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bioRxiv2016

On the (un-)predictability of a large intragenic fitness landscape

The study of fitness landscapes, which aims at mapping genotypes to fitness, is receiving ever-increasing attention. Novel experimental approaches combined with NGS methods enable accurate and extensive studies of the fitness effects of mutations - allowing us to test theoretical predictions and improve our understanding of the shape of the true underlying fitness landscape, and its implications for the predictability and repeatability of evolution.\n\nHere, we present a uniquely large multi-allelic fitness landscape comprised of 640 engineered mutants that represent all possible combinations of 13 amino-acid changing mutations at six sites in the heat-shock protein Hsp90 in Saccharomyces cerevisiae under elevated salinity. Despite a prevalent pattern of negative epistasis in the landscape, we find that the global fitness peak is reached via four positively epistatic mutations. Combining traditional and extending recently proposed theoretical and statistical approaches, we quantify features of the global multi-allelic fitness landscape. Using subsets of the data, we demonstrate that extrapolation beyond a known part of the landscape is difficult owing to both local ruggedness and amino-acid specific epistatic hotspots, and that inference is additionally confounded by the non-random choice of mutations for experimental fitness landscapes.\n\nAuthor SummaryThe study of fitness landscapes is fundamentally concerned with understanding the relative roles of stochastic and deterministic processes in adaptive evolution. Here, the authors present a uniquely large and complete multi-allelic intragenic fitness landscape of 640 systematically engineered mutations in yeast Hsp90. Using a combination of traditional and recently proposed theoretical approaches, they study the accessibility of the global fitness peak, and the potential for predictability of the fitness landscape topography. They report local ruggedness of the landscape and the existence of epistatic hotspot mutations, which together make extrapolation and hence predictability inherently difficult, if mutation-specific information is not considered.

Evolutionary Biology↗

bioRxiv2016

Selective pressures on C4 photosynthesis evolution in grasses through the lens of optimality

CO2, temperature, water availability and light intensity were all potential selective pressures to propel the initial evolution and global expansion of C4 photosynthesis over the last 30 million years. To tease apart how the primary selective pressures varied along this evolutionary trajectory, we coupled photosynthesis and hydraulics models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of resource (e.g. nitrogen) reallocation from the dark to the light reactions during and after the initial formation of C4 syndrome. We show here that the primary selective pressures--all acting upon photorespiration in C3 progenitors--changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root allocation ratio enabled by the C4 carbon-concentrating mechanism led to a C4 advantage without any change in hydraulic properties, but selection on nitrogen reallocation varied. Water limitation was the primary driver for the initial evolution of C4 25-32 million years ago, and could positively select for C4 evolution with atmospheric CO2 as high as 600 ppm. Under these high CO2 conditions, nitrogen reallocation was necessary. Low CO2 and light intensity, but not nitrogen reallocation, were the primary drivers during the global radiation of C4 5-10 MYA. Finally, our results suggest that identifying the predominate selective pressures at the time C4 first evolved within a lineage should help explain current biogeographical distributions.\n\nStatement of authorshipHZ, BH and EA conceptualized the study. HZ and EA built the model, HZ and BH put the idea in a general evolutionary context, HZ performed the modeling work and analyzed output data. HZ wrote the first draft, BH and EA contributed substantially to revisions.\n\nSignificance StatementC4 photosynthesis pathway had evolved more than 60 times independently across the terrestrial plants through mid-Oligocene (~30 MYA) and diversified at late Miocene (5 to 10 MYA). We use an optimal physiology model to examine the primary selective pressures along the evolutionary history. Water limitation was the primary driver for C4 evolution from the initial evolutionary events 25-32 MYA until CO2 became low enough to, along with light intensity, drive the global radiation of C4 5-10 MYA. This modeling framework can be used to investigate evolution of other physiological traits (e.g. N reallocation, hydraulics) after the initial formation of C4 syndrome, which contributed to further increasing productivity of C4 in historical and current environmental conditions.

Evolutionary Biology↗

bioRxiv2016

An experimental evaluation of drug-induced mutational meltdown as an antiviral treatment strategy

The rapid evolution of drug resistance remains a critical public health concern. The treatment of influenza A virus (IAV) has proven particularly challenging, due to the ability of the virus to develop resistance against current antivirals and vaccines. Here we evaluate a novel antiviral drug therapy, favipiravir, for which the mechanism of action in IAV involves an interaction with the viral RNA-dependent RNA polymerase resulting in an effective increase in the viral mutation rate. We utilized an experimental evolution framework, combined with novel population genetic method development for inference from time-sampled data, in order to evaluate the effectiveness of favipiravir against IAV. Evaluating whole genome polymorphism data across fifteen time points under multiple drug concentrations and in controls, we present the first evidence for the ability of viral populations to effectively adapt to low concentrations of favipiravir. In contrast, under high concentrations, we observe population extinction, indicative of mutational meltdown. We discuss the observed dynamics with respect to the evolutionary forces at play and emphasize the utility of evolutionary theory to inform drug development.

Evolutionary Biology↗

bioRxiv2016

On the importance of skewed offspring distributions and background selection in viral population genetics

Many features of virus populations make them excellent candidates for population genetic study, including a very high rate of mutation, high levels of nucleotide diversity, exceptionally large census population sizes, and frequent positive selection. However, these attributes also mean that special care must be taken in population genetic inference. For example, highly skewed offspring distributions, frequent and severe population bottleneck events associated with infection and compartmentalization, and strong purifying selection all affect the distribution of genetic variation but are often not taken in to account. Here, we draw particular attention to multiple-merger coalescent events and background selection, discuss potential mis-inference associated with these processes, and highlight potential avenues for better incorporating them in to future population genetic analyses.

Evolutionary Biology↗

bioRxiv2016

Did viruses evolve as a distinct supergroup from common ancestors of cells?

The evolutionary origins of viruses according to marker gene phylogenies, as well as their relationships to the ancestors of host cells remains unclear. In a recent article Nasir and Caetano-Anolles reported that their genome-scale phylogenetic analyses identify an ancient origin of the \"viral supergroup\" (Nasir et al (2015) A phylogenomic data-driven exploration of viral origins and evolution. Science Advances, 1(8):e1500527). It suggests that viruses and host cells evolved independently from a universal common ancestor. Examination of their data and phylogenetic methods indicates that systematic errors likely affected the results. Reanalysis of the data with additional tests shows that small-genome attraction artifacts distort their phylogenomic analyses. These new results indicate that their suggestion of a distinct ancestry of the viral supergroup is not well supported by the evidence.

Evolutionary Biology↗

bioRxiv2016

Allele Surfing Promotes Microbial Adaptation from Standing Variation

The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from soft selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource-limited populations to cope with environmental challenges.

Evolutionary Biology↗

bioRxiv2016

Estimating seven coefficients of pairwise relatedness using population genomic data

Population structure can be described by genotypic correlation coefficients between groups of individuals, the most basic of which are the pair-wise relatedness coefficients between any two individuals. There are nine pair-wise relatedness coefficients in the most general model, and we show that these can be reduced to seven coefficients for biallelic loci. Although all nine coefficients can be estimated from pedigrees, six coefficients have been beyond empirical reach. We provide a numerical optimization procedure that estimates them from population-genomic data. Simulations show that the procedure is nearly unbiased, even at 3x coverage, and errors in five of the seven coefficients are statistically uncorrelated. The remaining two coefficients have a negative correlation of errors, but their sum provides an unbiased assessment of the overall correlation of heterozygosity between two individuals. Application of these new methods to four populations of the freshwater crustacean Daphnia pulex reveal the occurrence of half-siblings in our samples, as well as a number of identical individuals that are likely obligately asexual clone-mates. Statistically significant negative estimates of these pair-wise relatedness coefficients, including inbreeding coefficents that were typically negative, underscore the difficulties that arise when interpreting genotypic correlations as estimations of the probability that alleles are identical by descent.

Evolutionary Biology↗

bioRxiv2016

Evolution of mating types driven by purifying selection against mitochondrial mutations

Sexual cell fusion combines genetic material of two gametes, but why the two reproductive cells have to belong to distinct self-incompatible gamete classes is not known. In a vast majority of sexual eukaryotes, mitochondria are inherited uniparentally from only one of the two mating types, which is thought to facilitate purifying selection against deleterious mitochondrial mutations and limit the inter-genomic conflicts. Here I argue that two mating types in eukaryotes represent a mechanism of mitochondrial quality control through the highly asymmetric transmission of mitochondrial genes at cell fusion. I develop a mathematical model to explicitly study the evolution of two self-incompatible mating type alleles linked to the nuclear locus controlling the pattern of organelle inheritance. The invasion of mating-type alleles is opposed by the short-term fitness benefit of mitochondrial mixing under negative epistasis and the lower chance of encountering a compatible mating partner. Nevertheless, under high mitochondrial mutation rates purifying selection against defective mitochondria can drive two mating types with uniparental inheritance to fixation. The invasion is further facilitated by the paternal leakage of mitochondria under paternal control of cytoplasmic inheritance. In contrast to previous studies, the model does not rely on the presence of selfish cytoplasmic elements, providing a more universal solution to the longstanding evolutionary puzzle of two sexes.

Evolutionary Biology↗

bioRxiv2016

Sanctions, partner recognition, and variation in mutualistic symbiosis

Mutualistic interactions can be stabilized against invasion by non-cooperative individuals by putting such \"cheaters\" at a selective disadvantage. Selection against cheaters should eliminate genetic variation in partner quality -- yet such variation is often found in natural populations. One explanation for this paradox is that mutualism outcomes are determined not only by responses to partner performance, but also by partner signals. Here, we build a model of coevolution in a symbiotic mutualism, in which hosts ability to sanction non-cooperative symbionts and recognition of symbiont signals are determined by separate loci, as are symbionts cooperation and expression of signals. In the model, variation persists without destabilizing the interaction, in part because coevolution of symbiont signals and host recognition is altered by the coevolution of sanctions and cooperation, and vice-versa. Individual-based simulations incorporating population structure strongly corroborate these results. The dual systems of sanctions and partner recognition converge toward conditions similar to some economic models of mutualistic symbiosis in which hosts offering the right incentives to potential symbionts can initiate symbiosis without screening for partner quality. These results predict that mutualists can maintain variation in recognition of partner signals or in the ability to sanction non-cooperators without destabilizing mutualism, and reinforce the notion that studies of mutualism should consider communication between partners as well as the exchange of benefits.

Evolutionary Biology↗

bioRxiv2016

Inferring node dates from tip dates in fossil Canidae: the importance of tree priors

Tip-dating methods are becoming popular alternatives to traditional node calibration approaches for building time-scaled phylogenetic trees, but questions remain about their application to empirical datasets. We compared the performance of the most popular methods against a dated tree of fossil Canidae derived from previously published monographs. Using a canid morphology dataset, we performed tip-dating using Beast 2.1.3 and MrBayes 3.2.5. We find that for key nodes (Canis, ~3.2 Ma, Caninae ~11.7 Ma) a non-mechanistic model using a uniform tree prior produces estimates that are unrealistically old (27.5, 38.9 Ma). Mechanistic models (incorporating lineage birth, death, and sampling rates) estimate ages that are closely in line with prior research. We provide a discussion of these two families of models (mechanistic vs. non-mechanistic) and their applicability to fossil datasets.

Evolutionary Biology↗

bioRxiv2016

Evolutionary dynamics of chloroplast genomes in low light: a case study of the endolithic green alga Ostreobium quekettii

Some photosynthetic organisms live in extremely low light environments. Light limitation is associated with selective forces as well as reduced exposure to mutagens, and over evolutionary timescales it can leave a footprint on species genome. Here we present the chloroplast genomes of four green algae (Bryopsidales, Ulvophyceae), including the endolithic (limestone-boring) alga Ostreobium quekettii, which is a low light specialist. We use phylogenetic models and comparative genomic tools to investigate whether the chloroplast genome of Ostreobium corresponds to our expectations of how low light would affect genome evolution. Ostreobium has the smallest and most gene-dense chloroplast genome among Ulvophyceae reported to date, matching our expectation that light limitation would impose resource constraints. Rates of molecular evolution are significantly slower along the phylogenetic branch leading to Ostreobium, in agreement with the expected effects of low light and energy levels on molecular evolution. Given the exceptional ability of our model organism to photosynthesize under extreme low light conditions, we expected to observe positive selection in genes related to the photosynthetic machinery. However, we observed stronger purifying selection in these genes, which might either reflect a lack of power to detect episodic positive selection followed by purifying selection and/or a strengthening of purifying selection due to the loss of a gene related to light sensitivity. Besides shedding light on the genome dynamics associated with a low light lifestyle, this study helps to resolve the role of environmental factors in shaping the diversity of genome architectures observed in nature.\n\nData deposition: Chloroplast genome sequences will be deposited in GenBank

Evolutionary Biology↗

bioRxiv2016

Radical changes persist longer in the absence of sex

Harmful mutations are ubiquitous and inevitable, and the rate at which these mutations are removed from populations is a critical determinant of evolutionary fate. Closely related sexual and asexual taxa provide a particularly powerful setting to study deleterious mutation elimination because sexual reproduction should facilitate mutational clearance by reducing selective interference between sites and by allowing the production of offspring with different mutational complements than their parents. Here, we compared the rate of removal of conservative (i.e., similar biochemical properties) and radical (i.e., distinct biochemical properties) nonsynonymous mutations from mitochondrial genomes of sexual vs. asexual Potamopyrgus antipodarum, a New Zealand freshwater snail characterized by coexisting and ecologically similar sexual and asexual lineages. Our analyses revealed that radical nonsynonymous mutations are cleared at higher rates than conservative changes and that sexual lineages eliminate radical changes more rapidly than asexual counterparts. These results are consistent with reduced efficacy of purifying selection in asexual lineages allowing harmful mutations to remain polymorphic longer than in sexual lineages. Together, these data illuminate some of the population-level processes contributing to mitochondrial mutation accumulation and suggest that mutation accumulation could influence the outcome of competition between sexual and asexual lineages.

Evolutionary Biology↗

bioRxiv2016

No ′small genome attraction′ artifact: A response to Harish et al. ′Did viruses evolve as a distinct supergroup from common ancestors of cells?′

In a recent eLetter and associated preprint, Harish, Abroi, Gough and Kurland criticized our structural phylogenomic methods, which support the early cellular origin of viruses. Their claims include the argument that the rooting of our trees is artifactual and distorted by small genome (proteome) size. Here we uncover their aprioristic reasoning, which mingles with misunderstandings and misinterpretations of cladistic methodology. To demonstrate, we labeled the phylogenetic positions of the smallest proteomes in our phylogenetic trees and confirm that the smallest genomes were neither attracted towards the root nor caused any distortions in the four-supergroup tree of life. Their results therefore stem from confusing outgroups with ancestors and handpicking problematic taxa to distort tree reconstruction. In doing so, they ignored the details of our rooting method, taxa sampling rationale, the plethora of evidence given in our study supporting the ancient origin of the viral supergroup and also recent literature on viral evolution. Indeed, our tree of life uncovered many viral monophyletic groups consistent with ICTV classifications and showed remarkable evolutionary tracings of virion morphotypes onto a revealing tree topology.

Evolutionary Biology↗

bioRxiv2016

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes

Sperm cells provide crucial, if usually diminutive, ingredients to successful sexual reproduction as the source of centrioles and half the diploid genome. Despite this essential conserved function, sperm competition and coevolution with female traits can drive spectacular change in size and shape of these motile cells. Here we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Exploring potential genetic and developmental determinants of Caenorhabditis sperm size variation, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes of androdioecious species, as well as within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development, i.e. at the formation of primary spermatocytes while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter-and intraspecific sperm size differences in Caenorhabditis. Together, our results provide a novel integrative view on the developmental and evolutionary origins of Caenorhabditis sperm size variation. We hypothesize that life history and/or ecological differences among species favoured the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm, with gigantic sperm potentially providing a means of paternal care via gametic provisioning or as a potent vehicle for sexual conflict over offspring development.

Evolutionary Biology↗

bioRxiv2016

Nuclear and Plastid DNA Sequence-based Molecular Phylogeography of Salvadora oleoides (Salvadoraceae) in Punjab, India

Salvadora oleiodes is a tropical tree species belonging to the little-known family Salvadoraceae and distributed in the arid regions of Africa and Asia. Aims of our study were to trace the microevolutionary legacy of this tree species with the help of sequence-based multi-local phylogeography and to find the comparative placement of family Salvadoraceae within angiosperm clade malvids. A total 20 geographical isolates were collected from different regions of North India, covering a major part of its species range within the Indian Subcontinent. Sequence data from nuclear-encoded Internal Transcribed Spacer region (ITS1-5.8S-ITS2) and plastid-encoded trnL-F spacer region, were generated for this species for the first time in the world. ITS-based Bayesian phylogeographic analysis revealed the existence of four clades while trnL-F spacer based Bayesian analysis revealed one clade for this species distributed in the Indian subcontinent. Between these two loci, ITS revealed more distinct phylogeographic clades, indicating the phylogeographic utility of this locus for the systematics of Salvadoraceae. Phylogenetic analyzes based on trnL-F spacer suggested a synonymy of this species with Salvadora angustifolia. Maximum Likelihood gene tree based on ITS sequence data revealed that Salvadoraceae belongs to Sapindales rather than Brassicales. However, in the gene tree based on trnL-F spacer sequence, this family clustered within Brassicales. An evolutionary congruence of S. oleoides isolates across its range in North India is revealed in this study. Given the conflicting results on the relative placement of Salvadoraceae in Brassicales and Sapindales, the need for further phylogenetic analyses of malvids using supermatrix approach is highlighted.

Evolutionary Biology↗

bioRxiv2016

Urbanization drives parallel adaptive clines in plant populations

Urban areas are a new and increasingly dominant feature of terrestrial landscapes that dramatically alter environments. It is unclear whether wild populations can adapt to the unique challenges presented by urbanization. To address this problem, we sampled the frequency of a Mendelian-inherited trait--cyanogenesis--in white clover (Trifolium repens L.) plants along urbanization gradients in four large cities. Cyanogenesis protects plants from herbivores, but also reduces freezing tolerance. Plants evolved reduced cyanogenesis with increasing proximity to the urban center in three of the four cities. In an experiment, we demonstrate that gradients in herbivore pressure do not cause these clines. Instead, urban areas experience relatively cold minimum winter ground temperatures because of reduced snow cover within cities, which selects against cyanogenesis. Together, our study demonstrates that wild populations exhibit parallel adaptive evolution in response to urbanization, which likely facilitates the persistence of these plants and promotes pollinator abundance and diversity.

Evolutionary Biology↗

bioRxiv2016

Evolutionary mysteries in meiosis.

Meiosis is a key event of sexual life cycles in eukaryotes. Its mechanistic details have been uncovered in several model organisms, and most of its essential features have received various and often contradictory evolutionary interpretations. In this perspective, we present an overview of these often \"weird\" features. We discuss the origin of meiosis (origin of ploidy reduction and recombination, two-step meiosis), its secondary modifications (in polyploids or asexuals, inverted meiosis), its importance in punctuating life cycles (meiotic arrests, epigenetic resetting, meiotic asymmetry, meiotic fairness) and features associated with recombination (disjunction constraints, heterochiasmy, crossover interference and hotspots). We present the various evolutionary scenarios and selective pressures that have been proposed to account for these features, and we highlight that their evolutionary significance often remains largely mysterious. Resolving these mysteries will likely provide decisive steps towards understanding why sex and recombination are found in the majority of eukaryotes.

Evolutionary Biology↗

bioRxiv2016

How life history can sway the fixation probability of mutants

In this work, we study the effects of demographic structure on evolutionary dynamics, when selection acts on reproduction, survival, or both. In contrast with the previously discovered pattern that the fixation probability of a neutral mutant decreases while population becomes younger, we show that a mutant with constant selective advantage may have a maximum or a minimum of the fixation probability in populations with an intermediate fraction of young individuals. This highlights the importance of life history and demographic structure in studying evolutionary dynamics. We also illustrate the fundamental differences between selection on reproduction and on survival when age structure is present. In addition, we evaluate the relative importance of size and structure of the population in determining the fixation probability of the mutant. Our work lays the foundation for studying also density and frequency dependent effects in populations when demographic structures cannot be neglected.

Evolutionary Biology↗