Rapid Adaptive Evolution of the Tumor Suppressor Gene Pten in an Insect Lineage

The Pten gene was initially identified in humans as a tumor suppressor. It has since been shown to play important roles in the control of cell size, cell motility, apoptosis, and organ size, and it has also been implicated in aging. Pten is highly conserved among organisms as diverse as nematodes, insects, and vertebrates. In contrast, a phylogenetic analysis by maximum likelihood of a 133-amino acid region showed an average nonsynonymous-to-synonymous rate ratio of 10.4 for Pten in the lineage leading to parasitoid wasps of the Nasonia genus, indicating very strong positive selection. A previous study identified Pten as a potential QTL candidate gene for differences in male wing size in Nasonia. Most of the amino acid replacements that occurred in the Nasonia lineage cluster in a small region of the protein surface, suggesting that they might be involved in an interaction between Pten and another protein. The phenotypic changes due to Pten are not yet known, although it is not associated with known differences in male wing size. Introgression of Pten from one species to another does affect longevity, but a causal relationship is not established. [Reviewing Editor: Dr. Willie J. Swanson]     

Commercial Harvesting Has Driven the Evolution of Camouflage in an Alpine Plant

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Adaptation to Host-Specific Bacterial Pathogens Drives Rapid Evolution of a Human Innate Immune Receptor

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Ex Uno Plures: Clonal Reinforcement Drives Evolution of a Simple Microbial Community

A major goal of genetics is to define the relationship between phenotype and genotype, while a major goal of ecology is to identify the rules that govern community assembly. Achieving these goals by analyzing natural systems can be difficult, as selective pressures create dynamic fitness landscapes that vary in both space and time. Laboratory experimental evolution offers the benefit of controlling variables that shape fitness landscapes, helping to achieve both goals. We previously showed that a clonal population of E. coli experimentally evolved under continuous glucose limitation gives rise to a genetically diverse community consisting of one clone, CV103, that best scavenges but incompletely utilizes the limiting resource, and others, CV101 and CV116, that consume its overflow metabolites. Because this community can be disassembled and reassembled, and involves cooperative interactions that are stable over time, its genetic diversity is sustained by clonal reinforcement rather than by clonal interference. To understand the genetic factors that produce this outcome, and to illuminate the community''s underlying physiology, we sequenced the genomes of ancestral and evolved clones. We identified ancestral mutations in intermediary metabolism that may have predisposed the evolution of metabolic interdependence. Phylogenetic reconstruction indicates that the lineages that gave rise to this community diverged early, as CV103 shares only one Single Nucleotide Polymorphism with the other evolved clones. Underlying CV103''s phenotype we identified a set of mutations that likely enhance glucose scavenging and maintain redox balance, but may do so at the expense of carbon excreted in overflow metabolites. Because these overflow metabolites serve as growth substrates that are differentially accessible to the other community members, and because the scavenging lineage shares only one SNP with these other clones, we conclude that this lineage likely served as an “engine” generating diversity by creating new metabolic niches, but not the occupants themselves.     

Modeling the Evolution of Insect Phenology

Climate change is likely to disrupt the timing of developmental events (phenology) in insect populations in which development time is largely determined by temperature. Shifting phenology puts insects at risk of being exposed to seasonal weather extremes during sensitive life stages and losing synchrony with biotic resources. Additionally, warming may result in loss of developmental synchronization within a population making it difficult to find mates or mount mass attacks against well-defended resources at low population densities. It is unknown whether genetic evolution of development time can occur rapidly enough to moderate these effects. We present a novel approach to modeling the evolution of phenology by allowing the parameters of a phenology model to evolve in response to selection on emergence time and density. We use the Laplace method to find asymptotic approximations for the temporal variation in mean phenotype and phenotypic variance arising in the evolution model that are used to characterize invariant distributions of the model under periodic temperatures at leading order. At these steady distributions the mean phenotype allows for parents and offspring to be oviposited at the same time of year in consecutive years. Numerical simulations show that populations evolve to these steady distributions under periodic temperatures. We consider an example of how the evolution model predicts populations will evolve in response to warming temperatures and shifting resource phenology.     

TRIM5 alpha Drives SIVsmm Evolution in Rhesus Macaques

The antagonistic interaction with host restriction proteins is a major driver of evolutionary change for viruses. We previously reported that polymorphisms of the TRIM5α B30.2/SPRY domain impacted the level of SIVsmm viremia in rhesus macaques. Viremia in macaques homozygous for the non-restrictive TRIM5α allele TRIM5^Q was significantly higher than in macaques expressing two restrictive TRIM5alpha alleles TRIM5^TFP/TFP or TRIM5^Cyp/TFP. Using this model, we observed that despite an early impact on viremia, SIVsmm overcame TRIM5α restriction at later stages of infection and that increasing viremia was associated with specific amino acid substitutions in capsid. Two amino acid substitutions (P37S and R98S) in the capsid region were associated with escape from TRIM5^TFP restriction and substitutions in the CypA binding-loop (GPLPA87-91) in capsid were associated with escape from TRIM5^Cyp. Introduction of these mutations into the original SIVsmE543 clone not only resulted in escape from TRIM5α restriction in vitro but the P37S and R98S substitutions improved virus fitness in macaques with homozygous restrictive TRIM^TFP alleles in vivo. Similar substitutions were observed in other SIVsmm strains following transmission and passage in macaques, collectively providing direct evidence that TRIM5α exerts selective pressure on the cross-species transmission of SIV in primates.     

Wildlife Recovery During Tropical Forest Succession: Assessing Ecological Drivers of Community Change

Despite the high proportion of secondary forests in the tropics, their conservation value remains poorly understood, particularly with regard to animals. Most theoretical studies of succession have focused on plants, linking life history trade‐offs to well‐known patterns of community change. However, the same trade‐offs proposed for plants should apply to animals, and indeed, animal studies show a change in community dominance from habitat generalist to forest specialist species during succession. Focusing on the diverse terrestrial small mammals of the endangered Atlantic Forest, we assessed which ecological drivers (habitat structure and food availability) affect community changes during succession. If the change in community dominance is driven by trade‐offs between productivity and efficiency, it should be mainly associated with a decrease in food availability. As expected, from younger to older forest, habitat generalists decreased in richness and total abundance, concurrent with a decrease in arthropod biomass. By contrast, the increase in richness and total abundance of forest specialists was not clearly supported by the data; however, this group was not affected by food availability. These results are congruent with a trade‐off between competitive ability and ability to use abundant resources, and indicate that the major community change during succession involves habitat generalists. Secondary forests may thus be valuable for conservation, at least where habitat loss and fragmentation are not high, and old growth forest is available.     

Osmotic Challenge Drives Rapid and Reversible Chromatin Condensation in Chondrocytes

Changes in extracellular osmolality have been shown to alter gene expression patterns and metabolic activity of various cell types, including chondrocytes. However, mechanisms by which physiological or pathological changes in osmolality impact chondrocyte function remain unclear. Here we use quantitative image analysis, electron microscopy, and a DNase I assay to show that hyperosmotic conditions (>400 mOsm/kg) induce chromatin condensation, while hypoosmotic conditions (100 mOsm/kg) cause decondensation. Large density changes (p < 0.001) occur over a very narrow range of physiological osmolalities, which suggests that chondrocytes likely experience chromatin condensation and decondensation during a daily loading cycle. The effect of changes in osmolality on nuclear morphology (p < 0.01) and chromatin condensation (p < 0.001) also differed between chondrocytes in monolayer culture and three-dimensional agarose, suggesting a role for cell adhesion. The relationship between condensation and osmolality was accurately modeled by a polymer gel model which, along with the rapid nature of the chromatin condensation (<20 s), reveals the basic physicochemical nature of the process. Alterations in chromatin structure are expected to influence gene expression and thereby regulate chondrocyte activity in response to osmotic changes.     

Strong Positive Selection Drives Rapid Diversification of R-Genes in Arabidopsis Relatives

Although plant resistance (R) genes are extremely diverse and evolve rapidly, little is known about the mechanisms that generate this sequence divergence. To investigate these forces, we compared all nucleotide binding sites and leucine-rich repeat R-genes between two closely related species, Arabidopsis thaliana and Arabidopsis lyrata. Our analyses revealed two distinct evolutionary patterns driven by either positive or stabilizing selection. Most R-genes (>50%) were evolving under strong positive selection characterized by high Ka/Ks ratios (>1), frequent recombination, copy number variation, and extremely high sequence divergence between the two species. The stably selected R-genes (<30%) have exactly the opposite four characters as the positively selected genes. The remaining R-genes (about 20%) are present in only one genome and absent from the other. A higher proportion of such genes were found to be part of TNL class (23.5%) compared to the non-TNL class (5.6%), suggesting different evolutionary patterns between these two groups. A significant correlation between Ka and divergence was revealed, indicating that the rapid evolution and diversification of R-genes were initiated by selectively generated, frequently shuffled and selectively maintained non-synonymous substitutions. Our genome-wide analyses confirmed an amazing mechanism by which plants to selectively accumulate and efficiently exploit these non-synonymous substitutions for their resistance to various pathogens.     

Partner Choice Drives the Evolution of Cooperation via Indirect Reciprocity

Indirect reciprocity potentially provides an important means for generating cooperation based on helping those who help others. However, the use of ‘image scores’ to summarize individuals’ past behaviour presents a dilemma: individuals withholding help from those of low image score harm their own reputation, yet giving to defectors erodes cooperation. Explaining how indirect reciprocity could evolve has therefore remained problematic. In all previous treatments of indirect reciprocity, individuals are assigned potential recipients and decide whether to cooperate or defect based on their reputation. A second way of achieving discrimination is through partner choice, which should enable individuals to avoid defectors. Here, I develop a model in which individuals choose to donate to anyone within their group, or to none. Whereas image scoring with random pairing produces cycles of cooperation and defection, with partner choice there is almost maximal cooperation. In contrast to image scoring with random pairing, partner choice results in almost perfect contingency, producing the correlation between giving and receiving required for cooperation. In this way, partner choice facilitates much higher and more stable levels of cooperation through image scoring than previously reported and provides a simple mechanism through which systems of helping those who help others can work.     

Rapid Recovery of an Urban Remnant Reptile Community following Summer Wildfire

Reptiles in urban remnants are threatened with extinction by increased fire frequency, habitat fragmentation caused by urban development, and competition and predation from exotic species. Understanding how urban reptiles respond to and recover from such disturbances is key to their conservation. We monitored the recovery of an urban reptile community for five years following a summer wildfire at Kings Park in Perth, Western Australia, using pitfall trapping at five burnt and five unburnt sites. The reptile community recovered rapidly following the fire. Unburnt sites initially had higher species richness and total abundance, but burnt sites rapidly converged, recording a similar total abundance to unburnt areas within two years, and a similar richness within three years. The leaf-litter inhabiting skink Hemiergis quadrilineata was strongly associated with longer unburnt sites and may be responding to the loss of leaf litter following the fire. Six rarely-captured species were also strongly associated with unburnt areas and were rarely or never recorded at burnt sites, whereas two other rarely-captured species were associated with burnt sites. We also found that one lizard species, Ctenotus fallens, had a smaller average body length in burnt sites compared to unburnt sites for four out of the five years of monitoring. Our study indicates that fire management that homogenises large areas of habitat through frequent burning may threaten some species due to their preference for longer unburnt habitat. Careful management of fire may be needed to maximise habitat suitability within the urban landscape.