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What have two decades of laboratory life-history evolution studies on Drosophila melanogaster taught us?

A series of laboratory selection experiments on Drosophila melanogaster over the past two decades has provided insights into the specifics of life-history tradeoffs in the species and greatly refined our understanding of how ecology and genetics interact in life-history evolution. Much of what has been learnt from these studies about the subtlety of the microevolutionary process also has significant implications for experimental design and inference in organismal biology beyond life-history evolution, as well as for studies of evolution in the wild. Here we review work on the ecology and evolution of life-histories in laboratory populations of D. melanogaster, emphasizing how environmental effects on life-history-related traits can influence evolutionary change. We discuss life-history tradeoffs - many unexpected - revealed by selection experiments, and also highlight recent work that underscores the importance to life-history evolution of cross-generation and cross-life-stage effects and interactions, sexual antagonism and sexual dimorphism, population dynamics, and the possible role of biological clocks in timing life-history events. Finally, we discuss some of the limitations of typical selection experiments, and how these limitations might be transcended in the future by a combination of more elaborate and realistic selection experiments, developmental evolutionary biology, and the emerging discipline of phenomics.

Adaptation, Physiological↗

Detecting natural selection at the molecular level: a reexamination of some "classic" examples of adaptive evolution.

An important criterion used to detect adaptive evolution in DNA sequence data is omega(i) > 1, where omega(i) is the ratio of nonsynonymous to synonymous substitution rates in lineage i. However, the evaluation of multiple omega(i) within a phylogenetic tree can easily inflate the statistical type I error rate. We developed two rigorous methods of analysis that avoid this and other potential pitfalls. We applied these methods to four published examples of adaptive evolution. One case was strongly supported by our reanalysis (abalone sperm lysin), and one was weakly supported (baboon alpha-globin), but two examples (primate lysozyme and Antarctic fish beta-globin) did not show significant evidence of adaptive evolution. Our first method is a "bottom-up" hierarchical maximum likelihood approach, which (1) tests for significant heterogeneity in omega across the phylogeny, (2) locates its source using a sequence of planned comparisons, and (3) tests homogeneous groups of omega for omega > 1, using a modified level of significance that incorporates the pretesting. The second method is a "top-down" log-linear analysis based on estimates of nonsynonymous and synonymous substitutions in pairs of lineages. The log-linear test is applied to pairs of lineages joined at progressively deeper nodes. For each pair, the analysis simultaneously tests for adaptive evolution (omega > 1), a shift in natural selection (omega1 does not = omega2), and unequal evolution rate (the relative rate test). In both tests, we emphasized that the criterion omega1 not equal omega2 is an important additional indicator of a phylogenetic shift in the balance between natural selection and genetic drift between two related lineages.

Adaptation, Biological↗

Plasticity of fitness and diversification process during an experimental molecular evolution.

A simplified experimental evolution encompassing the essence of natural one was designed in an attempt to understand the involved mechanism. In our system, molecular evolution was observed through three serial cycles of consecutive random mutagenesis of the glutamine synthetase gene and chemostat culture of the transformed Escherichia coli cells containing the mutated genes. Selection pressure was imposed solely on the glutamine synthetase gene when varieties of mutant genes compete in an unstructured environment of the chemostat. The molecular phylogeny and population dynamics were deduced from the nucleotide sequences of the genes isolated from each of the chemostat runs. An initial mutant population in each cycle, comprised of diversified closely-related genes, ended up with several varieties of mutants in a state of coexistence. Competition between two mutant genes in the final population of the first cycle ascertained that the observed coexisting state is not an incidental event and that cellular interaction via environmental nutrients is a possible mechanism of coexistence. In addition, the mutant gene once extinct in the previous passage was found to have the capacity to reinvade and constitute the gene pool of the later cycle of molecular evolution. These results, including the kinetic characteristics of the purified wild-type and mutant glutamine synthetases in the phylogenetic tree, revealed that the enzyme activity had diverged, rather than optimized, to a fittest value during the course of evolution. Here, we proposed that the plasticity of gene fitness in consequence of cellular interaction via the environment is an essential mechanism governing molecular evolution.

Escherichia coli↗

Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi.

The evolution of multiple, independent and multispecific mating-type loci is a feature unique to homobasidiomycete fungi. To propose a model of evolution, data assembled for the wood-rotting fungus Schizophyllum commune were analyzed. In one mating-type locus, pheromone receptors and several pheromones are encoded which have been investigated in some detail and can be used to understand the ligand-receptor interactions and activation of signal transduction which are essential to sexual propagation. Previous models for the evolution of new alleles were complicated and involved three subsequent steps (without selectable phenotype) prior to the establishment of a new stable pheromone-receptor pair. This paper presents a model for the evolution of new specificities by recombination and selection that incorporates the multi-state receptor activation recently established for S. commune, explaining differential responses to different pheromones in one receptor molecule. The model takes into account the occurrence of multiple pheromone genes in each locus and unilateral nuclear donor/acceptor strains that may in nature act as steps in the evolution of new specificities. A second homobasidiomycete fungus, Coprinus cinereus, was similarly characterized at the molecular level. Data acquired in this system support the conclusion that the presented model can be generalized.

Basidiomycota↗

Variation and evolution of plant virus populations.

Over the last 15 years, interest in plant virus evolution has re-emerged, as shown by the increasing number of papers published on this subject. In recent times, research in plant virus evolution has been viewed from a molecular, rather than populational, standpoint, and there is a need for work aimed at understanding the processes involved in plant virus evolution. However, accumulated data from analyses of experimental and natural populations of plant viruses are beginning to delineate some trends that often run contrary to accepted opinion: (1) high mutation rates are not necessarily adaptive, as a large fraction of the mutations are deleterious or lethal; (2) in spite of high potential for genetic variation, populations of plant viruses are not highly variable, and genetic stability is the rule rather than the exception; (3) the degree of constriction of genetic variation in virus-encoded proteins is similar to that in their eukaryotic hosts and vectors; and (4) in spite of huge census sizes of plant virus populations, selection is not the sole factor that shapes their evolution, and genetic drift may be important. Here, we review recent advances in understanding plant virus evolution, and describe the experimental and analytical methods most suited to this purpose.

Biological Evolution↗

Adaptation, plant evolution, and the fossil record.

The importance of adaptation in determining patterns of evolution has become an important focus of debate in evolutionary biology. As it pertains to paleobotany, the issue is whether or not adaptive evolution mediated by natural selection is sufficient to explain the stratigraphic distributions of taxa and character states observed in the plant fossil record. One means of addressing this question is the functional evaluation of stratigraphic series of plant organs set in the context of paleoenvironmental change and temporal patterns of floral composition within environments. For certain organ systems, quantitative estimates of biophysical performance can be made on the basis of structures preserved in the fossil record. Performance estimates for plants separated in time or space can be compared directly. Implicit in different hypotheses of the forces that shape the evolutionary record (e.g. adaptation, mass extinction, rapid environmental change, chance) are predictions about stratigraphic and paleoenvironmental trends in the efficacy of functional performance. Existing data suggest that following the evolution of a significant structural innovation, adaptation for improved functional performance can be a major determinant of evolutionary changes in plants; however, there are structural and development limits to functional improvement, and once these are reached, the structure in question may no longer figure strongly in selection until and unless a new innovation evolves. The Silurian-Devonian paleobotanical record is consistent with the hypothesis that the succession of lowland floodplain dominants preserved in the fossil record of this interval was determined principally by the repeated evolution of new taxa that rose to ecological importance because of competitive advantages conferred by improved biophysical performance. This does not seem to be equally true for Carboniferous-Jurassic dominants of swamp and lowland floodplain environments. In these cases, environmental disruption appears to have been a major factor in shaping the fossil record. This does not mean that continuing adaptation was not important during this interval, but it may indicate that adaptive evolution was strongest in environments other than those best represented in the paleobotanical record.

Adaptation, Biological↗

Evolution of hepatitis delta virus RNA during chronic infection.

The complete RNA sequences of hepatitis delta virus (HDV) isolated at three different time points from a chronic delta hepatitis patient were determined. These time points represented three different periods of clinical flare-ups. The sequence analysis showed that these three different HDV isolates evolved at a rate ranging from 3.0 x 10(-2) to 3.0 x 10(-3) substitutions/nucleotide/year, depending on the period of infection. The evolution rates appeared to correlate with the changes of clinical pictures of hepatitis, i.e., the more drastic the change in the symptom of hepatitis was, the more nucleotide changes were detected. Except during the transition from the acute phase to chronic phase of delta hepatitis, when there was a much larger number of changes in HDV RNA sequence, the overall evolution rate of HDV RNA in the chronic phase appeared to be similar to those of other RNA viruses. Sequence relationship of these HDV RNAs suggested that acute exacerbations in chronic delta hepatitis were associated with the evolution of the persistently infected HDV, rather than resulting from new viral infections. However, some of the mutations were not cumulative, suggesting that HDV isolated at a later time was not directly evolved from the immediately previous one. Thus, HDV at any time point was a mixture of viruses with slight sequence variations, and a specific HDV RNA species was selected from this virus population under different environments. These findings indicate that HDV RNA is heterogeneous and evolves at a fast rate. The evolution rates in different parts of HDV RNA also varied. The evolution rate of HDV RNA determined here was higher than the ones determined previously from partial RNA sequences of two Japanese HDV isolates.

Adult↗

The measure-unit of evolution.

A theoretical study on evolution has been carried out, with the aim of disproving some value judgements essentially represented by the idea that the degree of evolution can increase. Our conclusions are based upon the preliminary statement that efficiency of survival is directly related to regulative ability. On this ground our reasoning led us to conclude that: (i) actual fitness measure units derive from an anthropocentric bias, and they mainly evaluate similarity to man rather than some objective parameter; (ii) a complete and meaningful unit is, at present, impossible to achieve in practice; (iii) since the study of evolution is only descriptive, and since the evolutionary process is time dependent, every ecological dominant living today must be considered as the most fitted to its environment; (iv) the view we can have of evolution is simply a transection, so that many generalized phyletic trees are trivial and it is impossible to claim the persistence today of those "ancestor organisms" upon which such trees are constructed. Moreover, a functional definition of the term "organism" is given, following criteria drawn from bioenergetics and from biological hierarchization. The concluding step is the assemblage of a slightly heterodox model for evolution.

Base Sequence↗

Cancer: re-evolution of eucaryotic to procaryotic replication units--a result of genetic transposition?

We have consistently tried to present our "procaryote-hypothesis" of oncogenesis in the light of evolution. It is suggested that the replication units are the essential starting points of oncogenesis, and cancer is the result of a short and compact re-evolution from eucaryotic to procaryotic replicons. In our view, the process of re-evolution or reactivation of procaryotic replication units and/or their precursors starts with the activity of a cancerogen and proceeds by genetic rearrangements, possibly by genetic transposition. Consequently, some remarks had to be made on: (a) the evolution of self-replicative species; (b) the evolvement of procaryotes to eucaryotes; and (c) the various mobile repeated genetic elements. Moreover, we have taken into consideration the important fact that most of the mammalian genome is reversibly repressed and "that there is in these modern genes still a memory of ancient sequences" ( Eigen et al., 1981). We can only speculate on the extent of the evolutionary conservation, particularly of certain ancient nucleotide sequences related to autonomous, indefinite self-replication. Nevertheless, no real argument can be made against the simple possibility that a re-evolution of eucaryotic to procaryotic replicons lead to cancer.

Animals↗

The evolution of calcium biochemistry.

The role of calcium in evolution is best understood from a perspective based on its intrinsic value as a divalent cation able to bind and precipitate inorganic and organic anions rapidly. This binding can be useful or inhibitory. Now treatment of binding or precipitation has two different interests in biological cells. The first is thermodynamic, that is the stress is on systems biology and the second is structure, that is molecular biology. In evolution both have equal weight being connected through exchange. This paper outlines first the systems biology of the evolution of calcium functions from prokaryotes to animals with brains. The calcium ion was the only good available candidate in the environment for the functions it performs. The second section of the paper describes the evolution of the proteins which allow the messenger function. We have discussed elsewhere the structure/function relationships of the proteins. Overall the evolving and increasing involvement of calcium as possibly the major control messenger of events outside cells to action inside them is an inevitable feature of the nature of ecological, that is environmental/organism, evolution.

Animals↗

Directed evolution of biocatalytic processes.

The benefits of applying biocatalysts to organic synthesis, such as their high chemo-, regio-, and enantio-specificity and selectivity, must be seriously considered, especially where chemical routes are unavailable, complex or prohibitively expensive. In cases where a potential biocatalytic route is not yet efficient enough to compete with chemical synthesis, directed evolution, and/or process engineering could be implemented for improvements. While directed evolution has demonstrated great potential to enhance enzyme properties, there will always be some aspects of biocatalytic processes that it does not address. Even where it can be successfully applied, the resources required for its implementation must currently be weighed against the feasibility of, and resources available for developing a chemical synthesis route. Here, we review the potential of combining directed evolution with process engineering, and recent developments to improve their implementation. Favourable targets for the directed evolution of new biocatalysts are the syntheses of highly complex molecules, especially where chemistry, metabolic engineering or recombineering provide a partial solution. We also review some of the recent advances in the application of these approaches alongside the directed evolution of biocatalysts.

Animals↗

A stochastic gene evolution model with time dependent mutations.

We develop here a new class of gene evolution models in which the nucleotide mutations are time dependent. These models allow to study nonlinear gene evolution by accelerating or decelerating the mutation rates at different evolutionary times. They generalize the previous ones which are based on constant mutation rates. The stochastic model developed in this class determines at some time t the occurrence probabilities of trinucleotides mutating according to 3 time dependent substitution parameters associated with the 3 trinucleotide sites. Therefore, it allows to simulate the evolution of the circular code recently observed in genes. By varying the class of function for the substitution parameters, 1 among 12 models retrieves after mutation the statistical properties of the observed circular code in the 3 frames of actual genes. In this model, the mutation rate in the 3rd trinucleotide site increases during gene evolution while the mutation rates in the 1st and 2nd sites decrease. This property agrees with the actual degeneracy of the genetic code. This approach can easily be generalized to study evolution of motifs of various lengths, e.g., dicodons, etc., with time dependent mutations.

Codon↗

The biology and evolution of music: a comparative perspective.

Studies of the biology of music (as of language) are highly interdisciplinary and demand the integration of diverse strands of evidence. In this paper, I present a comparative perspective on the biology and evolution of music, stressing the value of comparisons both with human language, and with those animal communication systems traditionally termed "song". A comparison of the "design features" of music with those of language reveals substantial overlap, along with some important differences. Most of these differences appear to stem from semantic, rather than structural, factors, suggesting a shared formal core of music and language. I next review various animal communication systems that appear related to human music, either by analogy (bird and whale "song") or potential homology (great ape bimanual drumming). A crucial comparative distinction is between learned, complex signals (like language, music and birdsong) and unlearned signals (like laughter, ape calls, or bird calls). While human vocalizations clearly build upon an acoustic and emotional foundation shared with other primates and mammals, vocal learning has evolved independently in our species since our divergence with chimpanzees. The convergent evolution of vocal learning in other species offers a powerful window into psychological and neural constraints influencing the evolution of complex signaling systems (including both song and speech), while ape drumming presents a fascinating potential homology with human instrumental music. I next discuss the archeological data relevant to music evolution, concluding on the basis of prehistoric bone flutes that instrumental music is at least 40,000 years old, and perhaps much older. I end with a brief review of adaptive functions proposed for music, concluding that no one selective force (e.g., sexual selection) is adequate to explaining all aspects of human music. I suggest that questions about the past function of music are unlikely to be answered definitively and are thus a poor choice as a research focus for biomusicology. In contrast, a comparative approach to music promises rich dividends for our future understanding of the biology and evolution of music.

Animal Communication↗

Evolutionary systems biology: links between gene evolution and function.

The recent accumulation of genome-wide data on various facets of gene expression, function and evolution stimulated the emergence of a new field, evolutionary systems biology. Many significant correlations were detected between variables that characterize the functioning of a gene, such as expression level, knockout effect, connectivity of genetic and protein-protein interaction networks, and variables that describe gene evolution, such as sequence evolution rate and propensity for gene loss. The first attempts on multidimensional analysis of genomic data yielded composite variables that describe the 'status' of a gene in the genomic community. However, it remains uncertain whether different functional variables affect gene evolution synergistically or there is a single, dominant factor. The number of translation events, linked to selection for translational robustness, was proposed as a candidate for such a major determinant of protein evolution. These developments show that, although the methodological basis of evolutionary systems biology is not yet fully solidified, this area of research is already starting to yield fundamental biological insights.

Evolution, Molecular↗

Protein evolution in viral quasispecies under selective pressure: a thermodynamic and phylogenetic analysis.

The evolution of RNA viruses under antiviral pressure is characterized by high mutation rates and strong selective forces that induce extremely rapid changes of protein sequences. This makes the course of molecular evolution directly observable on time scales of months. Here we study the interplay between selection for drug resistance and selection for thermodynamic stability in the protease (PR) and the reverse transcriptase (RT) of human immunodeficiency virus type 1 (HIV-1) clones extracted from two patients with complex treatment histories. This analysis shows that folding thermodynamic properties may fluctuate very strongly in the course of quasispecies evolution under selective pressure. For the first case, our data suggest that folding efficiency of the RT is sacrificed at the advantage of drug resistance, while the corresponding PR seems to undergo selection for thermodynamic stability in the absence of substitutions associated to resistance. The PR of the second case is not submitted to antiviral pressure during the period analyzed and seems to initiate random fluctuations that lead to the accidental increase of its folding efficiency. In summary, joint consideration of sequence evolution and thermodynamic parameters can represent a more comprehensive approach for the study of the evolution of RNA viruses.

Anti-HIV Agents↗

Adaptive evolution of MRGX2, a human sensory neuron specific gene involved in nociception.

MRGX2, a G-protein-coupled receptor, is specifically expressed in the sensory neurons of the human peripheral nervous system and involved in nociception. Here, we studied DNA polymorphism patterns and evolution of the MRGX2 gene in world-wide human populations and the representative nonhuman primate species. Our results demonstrated that MRGX2 had undergone adaptive changes in the path of human evolution, which were likely caused by Darwinian positive selection. The patterns of DNA sequence polymorphisms in human populations showed an excess of derived substitutions, which against the expectation of neutral evolution, implying that the adaptive evolution of MRGX2 in humans was a relatively recent event. The reconstructed secondary structure of the human MRGX2 revealed that three of the four human-specific amino acid substitutions were located in the extra-cellular domains. Such critical substitutions may alter the interactions between MRGX2 protein and its ligand, thus, potentially led to adaptive changes of the pain-perception-related nervous system during human evolution.

Adaptation, Physiological↗

Ancient evolution of stress-regulating peptides in vertebrates.

Recent studies on genomic sequences have led to the discovery of novel corticotropin-releasing factor (CRF) type 2 receptor-selective agonists, stresscopin (SCP)/urocortin III (UcnIII), and stresscopin-related peptide (SRP)/urocortin II (UcnII). In addition, analyses of vertebrate genomes showed that the CRF peptide family includes four distinct genes, CRF, urocortin/urotensin I, SCP/UcnIII, and SRP/UcnII. Each of these four genes is highly conserved during evolution and the identity between mammalian and teleost orthologs ranges from >96% for CRF to >55% for SCP. Phylogenetic studies showed that the origin of each of these peptides predates the evolution of tetrapods and teleosts, and that this family of peptide hormones evolved from an ancestor gene that developed the CRF/urocortin and SCP/SRP branches through an early gene duplication event. These two ancestral branches then gave rise to additional paralogs through a second round of gene duplication. Consequently, each of these peptides participates in the regulation of stress responses over the 550 million years of vertebrate evolution. The study also suggested that the fight-or-flight and stress-coping responses mediated mainly by CRF types 1 and 2 receptors evolved early in chordate evolution. In addition, we hypothesize that the CRF/CRF receptor signaling evolved from the same ancestors that also gave rise to the diuretic hormone/diuretic hormone receptors in insects. Thus, a complete inventory of CRF family ligands and their receptors in the genomes of different organisms provides an opportunity to reveal an integrated view of the physiology and pathophysiology of the CRF/SCP family peptides, and offers new insights into the evolution of stress regulation in vertebrates.

Amino Acid Sequence↗

Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives.

The sequencing of a wide variety of genomes and their transcripts has allowed researchers to determine how proteins or protein families evolved and how strongly during evolution a protein has been conserved. In this report, we analyze the evolution of the Class 2 ligands and their cognate receptors by analyzing Class 2 ligand and receptor chain gene sequences from a variety of DNA sequence databases. Both the Class 2 cytokines and receptor chains appear to have developed during the evolution of the chordate phyla: distant homologues of type I interferon (IFN) receptors are the only Class 2 cytokine receptors identified in the Ciona genomes, while a wide variety of Class 2 ligands and receptor chains are encoded in the currently available genomes of bony vertebrates (teleost fish, amphibians, reptiles, birds, mammals). Phylogenetic trees of ligands and ligand-binding receptor chains demonstrate that proteins involved in conferring antiviral activity diverged before those involved in adaptive immunity. Genes encoding IFNs and IFN receptors duplicated multiple times during chordate evolution, suggesting that duplication of genes encoding IFN activity conveyed an evolutionary advantage. Altogether, these data support a model whereby the original Class 2 cytokines and receptors evolved and duplicated during the evolution of the chordate innate immune response system; new receptor and ligand duplications evolved into signaling molecules to fulfill communication requirements of a highly specialized and differentiated vertebrate immune system. In addition, the genomic analysis led to the discovery of some new members of this family.

Amino Acid Sequence↗