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When is an evolutionary approach useful?

Evidence that human behavior is or has been adaptive comes from the likelihood that it would have been useful in our environment of evolutionary adaptedness, that it forms a coherent whole with other characteristics, and that variants contribute or would be likely to contribute to reproductive success. Belsky et al. use the second and third of these, though on the third their evidence is somewhat tenuous. However, their thesis does integrate diverse facts about parenting and development. In general an evolutionary approach is useful if it integrates diverse facts, if it aids clinical practice, and if it helps us toward a full understanding of human nature.

Animals↗

The diversity and evolution of the T4-type bacteriophages.

Recent studies suggest that viruses are the most numerous entities in the biosphere; bacteriophages, the viruses that infect Eubacteria and Archaea, constitute a substantial fraction of this population. In spite of their ubiquity, the vast majority of phages in the environment have never been studied and nothing is known about them. For the last 10 years our research has focused on an extremely widespread group of phages, the T4-type. It has now become evident that phage T4 has a myriad of relatives in nature that differ significantly in their host range. The genomes of all these phages have homology to the T4 genes that determine virion morphology. Although phylogenetically related, these T4-type phages can be subdivided into four groups that are increasingly distant from T4: the T-evens, the pseudo T-evens, the schizo T-evens and the exo T-evens. Genomic comparisons between the various T4-type phages and T4 indicate that these genomes share homology not only for virion structural components but also for most of the essential genes involved in the T4 life cycle. This suggests that horizontal transmission of the genetic information may have played a less general role in the evolution of these phages than has been supposed. Nevertheless, we have identified several regions of the T4-type genome, such as the segment containing the tail fiber genes that exhibit evidence of extensive modular shuffling during evolution. The T4-type genomes appear to be a mosaic containing a large and fixed group of essential genes as well as highly variable set of non-essential genes. These non-essential genes are probably important for the adaptation of these phages to their particular life-style. Furthermore, swapping autonomous domains within the essential proteins may slightly modify their function(s) and contribute to the adaptive ability of the T4-type phage family. Regulatory sequences also display considerable evolutionary plasticity and this too may facilitate the adaptation of phage gene expression to new environments and stresses.

Bacteriophage T4↗

Immunology of viral-vector-mediated gene transfer into the brain: an evolutionary and developmental perspective.

The immune system imposes limitations on gene transfer into the brain. Viral vectors injected into the brain's ventricular system elicit innate and adaptive immune responses. However, when injected directly into the brain parenchyma, they elicit only transient inflammation owing to the absence of dendritic cells, which transport antigen to lymph nodes and present it to naive T cells to initiate adaptive immune responses. This article explores the evolutionary and developmental basis of brain immune responses and their implications for viral-vector-mediated neurological gene therapy. Elucidating the cellular and molecular basis of these differential reactions is essential to the long-term success of neurological gene therapy.

Animals↗

Toward an integration of interpersonal and biological processes: evolutionary psychiatry as an empirically testable framework for psychiatric research.

Phenomenological, biological, and interpersonal aspects of psychiatric disorders lack an integrative empirical framework. In this paper evolutionary psychiatry is proposed as a meta-theory to integrate biological and interpersonal aspects of psychopathology. Pathological cognition, emotions, and behaviors may be examined according to specific biosocial goals originally pursued to increase the individual's inclusive fitness, similar to the ways that "normal" processes have been analyzed by evolutionary psychology. Sex-specific differences in prevalence rates and symptomatology of psychiatric disorders may also be better understood if divergent problems of adaptation for men and women in human evolutionary history are taken into account. Instead of mistaking the evolutionary approach for being deterministic and empirically untestable, it may rather be appropriate to provide a functional classification which adds to the contemporary psychiatric nosology through analysis according to specific conflicts of adaptation (at the ultimate level), the pursuit of biosocial goals, and proximate specifiers such as genetic, developmental, and interpersonal causes of disorders.

Adaptation, Psychological↗

Mutations in filamentous bacteriophages spark eco-evolutionary feedbacks in Pseudomonas aeruginosa.

Microbial populations strongly shape their environment, which can re-route adaptation toward organism-generated fitness optima. However, the conditions that promote these eco-evolutionary feedbacks are unclear. Here, we used experimental evolution to test whether high population density, by strengthening niche construction, drives eco-evolutionary feedbacks in the bacterial pathogen Pseudomonas aeruginosa (Pa) MPAO1. We tested for adaptation to organism-modified environments by measuring the relative performance of ancestral and endpoint populations in filtrate generated by each evolutionary line sampled across generations. Contrary to expectations, we found that endpoint populations had higher performance than the ancestral strain in filtrate across nearly all evolutionary lines regardless of population density. This was caused by the emergence of hyperactive filamentous bacterio(phage) mutants during experimental passaging that inhibited the ancestral strain but not endpoint populations in modified media. Hyperactive phages emerged from one of two avirulent prophages in MPAO1's genome (Pf4 or Pf6). Hyperactive phages drove the evolution of phage resistance in bacterial populations via mutations in the type IV pilus (TIVP), the phage's binding receptor. In a follow-up experiment, we showed that these TIVP mutations pleiotropically reduced motility and conferred resistance to a TIVP-targeting virulent phage, both of which are important traits for Pa infection and treatment. Overall, this work suggests that filamentous phage evolution can drive eco-evolutionary feedbacks in bacterial populations, causing phenotypic and genetic changes that would not be anticipated from adaptation to the extrinsic environment alone.

Pseudomonas aeruginosa↗

Antibiotic resistance in the absence of selective pressure.

Antibiotic resistance poses a serious threat to modern medical practice making treatment more difficult and is associated with increased mortality among patients infected with resistant organisms. There is clear evidence that acquisition of resistance is associated with a decrease in the fitness of the organisms at least in the short term. Evidence from in vitro experiments indicates that bacteria have the ability to adapt to this deficit and recover fitness on serial passage. More recent results show that identical organisms isolated from patients in outbreaks have an initial deficit but that adaptation occurs in vivo. Strategies directed towards controlling resistance must move beyond wishful thinking that supposes that these organisms will disappear merely with control of prescribing. In some cases, resistance will not disappear because there is no evolutionary disadvantage in being resistant once adaptation has taken place. It is important, therefore, that we direct our efforts towards preventing primary resistance emerging and in limiting the spread of resistant strains. Ultimately, we must look again to new drug discovery to improve our therapeutic armoury.

Adaptation, Physiological↗

Evolution of specialized pyramidal neurons in primate visual and motor cortex.

The neocortex of primates contains several distinct neuron subtypes. Among these, Betz cells of primary motor cortex and Meynert cells of primary visual cortex are of particular interest for their potential role in specialized sensorimotor adaptations of primates. Betz cells are involved in setting muscle tone prior to fine motor output and Meynert cells participate in the processing of visual motion. We measured the soma volumes of Betz cells, Meynert cells, and adjacent infragranular pyramidal neurons in 23 species of primate and two species of non-primate mammal (Tupaia glis and Pteropus poliocephalus) using unbiased stereological techniques to examine their allometric scaling relationships and socioecological correlations. Results show that Betz somata become proportionally larger with increases in body weight, brain weight, and encephalization whereas Meynert somata remain a constant proportion larger than other visual pyramidal cells. Phylogenetic variance in the volumetric scaling of these neuronal subtypes might be related to species-specific adaptations. Enlargement of Meynert cells in terrestrial anthropoids living in open habitats, for example, might serve as an anatomical substrate for predator detection. Modification of the connectional and physiological properties of these neurons could constitute an important evolutionary mode for species-specific adaptation.

Aged↗

Using genome scans of DNA polymorphism to infer adaptive population divergence.

Elucidating the genetic basis of adaptive population divergence is a goal of central importance in evolutionary biology. In principle, it should be possible to identify chromosomal regions involved in adaptive divergence by screening genome-wide patterns of DNA polymorphism to detect the locus-specific signature of positive directional selection. In the case of spatially separated populations that inhabit different environments or sympatric populations that exploit different ecological niches, it is possible to identify loci that underlie divergently selected traits by comparing relative levels of differentiation among large numbers of unlinked markers. In this review I first address the question of whether diversifying selection on polygenic traits can be expected to produce predictable patterns of allelic variation at the underlying quantitative trait loci (QTL), and whether the locus-specific effects of selection can be reliably detected against the genome-wide backdrop of stochastic variability. I then review different approaches that have been developed to identify loci involved in adaptive population divergence and I discuss the relative merits of model-based approaches that rely on assumptions about population structure vs. model-free approaches that are based on empirical distributions of summary statistics. Finally, I consider the evolutionary and functional insights that might be gained by conducting genome scans for loci involved in adaptive population divergence.

Adaptation, Biological↗

Historical metabolic adaptation potentiates the rapid evolution of flonicamid resistance in Myzus persicae.

Rapid adaptation to novel environments is often shaped not only by newly acquired mutations but also by historical genetic backgrounds established through prior evolutionary events. However, the extent to which such historical contingency contributes to the rapid evolution of insecticide resistance remains poorly understood. Here, we investigated the emergence of resistance to flonicamid, a recently deployed insecticide, in the green peach aphid, Myzus persicae. We show that constitutive overexpression of the P450 enzymes CYP6CY3 and CYP6CY4, already widespread in populations of M. persicae before flonicamid deployment, confers a previously cryptic tolerance phenotype to flonicamid. However, biochemical and transgenic analyses demonstrated that these metabolic adaptations provide only weak protection against flonicamid. Following flonicamid deployment, however, a novel target-site mutation, NaamV251I, in the recently identified molecular target of 4-trifluoromethylnicotinamide (TFNA-AM), emerged in M. persicae on a genetic background of CYP6CY3 or CYP6CY4 overexpression. Structural modeling, enzymatic assays, and CRISPR-Cas9 genome editing demonstrated that this mutation reduces target sensitivity and independently confers moderate resistance. Strikingly, combining the nicotinamidase (Naam) mutation with pre-existing CYP6CY3 or CYP6CY4 overexpression produced substantially elevated resistance phenotypes that far exceeded the effects of either mechanism alone. Our results demonstrate that the pre-existing metabolic background did not itself evolve further following flonicamid deployment but fundamentally altered the phenotypic consequences of a subsequently acquired target-site mutation. These findings provide direct evidence that historical adaptive variation can potentiate rapid resistance evolution to newly introduced insecticides and reveal how interactions between past and contemporary adaptations shape evolutionary responses to novel environmental challenges.

Animals↗

Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature.

The involvement of heat-inducible genes, including the heat-shock genes, in the acute response to temperature stress is well established. However, their importance in genetic adaptation to long-term temperature stress is less clear. Here we use high-density arrays to examine changes in expression for 35 heat-inducible genes in three independent lines of Escherichia coli that evolved at high temperature (41.5 degrees C) for 2,000 generations. These lines exhibited significant changes in heat-inducible gene expression relative to their ancestor, including parallel changes in fkpA, gapA, and hslT. As a group, the heat-inducible genes were significantly more likely than noncandidate genes to have evolved changes in expression. Genes encoding molecular chaperones and ATP-dependent proteases, key components of the cytoplasmic stress response, exhibit relatively little expression change; whereas genes with periplasmic functions exhibit significant expression changes suggesting a key role for the extracytoplasmic stress response in the adaptation to high temperature. Following acclimation at 41.5 degrees C, two of the three lines exhibited significantly improved survival at 50 degrees C, indicating changes in inducible thermotolerance. Thus evolution at high temperature led to significant changes at the molecular level in heat-inducible gene expression and at the organismal level in inducible thermotolerance and fitness.

Adaptation, Physiological↗

Dikaryons of the basidiomycete fungus Schizophyllum commune: evolution in long-term culture.

The impact of ploidy on adaptation is a central issue in evolutionary biology. While many eukaryotic organisms exist as diploids, with two sets of gametic genomes residing in the same nucleus, most basidiomycete fungi exist as dikaryons in which the two genomes exist in separate nuclei that are physically paired and that divide in a coordinated manner during hyphal extension. To determine if haploid monokaryotic and dikaryotic mycelia adapt to novel environments under natural selection, we serially transferred replicate populations of each ploidy state on minimal medium for 18 months (approximately 13,000 generations). Dikaryotic mycelia responded to selection with increases in growth rate, while haploid monokaryotic mycelia did not. To determine if the haploid components of the dikaryon adapt reciprocally to one another's presence over time, we recovered the intact haploid components of dikaryotic mycelia at different time points (without meiosis) and mated them with nuclei of different evolutionary histories. We found evidence for coadaptation between nuclei in one dikaryotic line, in which a dominant deleterious mutation in one nucleus was followed by a compensatory mutation in the other nucleus; the mutant nuclei that evolved together had the best overall fitness. In other lines, nuclei had equal or higher fitness when paired with nuclei of other histories, indicating a heterozygote advantage. To determine if genetic exchange occurs between the two nuclei of a dikaryon, we developed a 24-locus genotyping system based on single nucleotide polymorphisms to monitor somatic exchange. We observed genetic exchange and recombination between the nuclei of several different dikaryons, resulting in genotypic variation in these mitotic cell lineages.

Base Sequence↗

Necessary and sufficient conditions for evolutionary suicide.

Evolutionary suicide is an evolutionary process where a viable population adapts in such a way that it can no longer persist. It has already been found that a discontinuous transition to extinction is a necessary condition for suicide. Here we present necessary and sufficient conditions, concerning the bifurcation point, for suicide to occur. Evolutionary suicide has been found in structured metapopulation models. Here we show that suicide can occur also in unstructured population models. Moreover, a structured model does not guarantee the possibility of suicide: we show that suicide cannot occur in age-structured population models of the Gurtin-MacCamy type. The point is that the mutant's fitness must explicitly depend not only on the environmental interaction variable, but also on the resident strategy.

Adaptation, Biological↗

r- and K-selection in experimental populations of vesicular stomatitis virus.

Here we explore the adaptation of vesicular stomatitis RNA virus to different population densities and the existence of a trade-off between r- and K-selection. Increasing population density represents a challenging special situation for viruses, since different selective pressures arise depending upon the number of available host cells per virus. Adaptation to low density represents a prototypical case of r-selection, where the optimal evolutionary solution should be a high replication rate. Adaptation to high density represents a case of K-selection. In this case, genotypes optimally exploiting the resources, instead of faster replicating ones, should be selected. Five independent populations were maintained in two environments, called r and K, for 100 generations. In the r environment, effective population size was small. In contrast, the effective population size in the K environment was large. Our results support the existence of the expected trade-offs between these two types of selections. Viral populations evolved at low density performed worse as population density increased. Similarly, viral populations evolved at high density showed reduced fitness at low density. Finally, we compare our results with those obtained for other RNA viruses.

Biological Evolution↗

Convergent evolution on the molecular level.

Divergence and convergence are two evolutionary processes by which organisms become adapted to their environments. With the advent of molecular biological techniques it is possible to ask if these processes are observed at the molecular level. There are many examples of molecular divergence in which molecular sequence or function change over evolutionary time. There are fewer reports of convergent evolution on the molecular level, and these claims are sometimes controversial. In this paper I discuss the types of convergent molecular evolution, describe the criteria for accepting or rejecting convergence, and give some examples relevant to neurobiology where convergence has been claimed. These include convergent evolution of opsins, gap junction proteins, neurotransmitter receptors, ion channels, and venoms directed against ion channels.

Animals↗

Divergent and stabilizing selection shape the phenotypic space of Arabidopsis thaliana.

Why do we observe some plant phenotypes but not others? The multivariate phenotypic space occupied by individuals or species often reveals both limits and phenotypes strikingly deviating from main syndromes. These observations are usually thought to indicate, respectively, inviable trait combinations and unique phenotypes adapted to specific environments. However, the evolutionary drivers underlying trait covariations often remain unclear. Here, we characterized the phenotypic space of Arabidopsis thaliana by comparing 713 wild accessions collected across the globe with 2,544 artificially-created recombinant individuals. This, combined with the detection of adaptive processes operating within species, allowed us to elucidate the roles of natural selection as a driver of phenotypic (co)variations within A. thaliana. We found that the phenotypic space of this species is constrained and driven by varying levels of divergent and stabilizing selection across different traits. Moreover, at the margins of the European geographic range, strong directional selection favored outlier phenotypes characterized by very late flowering and variation in a WRKY transcription factor gene. Genome analyses revealed that these extreme phenotypes may be explained by hybridization between ancestral and modern lineages of A. thaliana. Our findings demonstrate how interplays between population history and natural selection shape phenotypic diversity in a plant species.

Arabidopsis↗

Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses.

Maternal effects such as androgen in avian eggs can mediate evolutionary responses to selection, allowing manipulation of offspring phenotype and promoting trans-generational adaptive effects. We tested the predictions of two adaptive hypotheses that have been proposed to explain female variation in yolk androgen allocation in birds, using the barn swallow Hirundo rustica as a model. We found no support for the first hypothesis proposing that yolk androgen varies as a function of breeding density in order to prepare offspring for different breeding densities. However, we found experimental support for the hypothesis that female yolk androgen allocation depends on mate attractiveness and that it constitutes an example of differential allocation. Females increased the concentration of androgens in their eggs when mated to males with experimentally elongated tails. Female phenotypic quality as measured by arrival date and clutch size was positively related to egg androgen concentration, consistent with the hypothesis that this is a costly investment, constrained by female condition. We found correlative evidence of a direct relationship between egg androgen concentration and performance of offspring as measured by mass increase.

Adaptation, Physiological↗

Mechanism for the origin and the evolutionary significance of heterochronia.

Using material on the evolution of the fundus of the oral cavity in amphibians, four principles were established for the origin of heterochronia: efficiency of ontogenesis; adaptability of an earlier (than in ancestors) beginning for functioning of traits; loss of the adaptive significance of a trait at a previous stage, but a preservation of it at a subsequent stage; and, a prolongation of the adaptive significance of a trait at later stages. The origin of heterochronia is associated with changes in the succession of the functioning of genes, with reorganization of systems of morphogenetic correlations, and with change in the traits themselves that undergo heterochronia. The uniqueness of heterochronia as an adaptation consists of an increase in the evolutionary flexibility of specific stages of ontogenesis.

Age Factors↗

Evolutionary potential of an RNA virus.

RNA viruses are remarkably adaptable to changing environments. This is medically important because it enables pathogenic viruses to escape the immune response and chemotherapy and is of considerable theoretical interest since it allows the investigation of evolutionary processes within convenient time scales. A number of earlier studies have addressed the dynamics of adapting RNA virus populations. However, it has been difficult to monitor the trajectory of molecular changes in RNA genomes in response to selective pressures. To address the problem, we developed a novel in vitro evolution system based on a recombinant double-stranded RNA bacteriophage, phi 6, containing a beta-lactamase (bla) gene marker. Carrier-state bacterial cells are resistant to ampicillin, and after several passages, they become resistant to high concentrations of another beta-lactam antibiotic, cefotaxime, due to mutations in the virus-borne bla gene. We monitored the changes in bla cDNAs induced by cefotaxime selection and observed an initial explosion in sequence variants with multiple mutations throughout the gene. After four passages, a stable, homogeneous population of bla sequences containing three specific nonsynonymous mutations was established. Of these, two mutations (E104K and G238S) have been previously reported for beta-lactamases from cefotaxime-resistant bacterial isolates. These results extend our understanding of the molecular mechanisms of viral adaptation and also demonstrate the possibility of using an RNA virus as a vehicle for directed evolution of heterologous proteins.

Adaptation, Physiological↗