional view of allopatric speciation. Even during the ongoing paradigm shift towards other modes of speciation, island radiations, such as the Lesser Antillean anoles, are thought to exemplify this process. Geological and molecular phylogenetic evidence show that, in this archipelago, Martinique anoles provide several examples of secondary contact of island species. Four precursor island species, with up to 8 mybp divergence, met when their islands coalesced to form the current island of Martinique. Moreover, adjacent anole populations also show marked adaptation to distinct habitat zonation, allowing both allopatric and ecological speciation to be tested in this system. We take advantage of this opportunity of replicated island coalescence and independent ecological adaptation to carry out an extensive population genetic study of hypervariable neutral nuclear markers to show that even after these very substantial periods of spatial isolation these putative allospecies show less reproductive isolation than conspecific populations in adjacent habitats in all three cases of subsequent island coalescence. The degree of genetic interchange shows that while there is always a significant genetic signature of past allopatry, and this may be quite strong if the selection regime allows, there is no case of complete allopatric speciation, in spite of the strong primae facie case for it. Importantly there is greater genetic isolation across the xeric/rainforest ecotone than is associated with any secondary contact. This rejects the development of reproductive isolation in allopatric divergence, but supports the potential for ecological speciation, even though full speciation has not been achieved in this case. It also explains the paucity of anole species in the Lesser Antilles compared to the Greater Antilles.
Author Summary
Over the last 150 years, since Darwin's study of islands and his “Origin of Species,” island archipelagos have played a central role in the understanding of evolution and how species multiply (speciation). Islands epitomise the conventional view of geographic (allopatric) speciation, where genomes diverge in isolation until accumulated differences result in reproductive isolation and the capacity to coexist without interbreeding. Current-day Martinique in the Lesser Antilles is composed of several ancient islands that have only recently coalesced into a single entity. The molecular phylogeny and geology show that these ancient islands have had their own tree lizard (anole) species for a very long time, about six to eight million years. Now they have met, we can genetically test for reproductive isolation. However, when we use selectively neutral markers from the nuclear genome, on this naturally replicated system, we can see that these anoles are freely exchanging genes and not behaving as species. Indeed, there is more genetic isolation between adjacent populations of the same species from different habitats than between separate putative allospecies from the ancient islands. This rejects allopatric speciation in a case study from a system thought to exemplify it, and suggests the potential importance of ecological speciation.
doi:10.1371/journal.pgen.1000929
PMCID: PMC2861690  PMID: 20442860
7.  Darwin's Galápagos finches in modern biology 
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.
doi:10.1098/rstb.2009.0321
PMCID: PMC2830240  PMID: 20194163
Darwin's finches; evolution; speciation; adaptive radiation
8.  Characterising the Phenotypic Diversity of Papilio dardanus Wing Patterns Using an Extensive Museum Collection 
PLoS ONE  2014;9(5):e96815.
The history of 20th Century evolutionary biology can be followed through the study of mimetic butterflies. From the initial findings of discontinuous polymorphism through the debates regarding the evolution of mimicry and the step-size of evolutionary change, to the studies on supergene evolution and molecular characterisation of butterfly genomes, mimetic butterflies have been at the heart of evolutionary thought for over 100 years. During this time, few species have received as much attention and in-depth study as Papilio dardanus. To assist all aspects of mimicry research, we present a complete data-derived overview of the extent of polymorphism within this species. Using historical samples permanently held by the NHM London, we document the extent of phenotypic variation and characterise the diversity present in each of the subspecies and how it varies across Africa. We also demonstrate an association between “imperfect” mimetic forms and the transitional race formed in the area where Eastern and Western African populations meet around Lake Victoria. We present a novel portal for access to this collection, www.mimeticbutterflies.org, allowing remote access to this unique repository. It is hoped that this online resource can act as a nucleus for the sharing and dissemination of other collections databases and imagery connected with mimetic butterflies.
doi:10.1371/journal.pone.0096815
PMCID: PMC4023932  PMID: 24837717
9.  Biogeographic and diversification patterns of Neotropical Troidini butterflies (Papilionidae) support a museum model of diversity dynamics for Amazonia 
Background
The temporal and geographical diversification of Neotropical insects remains poorly understood because of the complex changes in geological and climatic conditions that occurred during the Cenozoic. To better understand extant patterns in Neotropical biodiversity, we investigated the evolutionary history of three Neotropical swallowtail Troidini genera (Papilionidae). First, DNA-based species delimitation analyses were conducted to assess species boundaries within Neotropical Troidini using an enlarged fragment of the standard barcode gene. Molecularly delineated species were then used to infer a time-calibrated species-level phylogeny based on a three-gene dataset and Bayesian dating analyses. The corresponding chronogram was used to explore their temporal and geographical diversification through distinct likelihood-based methods.
Results
The phylogeny for Neotropical Troidini was well resolved and strongly supported. Molecular dating and biogeographic analyses indicate that the extant lineages of Neotropical Troidini have a late Eocene (33–42 Ma) origin in North America. Two independent lineages (Battus and Euryades + Parides) reached South America via the GAARlandia temporary connection, and later became extinct in North America. They only began substantive diversification during the early Miocene in Amazonia. Macroevolutionary analysis supports the “museum model” of diversification, rather than Pleistocene refugia, as the best explanation for the diversification of these lineages.
Conclusions
This study demonstrates that: (i) current Neotropical biodiversity may have originated ex situ; (ii) the GAARlandia bridge was important in facilitating invasions of South America; (iii) colonization of Amazonia initiated the crown diversification of these swallowtails; and (iv) Amazonia is not only a species-rich region but also acted as a sanctuary for the dynamics of this diversity. In particular, Amazonia probably allowed the persistence of old lineages and contributed to the steady accumulation of diversity over time with constant net diversification rates, a result that contrasts with previous studies on other South American butterflies.
doi:10.1186/1471-2148-12-82
PMCID: PMC3464124  PMID: 22690927
Amazon rainforest; Andean uplift; Biogeography; Diversification; GAARlandia connection; Swallowtail butterflies
10.  Gulliver's further travels: the necessity and difficulty of a hierarchical theory of selection. 
For principled and substantially philosophical reasons, based largely on his reform of natural history by inverting the Paleyan notion of overarching and purposeful beneficence in the construction of organisms, Darwin built his theory of selection at the single causal level of individual bodies engaged in unconscious (and metaphorical) struggle for their own reproductive success. But the central logic of the theory allows selection to work effectively on entities at several levels of a genealogical hierarchy, provided that they embody a set of requisite features for defining evolutionary individuality. Genes, cell lineages, demes, species, and clades-as well as Darwin's favoured organisms-embody these requisite features in enough cases to form important levels of selection in the history of life. R. A. Fisher explicitly recognized the unassailable logic of species selection, but denied that thsi real process could be important in evolution because, compared with the production of new organisms within a species, the origin of new species is so rare, and the number of species within most clades so low. I review this and other classical arguments against higher-level selection, and conclude (in the first part of this paper) that they are invalid in practice for interdemic selection, and false in principle for species selection. Punctuated equilibrium defines the individuality of species and refutes Fisher's classical argument based on cycle time. In the second part of the paper, I argue that we have failed to appreciate the range and power of selection at levels above and below the organismic because we falsely extrapolate the defining properties of organisms to these other levels (which are characterized by quite different distinctive features), and then regard the other levels as impotent because their effective individuals differ so much from organisms. We would better appreciate the power and generality of hierarchical models of selection if we grasped two key principles: first, that levels can interact in all modes (positively, negatively, and orthogonally), and not only in the negative style (with a higher level suppressing an opposing force of selection from the lower level) that, for heuristic and operational reasons, has received almost exclusive attention in the existing literature; and second, that each hierarchical level differs from all others in substantial and interesting ways, both in the style and frequency of patterns in change and causal modes.
PMCID: PMC1692213  PMID: 9533127
11.  From the scala naturae to the symbiogenetic and dynamic tree of life 
Biology Direct  2011;6:33.
All living beings on Earth, from bacteria to humans, are connected through descent from common ancestors and represent the summation of their corresponding, ca. 3500 million year long evolutionary history. However, the evolution of phenotypic features is not predictable, and biologists no longer use terms such as "primitive" or "perfect organisms". Despite these insights, the Bible-based concept of the so-called "ladder of life" or Scala Naturae, i.e., the idea that all living beings can be viewed as representing various degrees of "perfection", with humans at the very top of this biological hierarchy, was popular among naturalists until ca. 1850 (Charles Bonnet, Jean Lamarck and others). Charles Darwin is usually credited with the establishment of a branched evolutionary "Tree of Life". This insight of 1859 was based on his now firmly corroborated proposals of common ancestry and natural selection. In this article I argue that Darwin was still influenced by "ladder thinking", a theological view that prevailed throughout the 19th century and is also part of Ernst Haeckel's famous Oak tree (of Life) of 1866, which is, like Darwin's scheme, static. In 1910, Constantin Mereschkowsky proposed an alternative, "anti-selectionist" concept of biological evolution, which became known as the symbiogenesis-theory. According to the symbiogenesis-scenario, eukaryotic cells evolved on a static Earth from archaic prokaryotes via the fusion and subsequent cooperation of certain microbes. In 1929, Alfred Wegener published his theory of continental drift, which was later corroborated, modified and extended. The resulting theory of plate tectonics is now the principal organizing concept of geology. Over millions of years, plate tectonics and hence the "dynamic Earth" has caused destructive volcanic eruptions and earthquakes. At the same time, it created mountain ranges, deep oceans, novel freshwater habitats, and deserts. As a result, these geologic processes destroyed numerous populations of organisms, and produced the environmental conditions for new species of animals, plants and microbes to adapt and evolve. In this article I propose a tree-like "symbiogenesis, natural selection, and dynamic Earth (synade)-model" of macroevolution that is based on these novel facts and data.
Reviewers
This article was reviewed by Mark Ragan, W. Ford Doolittle, and Staffan Müller-Wille.
doi:10.1186/1745-6150-6-33
PMCID: PMC3154191  PMID: 21714937
12.  Evolution of Genome Architecture 
Charles Darwin believed that all traits of organisms have been honed to near perfection by natural selection. The empirical basis underlying Darwin’s conclusions consisted of numerous observations made by him and other naturalists on the exquisite adaptations of animals and plants to their natural habitats and on the impressive results of artificial selection. Darwin fully appreciated the importance of heredity but was unaware of the nature and, in fact, the very existence of genomes. A century and a half after the publication of the “Origin”, we have the opportunity to draw conclusions from the comparisons of hundreds of genome sequences from all walks of life. These comparisons suggest that the dominant mode of genome evolution is quite different from that of the phenotypic evolution. The genomes of vertebrates, those purported paragons of biological perfection, turned out to be veritable junkyards of selfish genetic elements where only a small fraction of the genetic material is dedicated to encoding biologically relevant information. In sharp contrast, genomes of microbes and viruses are incomparably more compact, with most of the genetic material assigned to distinct biological functions. However, even in these genomes, the specific genome organization (gene order) is poorly conserved. The results of comparative genomics lead to the conclusion that the genome architecture is not a straightforward result of continuous adaptation but rather is determined by the balance between the selection pressure, that is itself dependent on the effective population size and mutation rate, the level of recombination, and the activity of selfish elements. Although genes and, in many cases, multigene regions of genomes possess elaborate architectures that ensure regulation of expression, these arrangements are evolutionarily volatile and typically change substantially even on short evolutionary scales when gene sequences diverge minimally. Thus, the observed genome archtiectures are, mostly, products of neutral processes or epiphenomena of more general selective processes, such as selection for genome streamlining in successful lineages with large populations. Selection for specific gene arrangements (elements of genome architecture) seems only to modulate the results of these processes.
doi:10.1016/j.biocel.2008.09.015
PMCID: PMC3272702  PMID: 18929678
13.  Rhizome of life, catastrophes, sequence exchanges, gene creations, and giant viruses: how microbial genomics challenges Darwin 
Darwin's theory about the evolution of species has been the object of considerable dispute. In this review, we have described seven key principles in Darwin's book The Origin of Species and tried to present how genomics challenge each of these concepts and improve our knowledge about evolution. Darwin believed that species evolution consists on a positive directional selection ensuring the “survival of the fittest.” The most developed state of the species is characterized by increasing complexity. Darwin proposed the theory of “descent with modification” according to which all species evolve from a single common ancestor through a gradual process of small modification of their vertical inheritance. Finally, the process of evolution can be depicted in the form of a tree. However, microbial genomics showed that evolution is better described as the “biological changes over time.” The mode of change is not unidirectional and does not necessarily favors advantageous mutations to increase fitness it is rather subject to random selection as a result of catastrophic stochastic processes. Complexity is not necessarily the completion of development: several complex organisms have gone extinct and many microbes including bacteria with intracellular lifestyle have streamlined highly effective genomes. Genomes evolve through large events of gene deletions, duplications, insertions, and genomes rearrangements rather than a gradual adaptative process. Genomes are dynamic and chimeric entities with gene repertoires that result from vertical and horizontal acquisitions as well as de novo gene creation. The chimeric character of microbial genomes excludes the possibility of finding a single common ancestor for all the genes recorded currently. Genomes are collections of genes with different evolutionary histories that cannot be represented by a single tree of life (TOL). A forest, a network or a rhizome of life may be more accurate to represent evolutionary relationships among species.
doi:10.3389/fcimb.2012.00113
PMCID: PMC3428605  PMID: 22973559
catastrophes; Darwin; gene creation; giant viruses; micorbial genomics; rhizome of life; sequence exchange
14.  Frequency-Dependent Selection Predicts Patterns of Radiations and Biodiversity 
PLoS Computational Biology  2010;6(8):e1000892.
Most empirical studies support a decline in speciation rates through time, although evidence for constant speciation rates also exists. Declining rates have been explained by invoking pre-existing niches, whereas constant rates have been attributed to non-adaptive processes such as sexual selection and mutation. Trends in speciation rate and the processes underlying it remain unclear, representing a critical information gap in understanding patterns of global diversity. Here we show that the temporal trend in the speciation rate can also be explained by frequency-dependent selection. We construct a frequency-dependent and DNA sequence-based model of speciation. We compare our model to empirical diversity patterns observed for cichlid fish and Darwin's finches, two classic systems for which speciation rates and richness data exist. Negative frequency-dependent selection predicts well both the declining speciation rate found in cichlid fish and explains their species richness. For groups like the Darwin's finches, in which speciation rates are constant and diversity is lower, speciation rate is better explained by a model without frequency-dependent selection. Our analysis shows that differences in diversity may be driven by incipient species abundance with frequency-dependent selection. Our results demonstrate that genetic-distance-based speciation and frequency-dependent selection are sufficient to explain the high diversity observed in natural systems and, importantly, predict decay through time in speciation rate in the absence of pre-existing niches.
Author Summary
Ecological opportunity, or filling a pre-existing unoccupied adaptive zone, is considered the dominant mechanism explaining the initial explosion of diversity. Although this type of niche filling can explain rates of diversification in some lineages, it is not sufficient for a radiation to occur. Instead of attributing the propensity to have an explosion of new species to external influences like niche availability, an alternative hypothesis can be based in frequency-dependent selection driven by the ecology in which organisms are embedded or endogenous sources mediated by gametes during fertilization. We show that genome diversification driven by higher reproductive probability of rare genotypes generates rapid initial speciation followed by a plateau with very low speciation rates, as shown by most empirical data. The absence of advantage of rare genotypes generates speciation events at constant rates. We predict decline over time and constant speciation rate in the cichlids and Darwin's finches, respectively, thus providing an alternative hypothesis for the origin of radiations and biodiversity in the absence of pre-existing niche filling. In addition to predicting observed temporal trends in diversification, our analysis also highlights new mechanistic models of evolutionary biodiversity dynamics that may become suitable to generate neutral models for testing observed patterns in speciation rates and species diversity.
doi:10.1371/journal.pcbi.1000892
PMCID: PMC2928887  PMID: 20865126
15.  Formalizing Darwinism and inclusive fitness theory 
Inclusive fitness maximization is a basic building block for biological contributions to any theory of the evolution of society. There is a view in mathematical population genetics that nothing is caused to be maximized in the process of natural selection, but this is explained as arising from a misunderstanding about the meaning of fitness maximization. Current theoretical work on inclusive fitness is discussed, with emphasis on the author's ‘formal Darwinism project’. Generally, favourable conclusions are drawn about the validity of assuming fitness maximization, but the need for continuing work is emphasized, along with the possibility that substantive exceptions may be uncovered. The formal Darwinism project aims more ambitiously to represent in a formal mathematical framework the central point of Darwin's Origin of Species, that the mechanical processes of inheritance and reproduction can give rise to the appearance of design, and it is a fitting ambition in Darwin's bicentenary year to capture his most profound discovery in the lingua franca of science.
doi:10.1098/rstb.2009.0056
PMCID: PMC2781868  PMID: 19805422
formal Darwinism; fitness optimization; Price equation; uncertainty; dynamic insufficiency
16.  Towards a postmodern synthesis of evolutionary biology 
Cell cycle (Georgetown, Tex.)  2009;8(6):799-800.
In 2009, we are celebrating the 200th anniversary of Charles Darwin and the 150th jubilee of his masterpiece, the Origin of Species. Darwin developed the first coherent and compelling narrative of biological evolution and thus founded evolutionary biology—and modern biology in general, remembering the famous dictum of Dobzhansky. It is, however, counter-productive, and ultimately, a disservice to Darwin’s legacy, to define modern evolutionary biology as neo-Darwinism. The current picture of evolution, informed, in particular, by results of comparative genomics and systems biology, is by far more complex than that presented in the Origin of Species, so that Darwinian principles, including natural selection, are incorporated into the evolving new synthesis as important but certainly not all-embracing tenets. This expansion of evolutionary biology does not denigrate Darwin in the least but rather emphasizes the fertility of his ideas.
PMCID: PMC3410441  PMID: 19242109
Darwin’s anniversary; Darwinism; modern synthesis; genome evolution; systems biology; horizontal gene transfer; Tree of Life
17.  Charles Darwin’s Mitochondria 
Genetics  2013;194(1):21-25.
Charles Darwin’s long-term illness has been the subject of much speculation. His numerous symptoms have led to conclusions that his illness was essentially psychogenic in nature. These diagnoses have never been fully convincing, however, particularly in regard to the proposed underlying psychological background causes of the illness. Similarly, two proposed somatic causes of illness, Chagas disease and arsenic poisoning, lack credibility and appear inconsistent with the lifetime history of the illness. Other physical explanations are simply too incomplete to explain the range of symptoms. Here, a very different sort of explanation will be offered. We now know that mitochondrial mutations producing impaired mitochondrial function may result in a wide range of differing symptoms, including symptoms thought to be primarily psychological. Examination of Darwin’s maternal family history supports the contention that his illness was mitochondrial in nature; his mother and one maternal uncle had strange illnesses and the youngest maternal sibling died of an infirmity with symptoms characteristic of mitochondrial encephalomyopathy, lactic acidosis, and stroke-like episodes (MELAS syndrome), a condition rooted in mitochondrial dysfunction. Darwin’s own symptoms are described here and are in accord with the hypothesis that he had the mtDNA mutation commonly associated with the MELAS syndrome.
doi:10.1534/genetics.113.151241
PMCID: PMC3632469  PMID: 23633139
18.  Alzheimer's disease and natural cognitive aging may represent adaptive metabolism reduction programs 
The present article examines several lines of converging evidence suggesting that the slow and insidious brain changes that accumulate over the lifespan, resulting in both natural cognitive aging and Alzheimer's disease (AD), represent a metabolism reduction program. A number of such adaptive programs are known to accompany aging and are thought to have decreased energy requirements for ancestral hunter-gatherers in their 30s, 40s and 50s. Foraging ability in modern hunter-gatherers declines rapidly, more than a decade before the average terminal age of 55 years. Given this, the human brain would have been a tremendous metabolic liability that must have been advantageously tempered by the early cellular and molecular changes of AD which begin to accumulate in all humans during early adulthood. Before the recent lengthening of life span, individuals in the ancestral environment died well before this metabolism reduction program resulted in clinical AD, thus there was never any selective pressure to keep adaptive changes from progressing to a maladaptive extent.
Aging foragers may not have needed the same cognitive capacities as their younger counterparts because of the benefits of accumulated learning and life experience. It is known that during both childhood and adulthood metabolic rate in the brain decreases linearly with age. This trend is thought to reflect the fact that children have more to learn. AD "pathology" may be a natural continuation of this trend. It is characterized by decreasing cerebral metabolism, selective elimination of synapses and reliance on accumulating knowledge (especially implicit and procedural) over raw brain power (working memory). Over decades of subsistence, the behaviors of aging foragers became routinized, their motor movements automated and their expertise ingrained to a point where they no longer necessitated the first-rate working memory they possessed when younger and learning actively. Alzheimer changes selectively and precisely mediate an adaptation to this major life-history transition.
AD symptomatology shares close similarities with deprivation syndromes in other animals including the starvation response. Both molecular and anatomical features of AD imitate brain changes that have been conceptualized as adaptive responses to low food availability in mammals and birds. Alzheimer's patients are known to express low overall metabolic rates and are genetically inclined to exhibit physiologically thrifty traits widely thought to allow mammals to subsist under conditions of nutritional scarcity. Additionally, AD is examined here in the contexts of anthropology, comparative neuroscience, evolutionary medicine, expertise, gerontology, neural Darwinism, neuroecology and the thrifty genotype.
doi:10.1186/1744-9081-5-13
PMCID: PMC2653533  PMID: 19250550
19.  Cooperation and deception: from evolution to mechanisms 
Nature is full of struggle, as predicted by the theory of evolution through natural selection, yet there are also paramount examples where individuals help each other. These instances of helping have been difficult to reconcile with Darwin's theory because it is not always obvious how individuals are working for their own direct benefit. Consequently, initial publications that offered solutions to subsets of the observed cases of helping, such as kin selection or reciprocity, are among the most influential and most cited papers in evolution/behavioural ecology. During the last few years, a wave of new studies and concepts has considerably advanced our understanding of the conditions under which individuals are selected to help others. On the empirical side, advances are due to stronger incorporation of the natural history of each study species and an emphasis on proximate questions regarding decision-making processes. In parallel, theorists have provided more realistic models together with an increased exploration of the importance of life history and ecology in understanding cooperation. The ideas presented by the authors of this volume represent, in many ways, the revolutionary new approach to studying behaviour which is currently underway.
doi:10.1098/rstb.2010.0155
PMCID: PMC2942876  PMID: 20679104
cooperation; game theory; helping; deception; cheating; cognition
20.  On the origins of sexual dimorphism in butterflies 
The processes governing the evolution of sexual dimorphism provided a foundation for sexual selection theory. Two alternative processes, originally proposed by Darwin and Wallace, differ primarily in the timing of events creating the dimorphism. In the process advocated by Darwin, a novel ornament arises in a single sex, with no temporal separation in the origin and sex-limitation of the novel trait. By contrast, Wallace proposed a process where novel ornaments appear simultaneously in both sexes, but are then converted into sex-limited expression by natural selection acting against showy coloration in one sex. Here, we investigate these alternative modes of sexual dimorphism evolution in a phylogenetic framework and demonstrate that both processes contribute to dimorphic wing patterns in the butterfly genera Bicyclus and Junonia. In some lineages, eyespots and bands arise in a single sex, whereas in other lineages they appear in both sexes but are then lost in one of the sexes. In addition, lineages displaying sexual dimorphism were more likely to become sexually monomorphic than they were to remain dimorphic. This derived monomorphism was either owing to a loss of the ornament (‘drab monomorphism’) or owing to a gain of the same ornament by the opposite sex (‘mutual ornamentation’). Our results demonstrate the necessity of a plurality in theories explaining the evolution of sexual dimorphism within and across taxa. The origins and evolutionary fate of sexual dimorphism are probably influenced by underlying genetic architecture responsible for sex-limited expression and the degree of intralocus sexual conflict. Future comparative and developmental work on sexual dimorphism within and among taxa will provide a better understanding of the biases and constraints governing the evolution of animal sexual dimorphism.
doi:10.1098/rspb.2010.2220
PMCID: PMC3107650  PMID: 21123259
Bicyclus; Junonia; phylogeny; Nymphalidae; stochastic character mapping
21.  A dataset comprising four micro-computed tomography scans of freshly fixed and museum earthworm specimens 
GigaScience  2014;3:6.
Background
Although molecular tools are increasingly employed to decipher invertebrate systematics, earthworm (Annelida: Clitellata: ‘Oligochaeta’) taxonomy is still largely based on conventional dissection, resulting in data that are mostly unsuitable for dissemination through online databases. In order to evaluate if micro-computed tomography (μCT) in combination with soft tissue staining techniques could be used to expand the existing set of tools available for studying internal and external structures of earthworms, μCT scans of freshly fixed and museum specimens were gathered.
Findings
Scout images revealed full penetration of tissues by the staining agent. The attained isotropic voxel resolutions permit identification of internal and external structures conventionally used in earthworm taxonomy. The μCT projection and reconstruction images have been deposited in the online data repository GigaDB and are publicly available for download.
Conclusions
The dataset presented here shows that earthworms constitute suitable candidates for μCT scanning in combination with soft tissue staining. Not only are the data comparable to results derived from traditional dissection techniques, but due to their digital nature the data also permit computer-based interactive exploration of earthworm morphology and anatomy. The approach pursued here can be applied to freshly fixed as well as museum specimens, which is of particular importance when considering the use of rare or valuable material. Finally, a number of aspects related to the deposition of digital morphological data are briefly discussed.
doi:10.1186/2047-217X-3-6
PMCID: PMC4023164  PMID: 24839546
MicroCT; Morphology; Anatomy; Taxonomy; Lumbricidae; Aporrectodea; μCT; Repository; Imaging
22.  Character displacement and the origins of diversity 
The American Naturalist  2010;176(Suppl 1):S26-S44.
In The Origin of Species, Darwin proposed his ‘principle of divergence of character’ (a process now termed ‘character displacement’) to explain how new species arise and why they differ from one other phenotypically. Darwin maintained that the origin of species, and the evolution of differences between them, is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin’s principle, specifically that: (1) competition promotes divergent trait evolution; (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors; (3) divergence can occur within species; and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how: (1) divergence can arise from selection acting to lessen reproductive interactions; (2) divergence is fueled by the intersection of character displacement and sexual selection; and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.
doi:10.1086/657056
PMCID: PMC3285564  PMID: 21043778
Competition; Darwin’s divergence of character; hybridization; phenotypic plasticity; sexual selection; speciation
23.  Evolution of microbes and viruses: a paradigm shift in evolutionary biology? 
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.
doi:10.3389/fcimb.2012.00119
PMCID: PMC3440604  PMID: 22993722
Darwin; modern synthesis; comparative genomics; tree of life; horizontal gene transfer
24.  The evolution of extreme altruism and inequality in insect societies 
In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual's life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.
doi:10.1098/rstb.2009.0129
PMCID: PMC2781879  PMID: 19805425
eusociality; worker policing; inclusive fitness theory; voluntary altruism; enforced altruism; acquiescence
25.  Systematic Identification and Evolutionary Analysis of Catalytically Versatile Cytochrome P450 Monooxygenase Families Enriched in Model Basidiomycete Fungi 
PLoS ONE  2014;9(1):e86683.
Genome sequencing of basidiomycetes, a group of fungi capable of degrading/mineralizing plant material, revealed the presence of numerous cytochrome P450 monooxygenases (P450s) in their genomes, with some exceptions. Considering the large repertoire of P450s found in fungi, it is difficult to identify P450s that play an important role in fungal metabolism and the adaptation of fungi to diverse ecological niches. In this study, we followed Sir Charles Darwin’s theory of natural selection to identify such P450s in model basidiomycete fungi showing a preference for different types of plant components degradation. Any P450 family comprising a large number of member P450s compared to other P450 families indicates its natural selection over other P450 families by its important role in fungal physiology. Genome-wide comparative P450 analysis in the basidiomycete species, Phanerochaete chrysosporium, Phanerochaete carnosa, Agaricus bisporus, Postia placenta, Ganoderma sp. and Serpula lacrymans, revealed enrichment of 11 P450 families (out of 68 P450 families), CYP63, CYP512, CYP5035, CYP5037, CYP5136, CYP5141, CYP5144, CYP5146, CYP5150, CYP5348 and CYP5359. Phylogenetic analysis of the P450 family showed species-specific alignment of P450s across the P450 families with the exception of P450s of Phanerochaete chrysosporium and Phanerochaete carnosa, suggesting paralogous evolution of P450s in model basidiomycetes. P450 gene-structure analysis revealed high conservation in the size of exons and the location of introns. P450s with the same gene structure were found tandemly arranged in the genomes of selected fungi. This clearly suggests that extensive gene duplications, particularly tandem gene duplications, led to the enrichment of selective P450 families in basidiomycetes. Functional analysis and gene expression profiling data suggest that members of the P450 families are catalytically versatile and possibly involved in fungal colonization of plant material. To our knowledge, this is the first report on the identification and comparative-evolutionary analysis of P450 families enriched in model basidiomycetes.
doi:10.1371/journal.pone.0086683
PMCID: PMC3899305  PMID: 24466198

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