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bioRxiv2016

Predicting the stability of homologous gene duplications in a plant RNA virus

One of the striking features of many eukaryotes is the apparent amount of redundancy in coding and non-coding elements of their genomes. Despite the possible evolutionary advantages, there are fewer examples of redundant sequences in viral genomes, particularly those with RNA genomes. The low prevalence of gene duplication in RNA viruses most likely reflects the strong selective constraints against increasing genome size. Here we investigated the stability of genetically redundant sequences and how adaptive evolution proceeds to remove them. We generated plant RNA viruses with potentially beneficial gene duplications, measured their fitness and performed experimental evolution, hereby exploring their genomic stability and evolutionary potential. We found that all gene duplication events resulted in a loss of viability or significant reductions in fitness. Moreover, upon evolving the viable viruses and analyzing their genomes, we always observed the deletion of the duplicated gene copy and maintenance of the ancestral copy. Interestingly, there were clear differences in the deletion dynamics of the duplicated gene associated with the passage duration, the size of the gene and the position for duplication. Based on the experimental data, we developed a mathematical model to characterize the stability of genetically redundant sequences, and showed that the fitness of viruses with duplications is not enough information to predict genomic stability as a recombination rate dependent on the genetic context - the duplicated gene and its position - is also required. Our results therefore demonstrate experimentally the deleterious nature of gene duplications in RNA viruses, and we identify factors that constrain the maintenance of duplicated genes.

Evolutionary Biology↗

bioRxiv2016

Coevolutionary Dynamics of Costly Bonding Ritual and Altruism

While altruistic behavior and bonding in altruistic pairs or groups of cooperators is observed throughout the animal kingdom, the genetic evolution of such is on an ongoing source of debate, curiosity, and conflict in the behavioral sciences. Many such bonded groups and pairs are observed to take part in costly ritualized movement behavior that is hypothesized to trigger or maintain altruistic sentiments amongst the participants. Such costly ritualized practices could have evolved if they engaged pre-existing behavioral instincts that manifest as altruism in the new context of ritual bonding. While this seems at first to be a Green Beard hypothesis ( marker (ie., green beard) as honest signal of altruistic intent', an hypothesis well-known to be problematic), it is distinct in two important ways. First, the ritual as marker is costly, and second the ritual engages a pre-existing behavioral potential caused by genes which, importantly, have some other benefit. This paper models the genetic coevolutionary dynamics both analytically and through simulation. It finds that such coevolution can lead to fixation of altruism in a population or to cycling of altruism in the population, depending on the balance of costs and benefits. Where cycling occurs, even though altruism is consistently present in the population, population mean fitness declines with the introduction of these bonding rituals.

Evolutionary Biology↗

bioRxiv2016

Gene-Culture Coevolution of Prosocial Rituals

It has been argued that costly socially learned rituals have the potential to generate prosocial emotional responses arising from genetically based behavioral dispositions, hijacking these behavioral dispositions to solve otherwise intractable cooperation problems. An example is the innovation of synchronous movement rituals which seem to engage the same altruistic response as instinctual mimicry. Arguments against this hypothesis are based in the idea that cheap markers of altruistic intent (\"Green Beards\")are vulnerable to manipulation from non-cooperating free-riders that are similarly marked. This paper formally models the gene-culture coevolutionary dynamics of a system in which a costly socially learned ritual practice coevolves with the genes underpinning the prosocial response. This takes a genetic mismatch hypothesis (where fast evolution of socially learned behaviors create a temporary mismatch with the coevolving genes, which take longer to evolve to equilibrium) and models it dynamically. The genetic and cultural fitness equations are first analyzed for equilibrium and then simulations are used to predicting trajectories for both the socially learned behavior and the hijacked genetic trait over time. Relying on fast culture and slow genes, it demonstrates how high levels of ritual efficacy may be established, at least temporarily, through gene culture interaction. It also shows how longer term feedbacks on the genes from culture may lead to decreases in the prosocial gene in the population and reduced overall population mean fitness, despite high levels of altruism in the population.

Evolutionary Biology↗

bioRxiv2016

Immunoecology of species with alternative reproductive tactics and strategies

Alternative reproductive tactics and strategies (ARTS) refer to polymorphic reproductive behaviours in which in addition to the usual two sexes, there are one or more alternative morphs, usually male, that have evolved the ability to circumvent direct intra-sexual competition. Each morph has its own morphological, ecological, developmental, behavioural, life-history, and physiological profile that shifts the balance between reproduction and self-maintenance, one aspect being immunity. Immunoecological work on species with ARTS, which is the topic of this review, is particularly interesting because the alternative morphs make it possible to separate the effects of sex, per se, from other factors that in other species are inextricably linked with sex. We first summarize the evolution, development and maintenance of ARTS. We then review immunoecological hypotheses relevant to species with ARTS, dividing them into physiological, life-history, and ecological hypotheses. In context of these hypotheses, we critically review in detail all immunoecological studies we could find on species with ARTS. Several interesting patterns emerge. Oddly, there is a paucity of studies on insects, despite the many benefits that arise from working with insects: larger sample sizes, simple immune systems, and countless forms of alternative reproductive strategies and tactics. Of all the hypotheses considered, the immunocompetence handicap hypothesis has generated the greatest amount of work, but not necessarily the greatest level of understanding. Unfortunately, it is often used as a general guiding principle rather than a source of explicitly articulated predictions. Other hypotheses are usually considered a posteriori, but it is perhaps time that they take centre stage. Whereas blanket concepts such as "immunocompetence" and "androgens" might useful to develop a rationale, predictions need to be far more explicitly articulated. Integration so far has been a one-way street, with ecologists delving deeper into physiology, seemingly at the cost of ignoring their organisms evolutionary history and ecology. One possible useful framework is to divide ecological and evolutionary factors affecting immunity into those that stimulate the immune system, and those that depress it. Finally, the contributions of genomics to ecology are being increasingly recognized, including in species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort, as there is no grandeur in the strict reductionist view of life.

Evolutionary Biology↗

bioRxiv2016

Inference of distribution of fitness effects and proportion of adaptive substitutions from polymorphism data

The distribution of fitness effects (DFE) encompasses deleterious, neutral and beneficial mutations. It conditions the evolutionary trajectory of populations, as well as the rate of adaptive molecular evolution (). Inference of DFE and from patterns of polymorphism (SFS) and divergence data has been a longstanding goal of evolutionary genetics. A widespread assumption shared by numerous methods developed so far to infer DFE and from such data is that beneficial mutations contribute only negligibly to the polymorphism data. Hence, a DFE comprising only deleterious mutations tends to be estimated from SFS data, and is only predicted by contrasting the SFS with divergence data from an outgroup. Here, we develop a hierarchical probabilistic framework that extends on previous methods and also can infer DFE and from polymorphism data alone. We use extensive simulations to examine the performance of our method. We show that both a full DFE, comprising both deleterious and beneficial mutations, and can be inferred without resorting to divergence data. We demonstrate that inference of DFE from polymorphism data alone can in fact provide more reliable estimates, as it does not rely on strong assumptions about a shared DFE between the outgroup and ingroup species used to obtain the SFS and divergence data. We also show that not accounting for the contribution of beneficial mutations to polymorphism data leads to substantially biased estimates of the DFE and . We illustrate these points using our newly developed framework, while also comparing to one of the most widely used inference methods available.

Evolutionary Biology↗

bioRxiv2016

With a little help from my friends: Cooperation can accelerate crossing of adaptive valleys

Natural selection favors changes that lead to genotypes possessing high fitness. A conflict arises when several mutations are required for adaptation, but each mutation is separately deleterious. The process of a population evolving from a genotype encoding for a local fitness maximum to a higher fitness genotype is termed an adaptive peak shift.\n\nHere we suggest cooperative behavior as a factor that can facilitate adaptive peak shifts. We model cooperation in a public goods scenario, wherein each individual contributes resources that are later equally redistributed among all cooperating individuals. We use mathematical modeling and stochastic simulations to study the effect of cooperation on peak shifts in well-mixed populations and structured ones. Our results show that cooperation can accelerate the rate of complex adaptation. Furthermore, we show that cooperation increases the population diversity throughout the peak shift process, thus increasing the robustness of the population to drastic environmental changes.\n\nOur work could help explain adaptive valley crossing in natural populations and suggest that the long term evolution of a species depends on its social behavior.

Evolutionary Biology↗

bioRxiv2016

Chaotic provinces in the kingdom of the Red Queen

The interplay between parasites and their hosts is found in all kinds of species and plays an important role in understanding the principles of evolution and coevolution. Usually, the different genotypes of hosts and parasites oscillate in their abundances. The well-established theory of oscillatory Red Queen dynamics proposes an ongoing change in frequencies of the different types within each species. So far, it is unclear in which way Red Queen dynamics persists with more than two types of hosts and parasites. In our analysis, an arbitrary number of types within two species are examined in a deterministic framework with constant or changing population size. This general framework allows for analytical solutions for internal fixed points and their stability. For more than two species, apparently chaotic dynamics has been reported. Here we show that even for two species, once more than two types are considered per species, irregular dynamics in their frequencies can be observed in the long run. The nature of the dynamics depends strongly on the initial configuration of the system; the usual regular Red Queen oscillations are only observed in some parts of the parameter region.

Evolutionary Biology↗

bioRxiv2016

Should tissue structure suppress or amplify selection to minimize cancer risk?

BackgroundIt has been frequently argued that tissues evolved to suppress the accumulation of growth enhancing cancer inducing mutations. A prominent example is the hierarchical structure of tissues with high cell turnover, where a small number of tissue specific stem cells produces a large number of specialised progeny during multiple differentiation steps. Another well known mechanism is the spatial organisation of stem cell populations and it is thought that this organisation suppresses fitness enhancing mutations. However, in small populations the suppression of advantageous mutations typically also implies an increased accumulation of deleterious mutations. Thus, it becomes an important question whether the suppression of potentially few advantageous mutations outweighs the combined effects of many deleterious mutations.\n\nResultsWe argue that the distribution of mutant fitness effects, e.g. the probability to hit a strong driver compared to many deleterious mutations, is crucial for the optimal organisation of a cancer suppressing tissue architecture and should be taken into account in arguments for the evolution of such tissues.\n\nConclusionWe show that for systems that are composed of few cells reflecting the typical organisation of a stem cell niche, amplification or suppression of selection can arise from subtle changes in the architecture. Moreover, we discuss special tissue structures that can suppress most types of non-neutral mutations simultaneously.

Evolutionary Biology↗

bioRxiv2016

The evolution of no-cost resistance at sub-MIC concentrations of streptomycin in Streptomyces coelicolor

At the high concentrations used in medicine, antibiotics exert strong selection on bacterial populations for the evolution of resistance. However, these lethal concentrations may not be representative of the concentrations bacteria face in soil, a recognition that has lead to questions of the role of antibiotics in soil environments as well as the dynamics of resistance evolution during sub-lethal challenge. Here we examine the evolution of resistance to sub-MIC concentrations of streptomycin in the filamentous soil bacterium Streptomyces coelicolor. First, we show that spontaneous resistance to streptomycin causes an average fitness deficit of ~21% in the absence of drugs; however, these costs are eliminated at concentrations as low as 1/10 the MIC of susceptible strains. Using experimental evolution, we next show that resistance readily evolves at these non-lethal doses. More important, S. coelicolor resistance that evolves at sub-MIC streptomycin is cost-free. Whole-genome analyses reveal that sub-MIC evolved clones fix a distinct set of mutations to those isolated at high drug concentrations. Our results broaden the conditions under which resistance can evolve in nature and suggest that the long-term persistence of these strains is facilitated by the absence of pleiotropic fitness costs. Finally, our data cast doubt on arguments that low-concentration antibiotics in nature are signals, instead supporting models that resistance evolves in response to antibiotics used as weapons.

Evolutionary Biology↗

bioRxiv2016

The evolution of DNA methylation and its relationship to sociality in insects

DNA methylation contributes to gene and transcriptional regulation in eukaryotes, and therefore has been hypothesized to facilitate the evolution of flexible traits such as sociality in insects. However, DNA methylation is sparsely studied in insects. Therefore, we documented patterns of DNA methylation across a wide diversity of insects. Furthermore, we tested the hypothesis that the DNA methylation system will be associated with presence/absence of sociality among insects. We also predicted that underlying enzymatic machinery is concordant with patterns of DNA methylation. We found DNA methylation to be widespread, detected in all orders examined except Diptera (flies). Whole genome bisulfite sequencing showed that orders differed in levels of DNA methylation. Hymenopteran (ants, bees, wasps and sawflies) had some of the lowest levels, including several potential losses. Blattodea (cockroaches) show all possible patterns, including a potential loss of DNA methylation in a eusocial species whereas solitary species had the highest levels. Phylogenetically corrected comparisons revealed no evidence that supports evolutionary dependency between sociality and DNA methylation. Species with DNA methylation do not always possess the typical enzymatic machinery. We identified a gene duplication event in the maintenance DNA methyltransferase 1 (DNMT1) that is shared by some hymenopteran, and paralogs have experienced divergent, non-neutral evolution. This diversity and non-neutral evolution of underlying machinery suggests alternative DNA methylation pathways may exist. Altogether, DNA methylation is highly variable in insects and is not a universal driver of social behavior. Future, functional studies are required to advance our understanding of DNA methylation in insects.

Evolutionary Biology↗

bioRxiv2016

Steady at the wheel: conservative sex and the benefits of bacterial transformation

Many bacteria are highly sexual, but the reasons for their promiscuity remain obscure. Did bacterial sex evolve to maximize diversity and facilitate adaptation in a changing world, or does it instead help to retain the bacterial functions that work right now? In other words, is bacterial sex innovative or conservative? Our aim in this review is to integrate experimental, bioinformatic and theoretical studies to critically evaluate these alternatives, with a main focus on natural genetic transformation, the bacterial equivalent of eukaryotic sexual reproduction. First, we provide a general overview of several hypotheses that have been put forward to explain the evolution of transformation. Next, we synthesize a large body of evidence highlighting the numerous passive and active barriers to transformation that have evolved to protect bacteria from foreign DNA, thereby increasing the likelihood that transformation takes place among clonemates. Our critical review of the existing literature provides support for the view that bacterial transformation is maintained as a means of genomic conservation that provides direct benefits to both individual bacterial cells and to transformable bacterial populations. We examine the generality of this view across bacteria and contrast this explanation with the different evolutionary roles proposed to maintain sex in eukaryotes.

Evolutionary Biology↗

bioRxiv2016

Manipulating virulence factor availability can have complex consequences for infections

Given the rise of bacterial resistance against antibiotics, we urgently need alternative strategies to fight infections. Some propose we should disarm rather than kill bacteria, through targeted disruption of their virulence factors. It is assumed that this approach (i) induces weak selection for resistance because it should only minimally impact bacterial fitness, and (ii) is specific, only interfering with the virulence factor in question. Given that pathogenicity emerges from complex interactions between pathogens, hosts, and their environment, such assumptions may be unrealistic. To address this issue in a test case, we conducted experiments with the opportunistic human pathogen Pseudomonas aeruginosa, where we manipulated the availability of a virulence factor, the iron-scavenging pyoverdine, within the insect host Galleria mellonella. We observed that pyoverdine availability was not stringently predictive of virulence, and affected bacterial fitness in non-linear ways. We show that this complexity could partly arise because pyoverdine availability affects host responses and alters the expression of regulatorily linked virulence factors. Our results reveal that virulence-factor manipulation feeds back on pathogen and host behavior, which in turn affects virulence. Our findings highlight that realizing effective and evolutionarily robust anti-virulence therapies will ultimately require deeper engagement with the intrinsic complexity of host-pathogen systems.

Evolutionary Biology↗

bioRxiv2016

Evolution of mutation rates in rapidly adapting asexual populations

Mutator and antimutator alleles often arise and spread in both natural microbial populations and laboratory evolution experiments. The evolutionary dynamics of these mutation rate modifiers are determined by indirect selection on linked beneficial and deleterious mutations. These indirect selection pressures have been the focus of much earlier theoretical and empirical work, but we still have a limited analytical understanding of how the interplay between hitchhiking and deleterious load influences the fates of modifier alleles. Our understanding is particularly limited when clonal interference is common, which is the regime of primary interest in laboratory microbial evolution experiments. Here, we calculate the fixation probability of a mutator or antimutator allele in a rapidly adapting asexual population, and we show how this quantity depends on the population size, the beneficial and deleterious mutation rates, and the strength of a typical driver mutation. In the absence of deleterious mutations, we find that clonal interference enhances the fixation probability of mutators, even as they provide a diminishing benefit to the overall rate of adaptation. When deleterious mutations are included, natural selection pushes the population towards a stable mutation rate that can be suboptimal for the adaptation of the population as a whole. The approach to this stable mutation rate is not necessarily monotonic, and selection can favor mutator and antimutator alleles that overshoot the stable mutation rate by substantial amounts.

Evolutionary Biology↗

bioRxiv2016

Inbreeding parents should invest more resources in fewer offspring

Inbreeding increases parent-offspring relatedness and commonly reduces offspring viability, shaping selection on reproductive interactions involving relatives and associated parental investment (PI). Nevertheless, theories predicting selection for inbreeding versus inbreeding avoidance and selection for optimal PI have only been considered separately, precluding prediction of optimal PI and associated reproductive strategy given inbreeding. We unify inbreeding and PI theory, demonstrating that optimal PI increases when a female's inbreeding decreases the viability of her offspring. Inbreeding females should therefore produce fewer offspring due to the fundamental trade-off between offspring number and PI. Accordingly, selection for inbreeding versus inbreeding avoidance changes when females can adjust PI with the degree that they inbreed. In contrast, optimal PI does not depend on whether a focal female is herself inbred. However, inbreeding causes optimal PI to increase given strict monogamy and associated biparental investment compared to female-only investment. Our model implies that understanding evolutionary dynamics of inbreeding strategy, inbreeding depression, and PI requires joint consideration of the expression of each in relation to the other. Overall, we demonstrate that existing PI and inbreeding theories represent special cases of a more general theory, implying that intrinsic links between inbreeding and PI affect evolution of behaviour and intra-familial conflict.

Evolutionary Biology↗

bioRxiv2016

Competition between continuously evolving lineages in asexual populations

In an asexual population, the fate of a beneficial mutation depends on how its lineage competes against other mutant lineages in the population. With high beneficial mutation rates or large population sizes, competition between contending mutations is strong, and successful lineages can accumulate multiple mutations before any single one achieves fixation. Most current theory about asexual population dynamics either neglects this multiple-mutations regime or introduces simplifying assumptions that may not apply. Here, we develop a theoretical framework that describes the dynamics of adaptation and substitution over all mutation-rate regimes by conceptualizing the population as a collection of continuously adapting lineages. This model of \"lineage interference\" shows that each new mutants advantage over the rest of the population must be above a critical threshold in order to likely achieve fixation, and we derive a simple expression for that threshold. We apply this framework to examine the role of beneficial mutations with different effect sizes across the transition to the multiple-mutations regime.

Evolutionary Biology↗

bioRxiv2016

Past climate changes, population dynamics and the origin of Bison in Europe

Climatic and environmental fluctuations as well as anthropogenic pressure have led to the extinction of much of Europes megafauna. Here we show that the emblematic European bison has experienced several waves of population expansion, contraction and extinction during the last 50,000 years in Europe, culminating in a major reduction of genetic diversity during the Holocene. Fifty-seven complete and partial ancient mitogenomes from throughout Europe, the Caucausus and Siberia reveal that three populations of wisent (Bison bonasus) and steppe bison (B. priscus) alternated in Western Europe correlating with climate-induced environmental changes. The Late Pleistocene European steppe bison originated from northern Eurasia whereas the modern wisent population emerged from a refuge in the southern Caucasus after the last glacial maximum. A population overlap in a transition period is reflected in ca. 36,000 year-old paintings in the French Chauvet cave. Bayesian analyses of these complete ancient mitogenomes yielded new dates of the various branching events during the evolution of Bison and its radiation with Bos that lead us to propose that the genetic affiliation between the wisent and cattle mitogenomes result from incomplete lineage sorting rather than post-speciation gene flow.\n\nSignificanceClimatic fluctuations during the Pleistocene had a major impact on the environment and led to multiple megafaunal extinctions. Through ancient DNA analyses we decipher these processes for one of the largest megafauna of Eurasia, the bison. We show that Western Europe was successively populated during the Late Pleistocene by three different bison clades or species originating from the Caucasus and North-Eastern Europe that can be correlated to major climatic fluctuations and environmental changes. Aurignacian cave artists were witnesses to the first replacement of bison species ~35,000 years ago. All of these populations went extinct except for one that survived into the Holocene where it experienced severe reductions of its genetic diversity due to anthropogenic pressure.

Evolutionary Biology↗

bioRxiv2016

Differential paralog divergence modulates evolutionary outcomes in yeast

Evolutionary outcomes depend not only on the selective forces acting upon a species, but also on the genetic background. However, large timescales and uncertain historical selection pressures can make it difficult to discern such important background differences between species. Experimental evolution is one tool to compare evolutionary potential of known genotypes in a controlled environment. Here we utilized a highly reproducible evolutionary adaptation in Saccharomyces cerevisiae to investigate whether other yeast species would adopt similar evolutionary trajectories. We evolved populations of S. cerevisiae, S. paradoxus, S. mikatae, S. uvarum, and interspecific hybrids between S. uvarum and S. cerevisiae for ~200-500 generations in sulfate-limited continuous culture. Wild-type S. cerevisiae cultures invariably amplify the high affinity sulfate transporter gene, SUL1. However, while amplification of the SUL1 locus was detected in S. paradoxus and S. mikatae populations, S. uvarum cultures instead selected for amplification of the paralog, SUL2. We measured the relative fitness of strains bearing deletions and amplifications of both SUL genes from different species, confirming that, converse to S. cerevisiae, S. uvarum SUL2 contributes more to fitness in sulfate limitation than S. uvarum SUL1. By measuring the fitness and gene expression of chimeric promoter-ORF constructs, we were able to delineate the cause of this differential fitness effect primarily to the promoter of S. uvarum SUL1. Our data show evidence of differential sub-functionalization among the sulfur transporters across Saccharomyces species through recent changes in noncoding sequence. Furthermore, these results show a clear example of how such background differences due to paralog divergence can drive significant changes in evolutionary trajectories of eukaryotes.

Evolutionary Biology↗

bioRxiv2016

The combinatorics of discrete time-trees: theory and open problems

A time-tree is a rooted phylogenetic tree such that all internal nodes are equipped with absolute divergence dates and all leaf nodes are equipped with sampling dates. Such time-trees have become a central object of study in phylogenetics but little is known about the parameter space of such objects. Here we introduce and study a hierarchy of discrete approximations of the space of time-trees from the graph-theoretic and algorithmic point of view. One of the basic and widely used phylogenetic graphs, the NNI graph, is the roughest approximation and bottom level of our hierarchy. More refined approximations discretize the relative timing of evolutionary divergence and sampling dates. We study basic graph-theoretic questions for these graphs, including the size of neighborhoods, diameter upper and lower bounds, and the problem of finding shortest paths. We settle many of these questions by extending the concept of graph grammars introduced by Sleator, Tarjan, and Thurston to our graphs. Although time values greatly increase the number of possible trees, we show that 1-neighborhood sizes remain linear, allowing for efficient local exploration and construction of these graphs. We also obtain upper bounds on the r-neighborhood sizes of these graphs, including a smaller bound than was previously known for NNI.\n\nOur results open up a number of possible directions for theoretical investigation of graph-theoretic and algorithmic properties of the time-tree graphs. We discuss the directions that are most valuable for phylogenetic applications and give a list of prominent open problems for those applications. In particular, we conjecture that the split theorem applies to shortest paths in time-tree graphs, a property not shared in the general NNI case.

Evolutionary Biology↗