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1.  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.
PMCID: PMC3632469  PMID: 23633139
2.  Charles Darwin's Reception in Germany and What Followed 
PLoS Biology  2009;7(7):e1000162.
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.
PMCID: PMC2709432
3.  Mitochondrial disorder caused Charles Darwin’s cyclic vomiting syndrome 
Charles Darwin (CD), “father of modern biology,” suffered from multisystem illness from early adulthood. The most disabling manifestation was cyclic vomiting syndrome (CVS). This study aims at finding the possible cause of CVS in CD.
A literature search using the PubMed database was carried out, and CD’s complaints, as reported in his personal writings and those of his relatives, friends, colleagues, biographers, were compared with various manifestations of mitochondrial disorders (MIDs), known to cause CVS, described in the literature.
Organ tissues involved in CD’s disease were brain, nerves, muscles, vestibular apparatus, heart, gut, and skin. Cerebral manifestations included episodic headache, visual disturbance, episodic memory loss, periodic paralysis, hysterical crying, panic attacks, and episodes of depression. Manifestations of polyneuropathy included numbness, paresthesias, increased sweating, temperature sensitivity, and arterial hypotension. Muscular manifestations included periods of exhaustion, easy fatigability, myalgia, and muscle twitching. Cardiac manifestations included episodes of palpitations and chest pain. Gastrointestinal manifestations were CVS, dental problems, abnormal seasickness, eructation, belching, and flatulence. Dermatological manifestations included painful lips, dermatitis, eczema, and facial edema. Treatments with beneficial effects to his complaints were rest, relaxation, heat, and hydrotherapy.
CVS in CD was most likely due to a multisystem, nonsyndromic MID. This diagnosis is based upon the multisystem nature of his disease, the fact that CVS is most frequently the manifestation of a MID, the family history, the variable phenotypic expression between affected family members, the fact that symptoms were triggered by stress, and that only few symptoms could not be explained by a MID.
PMCID: PMC3892961  PMID: 24453499
hyperemesis; cyclic vomiting; fatigue; metabolic disease; mitochondrial disorder; multisystem disorder; respiratory chain
4.  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.
PMCID: PMC2873000  PMID: 19571242
tree of life; lateral gene transfer; horizontal gene transfer; prokaryote genome evolution; phylogenetics
5.  Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin's 1871 prediction 
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.
PMCID: PMC2981960  PMID: 20855305
earliest hominids; central Africa; evolutionary grade; woodland origin
6.  Is Lamarckian evolution relevant to medicine? 
BMC Medical Genetics  2010;11:73.
200 years have now passed since Darwin was born and scientists around the world are celebrating this important anniversary of the birth of an evolutionary visionary. However, the theories of his colleague Lamarck are treated with considerably less acclaim. These theories centre on the tendency for complexity to increase in organisms over time and the direct transmission of phenotypic traits from parents to offspring.
Lamarckian concepts, long thought of no relevance to modern evolutionary theory, are enjoying a quiet resurgence with the increasing complexity of epigenetic theories of inheritance. There is evidence that epigenetic alterations, including DNA methylation and histone modifications, are transmitted transgenerationally, thus providing a potential mechanism for environmental influences to be passed from parents to offspring: Lamarckian evolution. Furthermore, evidence is accumulating that epigenetics plays an important role in many common medical conditions.
Epigenetics allows the peaceful co-existence of Darwinian and Lamarckian evolution. Further efforts should be exerted on studying the mechanisms by which this occurs so that public health measures can be undertaken to reverse or prevent epigenetic changes important in disease susceptibility. Perhaps in 2059 we will be celebrating the anniversary of both Darwin and Lamarck.
PMCID: PMC2876149  PMID: 20465829
7.  Formal Darwinism, the individual-as-maximizing-agent analogy and bet-hedging 
The central argument of The origin of species was that mechanical processes (inheritance of features and the differential reproduction they cause) can give rise to the appearance of design. The 'mechanical processes' are now mathematically represented by the dynamic systems of population genetics, and the appearance of design by optimization and game theory in which the individual plays the part of the maximizing agent. Establishing a precise individual-as-maximizing-agent (IMA) analogy for a population-genetics system justifies optimization approaches, and so provides a modern formal representation of the core of Darwinism. It is a hitherto unnoticed implication of recent population-genetics models that, contrary to a decades-long consensus, an IMA analogy can be found in models with stochastic environments (subject to a convexity assumption), in which individuals maximize expected reproductive value. The key is that the total reproductive value of a species must be considered as constant, so therefore reproductive value should always be calculated in relative terms. This result removes a major obstacle from the theoretical challenge to find a unifying framework which establishes the IMA analogy for all of Darwinian biology, including as special cases inclusive fitness, evolutionarily stable strategies, evolutionary life-history theory, age-structured models and sex ratio theory. This would provide a formal, mathematical justification of fruitful and widespread but 'intentional' terms in evolutionary biology, such as 'selfish', 'altruism' and 'conflict'.
PMCID: PMC1689909
8.  The Curious Case of Charles Darwin and Homeopathy 
In 1849, Charles Darwin was so ill that he was unable to work one out of every 3 days, and after having various troubling symptoms for 2–12 years, he wrote to a friend that he was ‘going the way of all flesh’. He sought treatment from Dr James Manby Gully, a medical doctor who used water cure and homeopathic medicines. Despite being highly skeptical of these treatments, he experienced a dramatic improvement in his health, though some of his digestive and skin symptoms returned various times in his life. He grew to appreciate water cure, but remained skeptical of homeopathy, even though his own experiments on insectivore plants using what can be described as homeopathic doses of ammonia salts surprised and shocked him with their significant biological effect. Darwin even expressed concern that he should publish these results. Two of Darwin's sons were as incredulous as he was, but their observations confirmed the results of his experiments. Darwin was also known to have read a book on evolution written by a homeopathic physician that Darwin described as similar to his own but ‘goes much deeper.’
PMCID: PMC2816387  PMID: 19875430
Charles Darwin; homeopathy; homeopathic; homeopath; James Manby Gully; hydrotherapy; water-cure; naturopathy; naturopathic medicine; history of medicine; history of science; extremely small doses; Drosera rotundifolia; Sir Charles Hastings; William Court Gully
9.  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
10.  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.
PMCID: PMC3440604  PMID: 22993722
Darwin; modern synthesis; comparative genomics; tree of life; horizontal gene transfer
11.  The ‘root-brain’ hypothesis of Charles and Francis Darwin 
Plant Signaling & Behavior  2009;4(12):1121-1127.
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.
PMCID: PMC2819436  PMID: 20514226
auxin; cognition; plant neurobiology; plant tropisms; roots; sensory biology; signaling
12.  Multilocus genotypes from Charles Darwin's finches: biodiversity lost since the voyage of the Beagle 
Genetic analysis of museum specimens offers a direct window into a past that can predate the loss of extinct forms. We genotyped 18 Galápagos finches collected by Charles Darwin and companions during the voyage of the Beagle in 1835, and 22 specimens collected in 1901. Our goals were to determine if significant genetic diversity has been lost since the Beagle voyage and to determine the genetic source of specimens for which the collection locale was not recorded. Using ‘ancient’ DNA techniques, we quantified variation at 14 autosomal microsatellite loci. Assignment tests showed several museum specimens genetically matched recently field-sampled birds from their island of origin. Some were misclassified or were difficult to classify. Darwin's exceptionally large ground finches (Geospiza magnirostris) from Floreana and San Cristóbal were genetically distinct from several other currently existing populations. Sharp-beaked ground finches (Geospiza difficilis) from Floreana and Isabela were also genetically distinct. These four populations are currently extinct, yet they were more genetically distinct from congeners than many other species of Darwin's finches are from each other. We conclude that a significant amount of the finch biodiversity observed and collected by Darwin has been lost since the voyage of the Beagle.
PMCID: PMC2830239  PMID: 20194164
ancient DNA; historical; microsatellite; NHC; population structure; SSR
13.  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.
PMCID: PMC2745620  PMID: 19633921
Darwin; Warm little pond; Origin of life; Spontaneous generation
14.  Charles Darwin (1758–1778) and the history of the early use of digitalis 
The evidence which I have just summarized establishes priority of publication concerning the action of digitalis for Erasmus Darwin, but on every other ground, Withering deserves full credit for the discovery. Charles Darwin, the medical student, had been informed of its action by his father and had attempted to account for it on the basis of improvement of lymphatic drainage. But the work, accomplished by the first Charles Darwin is less significant than the abundant evidence of his intellectual ability and precocity, and I have ventured to lay the details of his career before you because of their intrinsic interest and in the hope that the information will serve in a small way to clarify the unsolved problem of the relation of nature to nurture in establishing mental traits and capacities.
PMCID: PMC3456699  PMID: 10609600
15.  Earthworm genomes, genes and proteins: the (re)discovery of Darwin's worms 
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.
PMCID: PMC2664377  PMID: 19129111
Darwin; earthworms; evolution; genotypes; biogeography; transcriptomics
16.  The middle way of evolution 
This essay provides a critical review of two recent books on evolution: Richard Dawkins’ The Greatest Show on Earth, and Jerry Coyne’s Why Evolution is True, as well as a critique of mainstream evolutionary theory and of natural selection. I also suggest a generalization of sexual selection theory that acknowledges mind as pervasive in nature. Natural selection, as the primary theory of how biological change occurs, must be carefully framed to avoid the long-standing “tautology problem” and must also be modified to more explicitly include the role of mind in evolution. A propensity approach to natural selection, in which “expected fitness” is utilized rather than “fitness,” can save natural selection from tautology. But to be a productive theory, natural selection theory should be placed alongside sexual selection – which is explicitly agentic/intentional – as a twin force, but also placed alongside purely endogenous factors such as genetic drift. This framing is contrary to the normal convention that often groups all of these factors under the rubric of “natural selection.” I suggest some approaches for improving modern evolutionary theory, including a “generalized sexual selection,” a panpsychist extension of Darwin’s theory of sexual selection that explicitly recognizes the role of mind at all levels of nature and which may play the part of a general theory of evolution better than natural selection theory.
PMCID: PMC3502201  PMID: 23181154
Coyne; Dawkins; Whitehead; evolution; generalized agentic selection; generalized sexual selection; natural selection; panpsychism; sexual selection; tautology
17.  Comparative Evolutionary and Developmental Dynamics of the Cotton (Gossypium hirsutum) Fiber Transcriptome 
PLoS Genetics  2014;10(1):e1004073.
The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely one-half of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ∼5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution.
Author Summary
Ever since Darwin biologists have recognized that comparative study of crop plants and their wild relatives offers a powerful framework for generating insights into the mechanisms that underlie evolutionary change. Here, we study the domestication process in cotton, Gossypium hirsutum, an allopolyploid species (containing two different genomes) which initially was domesticated approximately 5000 years ago, and which primarily is grown for its single-celled seed fibers. Strong directional selection over the millennia was accompanied by transformation of the short, coarse, and brown fibers of wild plants into the long, strong, and fine white fibers of the modern cotton crop plant. To explore the evolutionary genetics of cotton domestication, we conducted transcriptome profiling of developing cotton fibers from multiple accessions of wild and domesticated cottons. Comparative analysis revealed that the domestication process dramatically rewired the transcriptome, affecting more than 5,000 genes, and with a more evenly balanced usage of the duplicated copies arising from genome doubling. We identify many different biological processes that were involved in this transformation, including those leading to a prolongation of fiber elongation and a reallocation of resources toward increased fiber growth in modern forms. The data provide a rich resource for future functional analyses targeting crop improvement and evolutionary objectives.
PMCID: PMC3879233  PMID: 24391525
18.  Aqueous Phase Separation as a Possible Route to Compartmentalization of Biological Molecules 
Accounts of Chemical Research  2012;45(12):2114-2124.
How could the incredible complexity of modern cells evolve from something simple enough to have appeared in a primordial soup? This enduring question has sparked the interest of researchers since Darwin first considered his theory of natural selection. Organic molecules, even potentially functional molecules including peptides and nucleotides, can be produced abiotically. Amphiphiles such as surfactants and lipids display remarkable self-assembly processes including the spontaneous formation of vesicles resembling the membranes of living cells. Nonetheless, numerous questions remain. Given the presumably dilute concentrations of macromolecules in the prebiotic pools where the earliest cells are thought to have appeared, how could the necessary components become concentrated and encapsulated within a semipermeable membrane? What would drive the further structural complexity that is a hallmark of modern living systems? The interior of modern cells is subdivided into microcompartments such as the nucleoid of bacteria or the organelles of eukaryotic cells. Even within what at first appears to be a single compartment, for example, the cytoplasm or nucleus, chemical composition is often nonuniform, containing gradients, macromolecular assemblies, and/or liquid droplets. What might the internal structure of intermediate evolutionary forms have looked like?
The nonideal aqueous solution chemistry of macromolecules offers an attractive possible answer to these questions. Aqueous polymer solutions will form multiple coexisting thermodynamic phases under a variety of readily accessible conditions. In this Account, we describe aqueous phase separation as a model system for biological compartmentalization in both early and modern cells, with an emphasis on systems that have been encapsulated within a lipid bilayer. We begin with an introduction to aqueous phase separation and discuss how this phenomenon can lead to microcompartmentalization and could facilitate biopolymer encapsulation by partitioning of solutes between the phases. We then describe primitive model cells based on phase separation inside lipid vesicles, which mimic several basic properties of biological cells: microcompartmentation, protein relocalization in response to stimulus, loss of symmetry, and asymmetric vesicle division. We observe these seemingly complex phenomena in the absence of genetic molecules, enzymes, or cellular machinery, and as a result these processes could provide clues to possible intermediates in the early evolution of cell-like assemblies.
PMCID: PMC3525015  PMID: 22330132
19.  Saving Darwin's muse: evolutionary genetics for the recovery of the Floreana mockingbird 
Biology Letters  2009;6(2):212-215.
The distribution of mockingbird species among the Galápagos Islands prompted Charles Darwin to question, for the first time in writing, the ‘stability of species’. Some 50 years after Darwin's visit, however, the endemic Floreana mockingbird (Mimus trifasciatus) had become extinct on Floreana Island and, today, only two small populations survive on two satellite islets. As Darwin noted, rarity often precedes extinction. To avert extinction, plans are being developed to reintroduce M. trifasciatus to Floreana. Here, we integrate evolutionary thinking and conservation practice using coalescent analyses and genetic data from contemporary and museum samples, including two collected by Darwin and Robert Fitzroy on Floreana in 1835. Our microsatellite results show substantial differentiation between the two extant populations, but our coalescence-based modelling does not indicate long, independent evolutionary histories. One of the populations is highly inbred, but both harbour unique alleles present on Floreana in 1835, suggesting that birds from both islets should be used to establish a single, mixed population on Floreana. Thus, Darwin's mockingbird specimens not only revealed to him a level of variation that suggested speciation following geographical isolation but also, more than 170 years later, return important information to their place of origin for the conservation of their conspecifics.
PMCID: PMC2865062  PMID: 19923141
museum specimens; genetic diversity; conservation; Galápagos; Nesomimus
20.  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.
PMCID: PMC2861690  PMID: 20442860
21.  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.
PMCID: PMC2653533  PMID: 19250550
22.  Darwin's Manufactory Hypothesis Is Confirmed and Predicts the Extinction Risk of Extant Birds 
PLoS ONE  2009;4(5):e5460.
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.
PMCID: PMC2674221  PMID: 19421332
23.  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
24.  Variation under domestication in plants: 1859 and today 
Charles Darwin began The Origin of Species with a chapter entitled variation under domestication, which encapsulated decades of his research on a diverse array of animal and plant domesticated species. Variation in these species compared with that in their wild relatives, their origins and their selection by humans, formed a paradigm for his theory of the evolutionary origin of species by means of natural selection. This chapter, its subsequent expansion into a two-volume monograph, together with the rediscovery of Mendel's laws, later became the foundation of scientific plant breeding. In the period up to the present, several advances in genetics (such as artificial mutation, polyploidy, adaptation and genetic markers) have amplified the discipline with concepts and questions, the seeds of which are in Darwin's original words. Today, we are witnessing a flowering of genomic research into the process of domestication itself, particularly the specific major and minor genes involved. In one striking way, our view of domestic diversity contrasts with that in Darwin's writing. He stressed the abundance of diversity and the diversifying power of artificial selection, whereas we are concerned about dwindling genetic diversity that attends modern agriculture and development. In this context, it is paramount to strive for a deeper understanding of how farmer selection including both deliberate selection and unconscious selection, might generate and retain diversity. This knowledge is essential for devising in situ conservation measures.
PMCID: PMC2935096  PMID: 20643742
crop diversity; genomics; landraces; farmer selection; mutual evolution
25.  Evolutionary Developmental Biology and Human Language Evolution: Constraints on Adaptation 
Evolutionary Biology  2012;39(4):613-637.
A tension has long existed between those biologists who emphasize the importance of adaptation by natural selection and those who highlight the role of phylogenetic and developmental constraints on organismal form and function. This contrast has been particularly noticeable in recent debates concerning the evolution of human language. Darwin himself acknowledged the existence and importance of both of these, and a long line of biologists have followed him in seeing, in the concept of “descent with modification”, a framework naturally able to incorporate both adaptation and constraint. Today, the integrated perspective of modern evolutionary developmental biology (“evo-devo”) allows a more subtle and pluralistic approach to these traditional questions, and has provided several examples where the traditional notion of “constraint” can be cashed out in specific, mechanistic terms. This integrated viewpoint is particularly relevant to the evolution of the multiple mechanisms underlying human language, because of the short time available for novel aspects of these mechanisms to evolve and be optimized. Comparative data indicate that many cognitive aspects of human language predate humans, suggesting that pre-adaptation and exaptation have played important roles in language evolution. Thus, substantial components of what many linguists call “Universal Grammar” predate language itself. However, at least some of these older mechanisms have been combined in ways that generate true novelty. I suggest that we can insightfully exploit major steps forward in our understanding of evolution and development, to gain a richer understanding of the principles that underlie human language evolution.
PMCID: PMC3514691  PMID: 23226905
Evo-devo; Language evolution; Adaptation; Exaptation; Constraints; Spandrel; Phenotypic plasticity

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