Viruses are the simplest replicating units, characterized by a limited number of coding genes and an exceptionally high rate of overlapping genes. We sought a unified explanation for the evolutionary constraints that govern genome sizes, gene overlapping and capsid properties. We performed an unbiased statistical analysis over the ~100 known viral families, and came to refute widespread assumptions regarding viral evolution. We found that the volume utilization of viral capsids is often low, and greatly varies among families. Most notably, we show that the total amount of gene overlapping is tightly bounded. Although viruses expand three orders of magnitude in genome length, their absolute amount of gene overlapping almost never exceeds 1500 nucleotides, and mostly confined to <4 significant overlapping instances. Our results argue against the common theory by which gene overlapping is driven by a necessity of viruses to compress their genome. Instead, we support the notion that overlapping has a role in gene novelty and evolution exploration.

The origin of the germline-soma distinction in metazoans is a fundamental unsolved question. Somatic gametogenesis in sessile sponges and corals contrasts starkly with early germline sequestration in bilaterians with higher energy requirements, elaborate body plans and fast evolution of small mitochondrial genomes. We develop an evolutionary model to investigate whether selection for mitochondrial quality can drive germline evolution. In basal metazoans with low mutation rates, somatic gametogenesis optimizes gamete quality through segregation of mitochondrial mutations in multiple cell divisions. The need to maintain mitochondrial quality in somatic tissues explains the evolution of oogamy and male-female gamete specialization. Higher mitochondrial mutation rates promote early sequestration of a dedicated germline, permitting complex developmental processes. Rising oxygen drove germline evolution in motile bilaterians, igniting the Cambrian explosion.

1) Micro-evolutionary predictions are complicated by ecological feedbacks like density dependence, while ecological predictions can be complicated by evolutionary change. A widely used approach in micro-evolution, quantitative genetics, struggles to incorporate ecological processes into predictive models, while structured population modelling, a tool widely used in ecology, rarely incorporates evolution explicitly. 2) In this paper we develop a flexible, general framework that links quantitative genetics and structured population models. We use the quantitative genetic approach to write down the phenotype as an additive map. We then construct integral projection models for each component of the phenotype. The dynamics of the distribution of the phenotype are generated by combining distributions of each of its components. Population projection models can be formulated on per generation or on shorter time steps. 3) We introduce the framework before developing example models with parameters chosen to exhibit specific dynamics. These models reveal (i) how evolution of a phenotype can cause populations to move from one dynamical regime to another (e.g. from stationarity to cycles), (ii) how additive genetic variances and covariances (the G matrix) are expected to evolve over multiple generations, (iii) how changing heritability with age can maintain additive genetic variation in the face of selection and (iii) life history, population dynamics, phenotypic characters and parameters in ecological models will change as adaptation occurs. 4) Our approach unifies population ecology and evolutionary biology providing a framework allowing a very wide range of questions to be addressed. The next step is to apply the approach to a variety of laboratory and field systems. Once this is done we will have a much deeper understanding of eco-evolutionary dynamics and feedbacks.

Genomic instability causes cancers to acquire hundreds to thousands of mutations and chromosomal alterations during their somatic evolution. Most of these mutations and alterations are termed passengers because they do not confer cancer phenotypes. Evolutionary simulations and cancer genomic studies suggested that mildly-deleterious passengers accumulate, collectively slow cancer progression, reduce the fitness of cancer cells and enhance the effects of therapeutics. However, these effects of passengers and their impact on clinical variables remain limited to genomic analysis. Here, to assess passengers’ effect on cell fitness and cancer, we specifically introduced increasing passenger loads into human cell lines and mouse models. We found that passenger load dramatically reduced cancer cell’s fitness in every model investigated. Passengers’ average fitness cost of ~3% per MB, indicates that genomic instability in cancer in patients can slow tumor growth and prevent metastatic progression. We conclude that genomic instability in cancer is a double-edged sword: it accelerates the accumulation of adaptive drivers, yet incurs a harmful passenger load that can outweigh drivers’ benefit. Passenger load could be a useful biomarker for tumor aggressiveness and response to mutagenic or passenger-exacerbating therapies, including anti-tumor immunity.

A fundamental consideration for the conservation of a species is the extent of its native range, however defining a native range is often challenging as changing environments drive shifts in species distributions over time. The crucian carp, Carassius carassius (L.) is a threatened freshwater fish native to much of Europe, however the extent of this range is ambiguous. One particularly contentious region is England, in which C. carassius is currently considered native on the basis of anecdotal evidence. Here, we use 13 microsatellite loci, population structure analyses and approximate bayesian computation (ABC), to empirically test the native status of C. carassius in England. Contrary to the current consensus, ABC yields strong support for introduced origins of C. carassius in England, with posterior distribution estimates placing their introduction in the 15th century, well after the loss of the doggerland landbridge. This result brings to light an interesting and timely debate surrounding our motivations for the conservation of species. We discuss this topic, and make arguments for the continued conservation of C. carassius in England, despite its non-native origins.

Forest trees generally show high levels of local adaptation and efforts focusing on understanding adaptation to climate will be crucial for species survival and management. Merging quantitative genetics and population genomics, we studied the molecular basis of climate adaptation in 433 Populus trichocarpa (black cottonwood) genotypes originating across western North America. Variation in 74 field-assessed traits (growth, ecophysiology, phenology, leaf stomata, wood, and disease resistance) was investigated for signatures of selection (comparing QST -FST) using clustering of individuals by climate of origin. 29,354 SNPs were investigated employing three different outlier detection methods. Narrow-sense QST for 53% of distinct field traits was significantly divergent from expectations of neutrality (indicating adaptive trait variation); 2,855 SNPs showed signals of diversifying selection, and of these, 118 SNPs (within 81 genes) were associated with adaptive traits (based on significant QST). Many SNPs were putatively pleiotropic for functionally uncorrelated adaptive traits, such as autumn phenology, height, and disease resistance. Evolutionary quantitative genomics in P. trichocarpa provides an enhanced understanding regarding the molecular basis of climate-driven selection in forest trees. We highlight that important loci underlying adaptive trait variation also show relationship to climate of origin.

Many long noncoding RNAs (lncRNAs) can regulate chromatin states, but the evolutionary origin and dynamics driving lncRNA-genome interactions are unclear. We developed an integrative strategy that identifies lncRNA orthologs in different species despite limited sequence similarity that is applicable to fly and mammalian lncRNAs. Analysis of the roX lncRNAs, which are essential for dosage compensation of the single X-chromosome in Drosophila males, revealed 47 new roX orthologs in diverse Drosophilid species across ~40 million years of evolution. Genetic rescue by roX orthologs and engineered synthetic lncRNAs showed that evolutionary maintenance of focal structural repeats mediates roX function. Genomic occupancy maps of roX RNAs in four species revealed rapid turnover of individual binding sites but conservation within nearby chromosomal neighborhoods. Many new roX binding sites evolved from DNA encoding a pre-existing RNA splicing signal, effectively linking dosage compensation to transcribed genes. Thus, evolutionary analysis illuminates the principles for the birth and death of lncRNAs and their genomic targets.