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bioRxiv2015

Variability in group size and the evolution of collective action

Models of the evolution of collective action typically assume that interactions occur in groups of identical size. In contrast, social interactions between animals occur in groups of widely dispersed size. This article models collective action problems as two-strategy multiplayer games and studies the effect of variability in group size on the evolution of cooperative behavior under the replicator dynamics. The analysis identifies elementary conditions on the payoff structure of the game implying that the evolution of cooperative behavior is promoted or inhibited when the group size experienced by a focal player is more or less variable. Similar but more stringent conditions are applicable when the confounding effect of size-biased sampling, which causes the group-size distribution experienced by a focal player to differ from the statistical distribution of group sizes, is taken into account.

Evolutionary Biology↗

bioRxiv2015

Ordering structured populations in multiplayer cooperation games

Spatial structure greatly affects the evolution of cooperation. While in two-player games the condition for cooperation to evolve depends on a single structure coefficient, in multiplayer games the condition might depend on several structure coefficients, making it difficult to compare different population structures. We propose a solution to this issue by introducing two simple ways of ordering population structures: the containment order and the volume order. If population structure [S]1 is greater than population structure [S]2 in the containment or the volume order, then [S]1 can be considered a stronger promoter of cooperation. We provide conditions for establishing the containment order, give general results on the volume order, and illustrate our theory by comparing different models of spatial games and associated update rules. Our results hold for a large class of population structures and can be easily applied to specific cases once the structure coefficients have been calculated or estimated.

Evolutionary Biology↗

bioRxiv2015

Adaptive evolution is substantially impeded by Hill-Robertson interference in Drosophila

It is known that rates of mutation and recombination vary across the genome in many species. Here we investigate whether these factors affect the rate at which genes undergo adaptive evolution both individually and in combination and quantify the degree to which Hill-Robertson interference (HRi) impedes the rate of adaptive evolution. To do this we compiled a dataset of 6,141 autosomal protein coding genes from Drosophila, for which we have polymorphism data from D. melanogaster and divergence out to D. yakuba. We estimated the rate of adaptive evolution using a derivative of the McDonald-Kreitman test that controls for the slightly deleterious mutations. We find that the rate of adaptive amino acid substitution is positively correlated to both the rates of recombination and mutation. We also find that these correlations are robust to controlling for each other, synonymous codon bias and gene functions related to immune response and testes. We estimate that HRi reduces the rate of adaptive evolution by [~]27%. We also show that this fraction depends on a genes mutation rate; genes with low mutation rates lose [~]11% of their adaptive substitutions while genes with high mutation rates lose [~]43%. In conclusion, we show that the mutation rate and the rate of recombination, are important modifiers of the rate of adaptive evolution in Drosophila.

Evolutionary Biology↗

bioRxiv2015

Life history evolution in response to changes in metapopulation structure in an arthropod herbivore

O_LIThe persistence and dynamics of populations largely depends on the way they are configured and integrated into space and the ensuing eco-evolutionary dynamics.\nC_LIO_LIWe manipulated spatial and temporal variation in patch size in replicated experimental metapopulations of the herbivore mite Tetranychus urticae and followed evolutionary dynamics over approximately 30 generations.\nC_LIO_LIA significant divergence in life history traits, physiological endpoints and gene expression was recorded in the spatially and spatiotemporally variable metapopulation, but also a remarkable convergence relative to the stable reference metapopulation in traits related to size and fecundity and in its transcriptional regulation.\nC_LIO_LIThe observed evolutionary dynamics are tightly linked to demographic changes, more specifically frequent episodes of resource shortage that increased the reproductive performance of mites on tomato, a challenging host plant. This points towards a general, adaptive stress response in stable spatial variable and spatiotemporal variable metapopulations that pre-adapts a herbivore arthropod to novel environmental stressors.\nC_LI

Evolutionary Biology↗

bioRxiv2015

SimPhy: Phylogenomic Simulation of Gene, Locus and Species Trees

We present here a fast and flexible software -SimPhy- for the simulation of multiple gene families evolving under incomplete lineage sorting, gene duplication and loss, horizontal gene transfer -all three potentially leading to the species tree/gene tree discordance- and gene conversion. SimPhy implements a hierarchical phylogenetic model in which the evolution of species, locus and gene trees is governed by global and local parameters (e.g., genome-wide, species-specific, locus-specific), that can be fixed or be sampled from a priori statistical distributions. SimPhy also incorporates comprehensive models of substitution rate variation among lineages (uncorrelated relaxed clocks) and the capability of simulating partitioned nucleotide, codon and protein multilocus sequence alignments under a plethora of substitution models using the program INDELible. We validate SimPhys output using theoretical expectations and other programs, and show that it scales extremely well with complex models and/or large trees, being an order of magnitude faster than the most similar program (DLCoal-Sim). In addition, we demonstrate how SimPhy can be useful to understand interactions among different evolutionary processes, conducting a simulation study to characterize the systematic overestimation of the duplication time when using standard reconciliation methods. SimPhy is available at https://github.com/adamallo/SimPhy, where users can find the source code, pre-compiled executables, a detailed manual and example cases.

Evolutionary Biology↗

bioRxiv2015

Accounting for genotype uncertainty in the estimation of allele frequencies in autopolyploids

Despite the increasing opportunity to collect large-scale data sets for population genomic analyses, the use of high throughput sequencing to study populations of polyploids has seen little application. This is due in large part to problems associated with determining allele copy number in the genotypes of polyploid individuals (allelic dosage uncertainty-ADU), which complicates the calculation of important quantities such as allele frequencies. Here we describe a statistical model to estimate biallelic SNP frequencies in a population of autopolyploids using high throughput sequencing data in the form of read counts. We bridge the gap from data collection (using restriction enzyme based techniques [e.g., GBS, RADseq]) to allele frequency estimation in a unified inferential framework using a hierarchical Bayesian model to sum over genotype uncertainty. Simulated data sets were generated under various conditions for tetraploid, hexaploid and octoploid populations to evaluate the models performance and to help guide the collection of empirical data. We also provide an implementation of our model in the R package O_SCPLOWPOLYFREQSC_SCPLOW and demonstrate its use with two example analyses that investigate (i) levels of expected and observed heterozygosity and (ii) model adequacy. Our simulations show that the number of individuals sampled from a population has a greater impact on estimation error than sequencing coverage. The example analyses also show that our model and software can be used to make inferences beyond the estimation of allele frequencies for autopolyploids by providing assessments of model adequacy and estimates of heterozygosity.

Evolutionary Biology↗

bioRxiv2015

How obstacles perturb population fronts and alter their genetic structure

As populations spread into new territory, environmental heterogeneities can shape the population front and genetic composition. We study here the effect of one important building block of inhomogeneous environments, compact obstacles. With a combination of experiments, theory, and simulation, we show how isolated obstacles both create long-lived distortions of the front shape and amplify the effect of genetic drift. A system of bacteriophage T7 spreading on a spatially heterogeneous Escherichia coli lawn serves as an experimental model system to study population expansions. Using an inkjet printer, we create well-defined replicates of the lawn and quantitatively study the population expansion manifested in plaque growth. The transient perturbations of the plaque boundary found in the experiments are well described by a model in which the front moves with constant speed. Independent of the precise details of the expansion, we show that obstacles create a kink in the front that persists over large distances and is insensitive to the details of the obstacle's shape. The small deviations between experimental findings and the predictions of the constant speed model can be understood with a more general reaction-diffusion model, which reduces to the constant speed model when the obstacle size is large compared to the front width. Using this framework, we demonstrate that frontier alleles that just graze the side of an isolated obstacle increase in abundance, a phenomenon we call 'geometry-enhanced genetic drift', complementary to the founder effect associated with spatial bottlenecks. Bacterial range expansions around nutrient-poor barriers and stochastic simulations confirm this prediction, the latter highlight as well the effect of the obstacle on the genealogy of individuals at the front. We argue that related ideas and experimental techniques are applicable to a wide variety of more complex environments, leading to a better understanding of how environmental heterogeneities affect population range expansions.

Evolutionary Biology↗

bioRxiv2015

How competition governs whether moderate or aggressive treatment minimizes antibiotic resistance

The growing burden of antimicrobial resistance is one of the most challenging problems facing public health today, and understanding how our approaches for using antimicrobial drugs shapes future levels of resistance is crucial. Recently there has been debate over whether an aggressive (i.e. high dose) or more moderate (i.e. lower dose) treatment of individuals will most limit the emergence and spread of resistant bacteria. Here we demonstrate how one can understand and resolve these apparently contradictory conclusions. We show that a key determinant of which treatment strategy will perform best at the individual level is the extent of effective competition between resistant and sensitive pathogens within a host. We extend our analysis to the community level, exploring the spectrum between strict inter-strain competition and strain independence. From this perspective as well, we find that the magnitude of effective competition between resistant and sensitive strains determines whether an aggressive approach or moderate approach minimizes the burden of resistance in the population.

Evolutionary Biology↗

bioRxiv2015

Flawed evidence for convergent evolution of the circadian CLOCK gene in mole-rats

Convergently evolved mole-rats (Mammalia, Rodentia) provide a fascinating model for studying convergent molecular evolution. Three genome sequences have recently been made available for the blind mole-rat (Nannospalax galili; Spalacidae; Muroidea)1, and the convergently evolved naked mole-rat (Heterocephalus glaber; Heterocephalidae; Ctenohystrica)2 and its close relative the Damaraland mole-rat (Fukomys damarensis; Bathyergidae; Ctenohystrica)3. In their genome paper1, Fang et al. evaluated convergent molecular evolution related to the subterranean life-style between the naked mole-rat and the blind mole-rat. One particularly striking result was the strong signal for amino acid convergence detected in the circadian rhythm CLOCK gene. Here I show that this unexpected result is erroneous because it is based on the use of the wrong sequence for the naked mole-rat, which has been mistakenly replaced by a sequence from a blind mole-rat. When the correct sequence is used, the evidence for convergent molecular evolution in this gene appears very limited.

Evolutionary Biology↗

bioRxiv2015

Computing the Internode Certainty and related measures from partial gene trees.

We present, implement, and evaluate an approach to calculate the internode certainty and tree certainty on a given reference tree from a collection of partial gene trees. Previously, the calculation of these values was only possible from a collection of gene trees with exactly the same taxon set as the reference tree. An application to sets of partial gene trees requires mathematical corrections in the internode certainty and tree certainty calculations. We implement our methods in RAxML and test them on empirical data sets. These tests imply that the inclusion of partial trees does matter. However, in order to provide meaningful measurements, any data set should also include trees containing the full species set.

Evolutionary Biology↗

bioRxiv2015

Structure and evolutionary history of a large family of NLR proteins in the zebrafish

NACHT- and Leucine-Rich-Repeat-containing domain (NLR) proteins act as cytoplasmic sensors for pathogen- and danger-associated molecular patterns and are found throughout the plant and animal kingdoms. In addition to having a small set of conserved NLRs, the genomes in some animal lineages contain massive expansions of this gene family. One of these arose in fishes, after the creation of a gene fusion that combined the core NLR domains with another domain used for immune recognition, the PRY/SPRY or B30.2 domain. We have analysed the expanded NLR gene family in zebrafish, which contains 368 genes, and studied its evolutionary history. The encoded proteins share a defining overall structure, but individual domains show different evolutionary trajectories. Our results suggest gene conversion homogenizes NACHT and B30.2 domain sequences among different gene subfamilies, however, the functional implications of its action remains unclear. The majority of the genes are located on the long arm of chromosome 4, interspersed with several other large multi-gene families, including a new family encoding proteins with multiple tandem arrays of Zinc fingers. This suggests that chromosome 4 may be a hotspot for rapid evolutionary change in zebrafish.

Evolutionary Biology↗

bioRxiv2015

How competition affects evolutionary rescue

Populations facing novel environments can persist by adapting. In nature, the ability to adapt and persist will depend on interactions between coexisting individuals. Here we use an adaptive dynamic model to assess how the potential for evolutionary rescue is affected by intra- and interspecific competition. Intraspecific competition (negative density-dependence) lowers abundance, which decreases the supply rate of beneficial mutations, hindering evolutionary rescue. On the other hand, interspecific competition can aid evolutionary rescue when it speeds adaptation by increasing the strength of selection. Our results clarify this point and give an additional requirement: competition must increase selection pressure enough to overcome the negative effect of reduced abundance. We therefore expect evolutionary rescue to be most likely in communities which facilitate rapid niche displacement. Our model, which aligns to previous quantitative and population genetic models in the absence of competition, provides a first analysis of when competitors should help or hinder evolutionary rescue.

Evolutionary Biology↗

bioRxiv2015

Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

While eukaryotic and archaean genomes encode the histone fold domain, only eukaryotes encode the core histones H2A, H2B, H3, and H4. Core histones assemble into a hetero-octamer rather than the homo-tetramer of Archaea. Thus it was unexpected that core histone \"doublets\" were identified in the cytoplasmic replication factories of the Marseilleviridae (MV), one family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV). Here we analyze the core histone doublet genes from all known Marseilleviridae genomes and show that they encode obligate H2B-H2A and H4-H3 dimers of likely proto-eukaryotic origin. Each MV core histone moiety forms a sister clade to a eukaryotic core histone clade inclusive of canonical core histone paralogs, suggesting that MV core histone moieties diverged prior to eukaryotic neofunctionalizations associated with paired linear chromosomes and variant histone octamer assembly. We also show that all MV genomes encode a eukaryote-like DNA topoisomerase II enzyme that forms a clade that is sister to the eukaryotic clade. As DNA topo II influences histone deposition and chromatin compaction and is the second most abundant nuclear protein after histones, we suggest MV genes underlie a proto-chromatinized replisome that diverged prior to diversification of eukaryotic core histone variants. Thus, combined domain architecture and phylogenomic analyses suggest that a primitive origin for MV chromatin genes is a more parsimonious explanation than horizontal gene transfers + gene fusions + long-branch attraction constrained to each core histone clade. These results imply that core histones were utilized ancestrally in viral DNA compaction, protection from host endonucleases, and/or other unknown processes associated with NCLDV-like progenitors.

Evolutionary Biology↗

bioRxiv2015

Coevolution of male and female reproductive traits drive cascading reinforcement in Drosophila yakuba

When the ranges of two hybridizing species overlap, individuals may waste gametes on inviable or infertile hybrids. In these cases, selection against maladaptive hybridization can lead to the evolution of enhanced reproductive isolation in a process called reinforcement. On the slopes of the African island of Sao Tome, Drosophila yakuba and its endemic sister species D. santomea have a well-defined hybrid zone. Drosophila yakuba females from within this zone show increased postmating-prezygotic isolation towards D. santomea males when compared with D. yakuba females from allopatric populations. To understand why reinforced gametic isolation is confined to areas of secondary contact and has not spread throughout the entire D. yakuba geographic range, we studied the costs of reinforcement in D. yakuba using a combination of natural collections and experimental evolution. We found that D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results suggest that the correlated evolution of male and female reproductive traits in sympatric D. yakuba have associated costs (i.e., reduced male fertility) that prevent the alleles responsible for enhanced isolation from spreading outside the hybrid zone.

Evolutionary Biology↗

bioRxiv2015

Inference of super-exponential human population growth via efficient computation of the site frequency spectrum for generalized models

The site frequency spectrum (SFS) and other genetic summary statistics are at the heart of many population genetics studies. Previous studies have shown that human populations had undergone a recent epoch of fast growth in effective population size. These studies assumed that growth is exponential, and the ensuing models leave unexplained excess amount of extremely rare variants. This suggests that human populations might have experienced a recent growth with speed faster than exponential. Recent studies have introduced a generalized growth model where the growth speed can be faster or slower than exponential. However, only simulation approaches were available for obtaining summary statistics under such models. In this study, we provide expressions to accurately and efficiently evaluate the SFS and other summary statistics under generalized models, which we further implement in a publicly available software. Investigating the power to infer deviation of growth from being exponential, we observed that decent sample sizes facilitate accurate inference, e.g. a sample of 3000 individuals with the amount of data expected from exome sequencing allows observing and accurately estimating growth with speed deviating by 10% or more from that of exponential. Applying our inference framework to data from the NHLBI Exome Sequencing Project, we found that a model with a generalized growth epoch fits the observed SFS significantly better than the equivalent model with exponential growth (p-value = 3.85 x 10-6). The estimated growth speed significantly deviates from exponential (p-value << 10-12), with the best-fit estimate being of growth speed 12% faster than exponential.

Evolutionary Biology↗

bioRxiv2015

Predicting microbial relative growth in a mixed culture from growth curve data

Estimates of microbial fitness from growth curves are inaccurate. Rather, competition experiments are necessary for accurate estimation. But competition experiments require unique markers and are difficult to perform with isolates derived from a common ancestor or non-model organisms. Here we describe a new approach for predicting relative growth of microbes in a mixed culture utilizing mono- and mixed culture growth curve data. We validated this approach using growth curve and competition experiments with E. coli. Our approach provides an effective way to predict growth in a mixed culture and infer relative fitness. Furthermore, by integrating several growth phases, it provides an ecological interpretation for microbial fitness.

Evolutionary Biology↗

bioRxiv2015

Monoallelic methylation and allele specific expression in a social insect

The social hymenoptera are emerging as models for epigenetics. DNA methylation, the addition of a methyl group, is a common epigenetic marker. In mammals and flowering plants methylation affects allele specific expression. There is contradictory evidence for the role of methylation on allele specific expression in social insects. The aim of this paper is to investigate allele specific expression and monoallelic methylation in the bumblebee, Bombus terrestris. We found nineteen genes that were both monoallelically methylated and monoallelically expressed in a single bee. Fourteen of these genes express the hypermethylated allele, while the other five express the hypomethylated allele. We also searched for allele specific expression in twenty-nine published RNA-seq libraries. We found 555 loci with allele-specific expression. We discuss our results with reference to the functional role of methylation in gene expression in insects and in the, as yet unquantified, role of genetic cis effects in insect allele specific methylation and expression.

Evolutionary Biology↗

bioRxiv2015

Adaptive variation in human toll-like receptors is contributed by introgression from both Neandertals and Denisovans

Pathogens and the diseases they cause have been among the most important selective forces experienced by humans during their evolutionary history. Although adaptive alleles generally arise by mutation, introgression can also be a valuable source of beneficial alleles. Archaic humans, who lived in Europe and Western Asia for over 200,000 years, were likely well-adapted to the environment and its local pathogens, and it is therefore conceivable that modern humans entering Europe and Western Asia who admixed with them obtained a substantial immune advantage from the introgression of archaic alleles.\n\nHere we document a cluster of three toll-like receptors (TLR6-TLR1-TLR10) in modern humans that carries three distinct archaic haplotypes, indicating repeated introgression from archaic humans. Two of these haplotypes are most similar to Neandertal genome, while the third haplotype is most similar to the Denisovan genome. The toll-like receptors are key components of innate immunity and provide an important first line of immune defense against bacteria, fungi and parasites. The unusually high allele frequencies and unexpected levels of population differentiation indicate that there has been local positive selection on multiple haplotypes at this locus. We show that the introgressed alleles have clear functional effects in modern humans; archaic-like alleles underlie differences in the expression of the TLR genes and are associated with reduced microbial resistance and increased allergic disease in large cohorts. This provides strong evidence for recurrent adaptive introgression at the TLR6-TLR1-TLR10 locus, resulting in differences in disease phenotypes in modern humans.

Evolutionary Biology↗