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bioRxiv2016

The Impact of Migratory Flyways on the Spread of Avian Influenza Virus in North America

Wild birds are the major reservoir hosts for influenza A viruses (AIVs) and have been implicated in the emergence of pandemic events in livestock and human populations. Understanding how AIVs spread within and across continents is therefore critical to the development of successful strategies to manage and reduce the impact of influenza outbreaks. In North America many bird species undergo seasonal migratory movements along a North-South axis, thereby fostering opportunities for viruses to spread over long distances. However, the role played by such avian flyways in shaping the genetic structure of AIV populations has proven controversial. To assess the relative contribution of bird migration along flyways to the genetic structure of AIV we performed a large-scale phylogeographic study of viruses sampled in the USA and Canada, involving the analysis of 3805 to 4505 sequences from 36 to 38 geographic localities depending on the gene data set. To assist this we developed a maximum likelihood-based genetic algorithm to explore a wide range of complex spatial models, thereby depicting a more complete picture of the migration network than previous studies. Based on phylogenies estimated from nucleotide data sets, our results show that AIV migration rates within flyways are significantly higher than those between flyways, indicating that the migratory patterns of birds play a key role in pathogen dispersal. These findings provide valuable insights into the evolution, maintenance and transmission of AIVs, in turn allowing the development of improved programs for surveillance and risk assessment.\n\nSignificance StatementAvian influenza viruses infect a wide variety of wild bird species and represent a potential disease threat to the poultry industry and hence to human and livestock populations. However, the ecological factors that drive the geographic spread and evolution of these viruses are both poorly understood and controversial at the continental scale, particularly the role played by migratory flyways in shaping patterns of virus dispersal. Using a novel phylogeographic analysis of large genomic data sets we show migration flyways act as important transmission barriers to the spread of avian influenza viruses in North America. Hence, these results indicate that the spread of avian influenza virus in wild birds in North America has an element of predictability.

Evolutionary Biology↗

bioRxiv2016

The species problem from the modeler’s point of view

How to define a partition of individuals into species is a long-standing question called the species problem in systematics. Here, we focus on this problem in the thought experiment where individuals reproduce clonally and both the differentiation process and the population genealogies are explicitly known. We point out three desirable properties of species partitions: (A) Heterotypy between species, (B) Homotypy within species and (M) Monophyly of each species. We then ask: How and when is it possible to delineate species in a way satisfying these properties?\n\nWe point out that the three desirable properties cannot in general be satisfied simultaneously, but that any two of them can. We mathematically prove the existence of the finest partition satisfying (A) and (M) and the coarsest partition satisfying (B) and (M). For each of them, we propose a simple algorithm to build the associated phylogeny out of the genealogy.\n\nThe ways we propose to phrase the species problem shed new light on the interaction between the genealogical and phylogenetic scales in modeling work. The two definitions centered on the monophyly property can readily be used at a higher taxonomic level as well, e.g. to cluster species into monophyletic genera.

Evolutionary Biology↗

bioRxiv2016

Multiple factors influence population sex ratios in the Mojave Desert moss Syntrichia caninervis

O_LIPremise of research: Natural populations of many mosses appear highly female-biased based on the presence of reproductive structures. This bias could be caused by increased male mortality, lower male growth rate, or a higher threshold for achieving sexual maturity in males. Here we test these hypotheses using samples from two populations of the Mojave Desert moss Syntrichia caninervis.\nC_LIO_LIMethods: We used double digest restriction-site associated DNA (RAD) sequencing to identify candidate sex-associated loci in a panel of sex-expressing plants. Next, we used putative sex-associated markers to identify the sex of individuals without sex structures.\nC_LIO_LIKey results: We found an 18:1 phenotypic female: male sex ratio in the higher elevation site (Wrightwood), and no sex expression at the low elevation site (Phelan). In contrast, based on genetic data we found a 2:1 female bias in the Wrightwood site and only females in the Phelan site. The area occupied by male and female genets was indistinguishable.\nC_LIO_LIConclusions: These data suggest that both differential mortality and sexual dimorphism in thresholds for sex expression likely contribute to population genetic and phenotypic sex ratio biases, and that phenotypic sex expression alone fails to capture the extent of actual sex ratio bias present in natural populations of S. caninervis.\nC_LI

Evolutionary Biology↗

bioRxiv2016

Pre-metazoan origin of animal miRNAs

microRNAs (miRNAs) are integrated parts of the developmental toolkit in animals. The evolutionary history and origins of animal miRNAs is however unclear, and it is not known when they evolved and on how many occasions. We have therefore investigated the presence of miRNAs and the necessary miRNA biogenesis machinery in a large group of unicellular relatives of animals, Ichthyosporea. By small RNA sequencing we find evidence for at least four genes in the genus Sphaeroforma that satisfy the criteria for the annotation of animal miRNA genes. Three of these miRNAs are conserved and expressed across sphaeroformid species. Furthermore, we identify homologues of the animal miRNA biogenesis genes across a wide range of ichthyosporeans, including Drosha and Pasha which make up the animal specific Microprocessor complex. Taken together we report the first evidence for bona fide miRNA genes and the presence of the miRNA-processing pathway in unicellular Choanozoa, implying that the origin of animal miRNAs and the Microprocessor complex predates multicellular animals.

Evolutionary Biology↗

bioRxiv2016

The Melting Snowball: A Test of the Snowball Model Using RNA

Genetic incompatibilities can emerge as a by-product of genetic divergence. According to Dobzhansky and Muller, alleles at different loci that have fixed in different genetic backgrounds may be incompatible when brought together in a hybrid. Orr showed that the number of Dobzhansky-Muller incompatibilities (DMIs) should accumulate faster than linearly--i.e., snowball--as two lineages diverge. Several studies have attempted to test the snowball model using data from natural populations. One limitation of these studies is that they have focused on predictions of the snowball model but not on its underlying assumptions. Here we use a computational model of RNA folding to test both predictions and assumptions of the snowball model. In this model, two populations are allowed to evolve in allopatry on a holey fitness landscape. We find that the number of DMIs involving pairs of loci (i.e., simple DMIs) does not snowball--rather, it increases approximately linearly with divergence. We show that the probability of emergence of a simple DMI is approximately constant, as assumed by the snowball model. However, simple DMIs can disappear after they have arisen, contrary to the assumptions of the snowball model. This occurs because simple DMIs become complex (i.e., involve alleles at three or more loci) as a result of later substitutions. We introduce a modified snowball model--the melting snowball model--where simple DMIs can become complex after they appear. The melting snowball model can account for the results of the RNA folding model. We also find that complex DMIs are common and, unlike simple ones, do snowball. Reproductive isolation, however, does not snowball because DMIs do not act independently of each other. We conclude that the RNA folding model supports the central prediction of the snowball model that the number of DMIs snowballs, but challenges some of its underlying assumptions.

Evolutionary Biology↗

bioRxiv2016

Deep-time parallel evolution of myrmecoid syndrome in rove beetle symbionts of army ants

Recent adaptive radiations provide striking examples of convergence, but the predictability of evolution over much deeper timescales is controversial, due to a scarcity of ancient clades exhibiting repetitive patterns of phenotypic evolution. Army ants are ecologically dominant arthropod predators of the world's tropics, with large nomadic colonies housing diverse communities of socially parasitic myrmecophiles. Remarkable among these are many species of rove beetle (Staphylinidae) that exhibit ant-mimicking \"myrmecoid\" body forms and are behaviorally accepted into their aggressive hosts' societies: emigrating with colonies and inhabiting temporary nest bivouacs, grooming and feeding with workers, but also consuming the brood. Here we demonstrate that myrmecoid rove beetles are strongly polyphyletic, with this novel adaptive morphological and behavioral syndrome having evolved at least twelve times during the evolution of a single staphylinid subfamily, Aleocharinae. Each independent myrmecoid clade is restricted to one zoogeographic region and highly host-specific on a single army ant genus. Dating estimates reveal that myrmecoid clades are separated by substantial phylogenetic distances--as much as 105 million years (My). All such groups arose in parallel during the Cenozoic, as army ants are proposed to have risen to ecological dominance. This work uncovers a rare example of an ancient system of complex morphological and behavioral convergence, with replicate beetle lineages following a predictable phenotypic trajectory during their parasitic coevolution with army ants.

Evolutionary Biology↗

bioRxiv2016

Seasonal influenza circulation patterns and projections for 2016-2017

This is not meant as a comprehensive report, but is instead intended as particular observations that may be of relevance. Please also note that observed patterns reflect the GISAID database and may not be entirely representative of underlying dynamics. All analyses are based on the nextflu pipeline [1] with continual updates posted to Correspondence:http://nextflu.org.

Evolutionary Biology↗

bioRxiv2016

Larger Numbers can Impede Adaptation in Microbial Populations despite Entailing Greater Genetic Variation

Periodic bottlenecks play a major role in shaping the adaptive dynamics of natural and laboratory populations of asexual microbes. Here we study how they affect the Extent of Adaptation (EoA), in such populations. EoA, the average fitness gain relative to the ancestor, is the quantity of interest in a large number of microbial experimental-evolution studies which assume that for any given bottleneck size (N0) and number of generations between bottlenecks (g), the harmonic mean size (HM=N0g) will predict the ensuing evolutionary dynamics. However, there are no theoretical or empirical validations for HM being a good predictor of EoA. Using experimental-evolution with Escherichia coli and individual-based simulations, we show that HM fails to predict EoA (i.e., higher N0g does not lead to higher EoA). This is because although higher g allows populations to arrive at superior benefits by entailing increased variation, it also reduces the efficacy of selection, which lowers EoA. We show that EoA can be maximized in evolution experiments by either maximizing N0 and/or minimizing g. We also conjecture that N0/g is a better predictor of EoA than N0g. Our results call for a re-evaluation of the role of population size in predicting fitness trajectories. They also aid in predicting adaptation in asexual populations, which has important evolutionary, epidemiological and economic implications.

Evolutionary Biology↗

bioRxiv2016

EARLY INFLAMMATION, IMMUNOPATHOLOGY AND AGING

Age-related diseases are often attributed to immunopathology, which results in self-damage caused by an inappropriate inflammatory response. Immunopathology associated with early-life inflammation also appears to cause faster ageing, although we lack direct experimental evidence for this association. To understand the interactions between ageing, inflammation and immunopathology, we used the mealworm beetle Tenebrio molitor as a study organism. We hypothesized that phenoloxidase (PO), an important immune effector in insect defence, may impose substantial immunopathological costs by causing tissue damage, in turn accelerating aging. In support of this hypothesis, we found that RNAi knockdown of PO transcripts in young adults reduced inflammation-induced autoreactive tissue damage to Malpighian tubules, and increased adult lifespan. Our work thus provides empirical evidence for a causative link between immunopathological costs of early life inflammation and faster ageing. We also reasoned that if natural selection weakens with age, older individuals should display increased immunopathological costs associated with an immune response. Indeed, we found that while old infected individuals cleared infection faster than young individuals, they displayed exacerbated immunopathological costs and higher post-infection mortality. RNAi-mediated knockdown of PO response reduced immunopathology in older beetles and increased their lifespan after infection. This is the first demonstration of a direct role of immunopathological consequences of immune response during ageing in insects. Our work is also the first report that highlights the pervasive role of immunopathology under diverse contexts of aging and immune response.

Evolutionary Biology↗

bioRxiv2016

The Opiliones Tree of Life: shedding light on harvestmen relationships through transcriptomics

Opiliones are iconic arachnids with a Paleozoic origin and a diversity that reflects ancient biogeographical patterns dating back at least to the times of Pangea. Due to interest in harvestman diversity, evolution and biogeography, their relationships have been thoroughly studied using morphology and PCR-based Sanger approaches to systematics. More recently, two studies utilized transcriptomics-based phylogenomics to explore their basal relationships and diversification, but sampling was limiting for understanding deep evolutionary patterns, as they lacked good taxon representation at the family level. Here we analyze a set of the 14 existing transcriptomes with 40 additional ones generated for this study, representing ca. 80% of the extant familial diversity in Opiliones. Our phylogenetic analyses, including a set of data matrices with different gene occupancy and evolutionary rates, and using a multitude of methods correcting for a diversity of factors affecting phylogenomic data matrices, provide a robust and stable Opiliones tree of life, where most families are precisely placed. Our dating analyses also using alternative calibration points, methods, and analytical parameters provide well-resolved old divergences, consistent with ancient regionalization in Pangea in some groups, and Pangean vicariance in others. The integration of state-of-the-art molecular techniques and analyses, together with the broadest taxonomic sampling to date presented in a phylogenomic study of harvestmen, provide new insights into harvestmen interrelationships, as well as a general overview of the general biogeographic patterns of this ancient arthropod group.

Evolutionary Biology↗

bioRxiv2016

The genetic basis and fitness consequences of sperm midpiece size in deer mice

An extraordinary array of reproductive traits vary among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive. Here we examine two sister-species of Peromyscus mice with divergent mating systems. We find that the promiscuous species produces sperm with longer midpiece than the monogamous species, and midpiece size correlates positively with competitive ability and swimming performance. Using forward genetics, we identify a gene associated with midpiece length: Prkar1a, which encodes the R1 regulatory subunit of PKA. R1 localizes to midpiece in Peromyscus and is differentially expressed in mature sperm of the two species yet is similarly abundant in the testis. We also show that genetic variation at this locus accurately predicts male reproductive success. Our findings suggest that rapid evolution of reproductive traits can occur through cell type-specific changes to ubiquitously expressed genes and have an important effect on fitness.

Evolutionary Biology↗

bioRxiv2016

Approximate Likelihood Inference of Complex Population Histories and Recombination from Multiple Genomes

We introduce ABLE (Approximate Blockwise Likelihood Estimation), a novel composite likelihood framework based on a recently introduced summary of sequence variation: the blockwise site frequency spectrum (bSFS). This simulation-based framework uses the the frequencies of bSFS configurations to jointly model demographic history and recombination and is explicitly designed to make inference using multiple whole genomes or genome-wide multi-locus data (e.g. RADSeq) catering to the needs of researchers studying model or non-model organisms respectively. The flexible nature of our method further allows for arbitrarily complex population histories using unphased and unpolarized whole genome sequences. In silico experiments demonstrate accurate parameter estimates across a range of divergence models with increasing complexity, and as a proof of principle, we infer the demographic history of the two species of orangutan from multiple genome sequences (over 160 Mbp in length) from each species. Our results indicate that the two orangutan species split approximately 650-950 thousand years ago but experienced a pulse of secondary contact much more recently, most likely during a period of low sea-level South East Asia ([~]300,000 years ago). Unlike previous analyses we can reject a history of continuous gene flow and co-estimate genome-wide recombination. ABLE is available for download at https://github.com/champost/ABLE.

Evolutionary Biology↗

bioRxiv2016

A phylogenetic codon substitution model for antibody lineages

Phylogenetic methods have shown promise in understanding the development of broadly neutralizing antibody lineages (bNAbs). However, the mutational process that generates these lineages - somatic hypermutation (SHM) - is biased by hotspot motifs, which violates important assumptions in most phylogenetic substitution models. Here, we develop a modified GY94-type substitution model that partially accounts for this context-dependency while preserving independence of sites during calculation. This model shows a substantially better fit to three well-characterized bNAb lineages than the standard GY94 model. We show through simulations that accounting for hotspot motifs can lead to reduced bias of other substitution parameters, and more accurate ancestral state reconstructions. We also demonstrate how our model can be used to test hypotheses concerning the roles of different hotspot and coldspot motifs in the evolution of B-cell lineages. Further, we explore the consequences of the idea that the number of hotspot motifs - and perhaps the mutation rate in general - is expected to decay over time in individual bNAb lineages.

Evolutionary Biology↗

bioRxiv2016

Quantifying the evolutionary potential and constraints of a drug-targeted viral protein

RNA viruses are notorious for their ability to evolve rapidly under selection in novel environments. It is known that the high mutation rate of RNA viruses can generate huge genetic diversity to facilitate viral adaptation. However, less attention has been paid to the underlying fitness landscape that represents the selection forces on viral genomes. Here we systematically quantified the distribution of fitness effects (DFE) of about 1,600 single amino acid substitutions in the drug-targeted region of NS5A protein of Hepatitis C Virus (HCV). We found that the majority of non-synonymous substitutions incur large fitness costs, suggesting that NS5A protein is highly optimized in natural conditions. We characterized the adaptive potential of HCV by subjecting the mutant viruses to selection by the antiviral drug Daclatasvir. Both the selection coefficient and the number of beneficial mutations are found to increase with the level of environmental stress, which is modulated by the concentration of Daclatasvir. The changes in the spectrum of beneficial mutations in NS5A protein can be explained by a pharmacodynamics model describing viral fitness as a function of drug concentration. We test theoretical predictions regarding the distribution of beneficial fitness effects of mutations. We also interpret the data in the context of Fishers Geometric Model and find an increased distance to optimum as a function of environmental stress. Finally, we show that replication fitness of viruses is correlated with the pattern of sequence conservation in nature and viral evolution is constrained by the need to maintain protein stability.

Evolutionary Biology↗

bioRxiv2016

Accuracy of demographic inferences from Site Frequency Spectrum: The case of the Yoruba population

Some methods for demographic inference based on the observed genetic diversity of current populations rely on the use of summary statistics such as the Site Frequency Spectrum (SFS). Demographic models can be either model-constrained with numerous parameters such as growth rates, timing of demographic events and migration rates, or model-flexible, with an unbounded collection of piecewise constant sizes. It is still debated whether demographic histories can be accurately inferred based on the SFS. Here we illustrate this theoretical issue on an example of demographic inference for an African population. The SFS of the Yoruba population (data from the 1000 Genomes Project) is fit to a simple model of population growth described with a single parameter (e.g., founding time). We infer a time to the most recent common ancestor of 1.7 million years for this population. However, we show that the Yoruba SFS is not informative enough to discriminate between several different models of growth. We also show that for such simple demographies, the fit of one-parameter models outperforms the model-flexible method recently developed by Liu and Fu. The use of this method on simulated data suggests that it is biased by the noise intrinsically present in the data.

Evolutionary Biology↗

bioRxiv2016

Combining phenotypic and genomic approaches reveals no evidence for adaptation to the local mutualist in Medicago lupulina

Local adaptation is a common but not ubiquitous feature of species interactions, and understanding the circumstances under which it evolves illuminates the factors that influence adaptive population divergence. Antagonistic species interactions dominate the local adaptation literature relative to mutualistic ones, preventing an overall assessment of adaptation within interspecific interactions. Here, we tested whether the legume Medicago lupulina is adapted to the locally abundant species of mutualistic nitrogen-fixing bacteria (\"rhizobia\"), which vary in frequency across its eastern North American range. We reciprocally inoculated northern and southern M. lupulina genotypes with the northern (Ensifer medicae) or southern bacterium (E. meliloti) in a greenhouse experiment. Neither northern nor southern plants produced more seed flowered earlier, or were more likely to flower when inoculated with their local rhizobium species, although plants produced more root nodules (the structures that house the bacteria) wit their local rhizobia. We used a pre-existing dataset to perform a genome scan for loci that showed elevated differentiation between field-collected plants that hosted different bacteria. None of the loci we identified belonged to the well-characterized suite of legume-rhizobia symbiosis genes, suggesting that the rhizobia do not drive genetic divergence between M. lupulina populations. Our results demonstrate that symbiont local adaptation is weak in this mutualism despite large-scale geographic variation in the identity of the interacting species.

Evolutionary Biology↗

bioRxiv2016

Determining the role of inflammation in the selection of JAK2 mutant cells in myeloproliferative neoplasms

Myeloproliferative neoplasm (MPN) is a hematologic malignancy characterized by the clonal outgrowth of hematopoietic cells with a somatically acquired mutation most commonly in JAK2 (JAK2V 617F). This mutation endows upon myeloid progenitors cytokine independent growth and consequently leads to excessive production of myeloid lineage cells. It has been previously suggested that inflammation may play a role in the clonal evolution of JAK2V 617F mutants. In particular, it is possible that one or more cellular kinetic parameters of hematopoietic stem cells (HSCs) are affected by inflammation, such as division or death rates of cells, and the probability of HSC differentiation. This suggests a mechanism that can steer the outcome of the cellular competition in favor of the mutants, initiating the disease. In this paper we create a number of mathematical evolutionary models, from very abstract to more concrete, that describe cellular competition in the context of inflammation. It is possible to build a model axiomatically, where only very general assumptions are imposed on the modeling components and no arbitrary (and generally unknown) functional forms are used, and still generate a set of testable predictions. In particular, we show that, if HSC death is negligible, the evolutionary advantage of mutant cells can only be conferred by an increase in differentiation probability of HSCs in the presence of inflammation, and if death plays a significant role in the dynamics, an additional mechanism may be an increase of HSCs division-to-death ratio in the presence of inflammation. Further, we show that in the presence of inflammation, the wild type cell population is predicted to shrink under inflammation (even in the absence of mutants). Finally, it turns out that if only the differentiation probability is affected by the inflammation, then the resulting steady state population of wild type cells will contain a relatively smaller percentage of HSCs under inflammation. If the division-to-death rate is also affected, then the percentage of HSCs under inflammation can either decrease or increase, depending on other parameters.

Evolutionary Biology↗

bioRxiv2016

The non-stationary dynamics of fitness distributions: asexual model with epistasis and standing variation.

Various models describe asexual evolution by mutation, selection and drift. Some focus directly on fitness, typically modelling drift but ignoring or simplifying both epistasis and the distribution of mutation effects (travelling wave models). Others follow the dynamics of quantitative traits determining fitness (Fishers geometrical model), imposing a complex but fixed form of mutation effects and epistasis, and often ignoring drift. In all cases, predictions are typically obtained in high or low mutation rate limits and for long-term stationary regimes, thus loosing information on transient behaviors and the effect of initial conditions. Here, we connect fitness-based and trait-based models into a single framework, and seek explicit solutions even away from stationarity. The expected fitness distribution is followed over time via its cumulant generating function, using a deterministic approximation that neglects drift. In several cases, explicit trajectories for the full fitness distribution are obtained, for arbitrary mutation rates and standing variance. For non-epistatic mutation, especially with beneficial mutations, this approximation fails over the long term but captures the early dynamics, thus complementing stationary stochastic predictions. The approximation also handles several diminishing return epistasis models (e.g. with an optimal genotype): it can then apply at and away from equilibrium. General results arise at equilibrium, where fitness distributions display a phase transition with mutation rate. Beyond this phase transition, in Fishers geometrical model, the full trajectory of fitness and trait distributions takes simple form, robust to details of the mutant phenotype distribution. Analytical arguments are explored for why and when the deterministic approximation applies.\n\nSignificance statementHow fast do asexuals evolve in new environments? Asexual fitness dynamics are well documented empirically. Various corresponding theories exist, to which they may be compared, but most typically describe stationary regimes, thus losing information on the shorter timescale of experiments, and on the impact of the initial conditions set by the experimenter. Here, a general deterministic approximation is proposed that encompasses many previous models as subcases, and shows surprising accuracy when compared to stochastic simulations. It can yield predictions over both short and long timescales, hopefully fostering the quantitative test of alternative models, using data from experimental evolution in asexuals.

Evolutionary Biology↗