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Results for “Evolutionary Biology”

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bioRxiv2016

Tunable bet hedging in yeast responses to osmotic stress

Microbes limit risk by stochastic bet hedging - low frequency expression of less fit, slow growing cells constitutively preadapted against many stresses including antibiotics. By contrast, here we report continuous variation in the induced frequency of cells with slow osmotic stress signaling, survival and proliferation among 50 ecologically-distinct strains of budding yeast challenged by sudden hyperosmotic stress. Despite extensive variation in early mortality, strains displayed robust perfect adaptation and recovery of steady-state viability in moderate stress. In severe stress survival depended on strain-specific proportions of cells with divergent strategies. Cautious cells survived without dividing; reckless cells attempted to divide too soon and failed, killing both mother and daughter. We show that heritable frequencies of cautious and reckless cells produce a rapidly diversifying template for microbial bet hedging that mimics natural variation in stress responses whose timing, amplitude and frequency could evolve - be tuned by - different patterns of environmental stress.

Evolutionary Biology↗

bioRxiv2016

High-resolution maps of hunter-gatherer social networks reveal human adaptation for cultural exchange

Are interactions with unrelated and even unknown individuals a by-product of modern life in megacities? Here we argue instead that social ties among non-kin are a crucial human adaptation. By deploying a new portable wireless sensing technology (motes), we mapped social networks in Agta and BaYaka hunter-gatherers in unprecedented detail. We show that strong friendships with non-kin optimize the global efficiency of their social networks thereby facilitating cultural exchange, and that the adaptation for forming friendship ties appears early in development. The ability to extend networks and form strong non-kin ties may explain some human distinctive characteristics such as hypersociality and cumulative culture, and the tendency to exchange ideas with unrelated and unknown individuals in megacities and online social networks.\n\nOne Sentence SummarySocial networks of two hunter-gatherer groups in Congo and the Philippines reveal that friendships are an ancestral adaptation for the exchange of information and culture.

Evolutionary Biology↗

bioRxiv2016

Conserved gene clusters in the scrambled plastomes of IRLC legumes (Fabaceae: Trifolieae and Fabeae).

The plastid genome retains several features from its cyanobacterial-like ancestor, one being the co-transcriptional organization of genes into operon-like structures. Some plastid operons have been identified but undoubtedly many more remain undiscovered. Here we utilize the highly variable plastome structure that exists within certain legumes of the inverted repeat lost clade (IRLC) to find conserved gene clusters. These plastomes exhibit an unusually high frequency of translocations and inversions. We analysed the plastomes of 23 legume species and identified 32 locally collinear blocks (LCBs), which are regions within the plastid genomes that occur in different orientation and/or order among the plastid genomes but are themselves free from internal rearrangements. Several represent gene clusters that have previously been recognized as plastid operons. It appears that the number of LCBs has reached saturation in our data set, suggesting that these LCBs are not random, but likely represent legume plastid operons protected from internal rearrangement by functional constraint. Some of the LCBs we identify, such as psbD/C/Z, are previously known plastid operons. Others, such as rpl32-ndhF-psbA-matK-rbcL-atpB-atpE, may represent novel polycistronic operons in legumes.

Evolutionary Biology↗

bioRxiv2016

Micro- and macroevolutionary trade-offs in plant-feeding insects

A long-standing hypothesis asserts that plant-feeding insects specialize on particular host plants because of negative interactions (trade-offs) between adaptations to alternative hosts, yet empirical evidence for such trade-offs is scarce. Most studies have looked for microevolutionary performance trade-offs within insect species, but host-use could also be constrained by macroevolutionary trade-offs caused by epistasis and historical contingency. On the other hand, evolutionary interactions between adaptations to diverse hosts could be neutral or positive rather than negative. Here we used a phylogenetic approach to estimate the micro-and macroevolutionary correlations between use of alternative host plants within two major orders of plant-feeding insects: Lepidoptera (caterpillars) and Hemiptera (true bugs). Across 1604 caterpillar species, we found both positive and negative pairwise correlations between use of diverse host taxa, with overall network patterns suggesting that different host-use constraints act over micro-and macroevolutionary timescales. In contrast, host-use patterns of 955 true bug species revealed uniformly positive correlations between presence on the same host taxa over both timescales. The lack of consistent patterns across timescales and insect orders indicates that host-use trade-offs are historically contingent rather than universal constraints. Moreover, we observed few negative correlations overall despite the wide taxonomic and ecological diversity of the focal host taxa, suggesting that positive interactions between host-use adaptations, not trade-offs, dominate the long-term evolution of host use in plant-feeding insects.

Evolutionary Biology↗

bioRxiv2016

The molecular chaperone DnaK accelerates protein evolution

Molecular chaperones, also known as heat-shock proteins, refold misfolded proteins and help other proteins reach their native conformation. Thanks to these abilities, some chaperones, such as the Hsp90 protein or the chaperonin GroEL, can buffer the deleterious phenotypic effects of mutations that alter protein structure and function. Hsp70 chaperones use a chaperoning mechanism different from Hsp90 and GroEL, and it is not known whether they can also buffer mutations. Here, we show that they can. To this end, we performed a mutation accumulation experiment in Escherichia coli, followed by whole-genome resequencing. Our sequence data shows that overexpression of the Hsp70 chaperone DnaK increases the tolerance of its clients for nonsynonymous nucleotide substitutions and nucleotide insertions and deletions. We also show that this elevated mutational buffering on short evolutionary time scales translates into differences in evolutionary rates on intermediate and long evolutionary time scales. To this end, we compared the evolutionary rates of DnaK clients and nonclients using the genomes of E. coli, Salmonella typhimurium, and 83 other gamma-proteobacterial species. We find that clients that interact strongly with DnaK evolve faster than weakly interacting clients. Our results imply that all three major chaperone classes can buffer mutations and affect protein evolution. They illustrate how an individual protein like a chaperone can have a disproportionate effect on proteome evolution.

Evolutionary Biology↗

bioRxiv2016

Analytical results for directional and quadratic selection gradients for log-linear models of fitness functions

O_LIEstablished methods for inference about selection gradients involve least-squares regression of fitness on phenotype. While these methods are simple and may generally be quite robust, they do not account well for distributions of fitness.\nC_LIO_LISome progress has previously been made in relating inferences about trait-fitness relationships from generalised linear models to selection gradients in the formal quantitative genetic sense. These approaches involve numerical calculation of average derivatives of relative fitness with respect to phenotype.\nC_LIO_LIWe present analytical results expressing selection gradients as functions of the coefficients of generalised linear models for fitness in terms of traits. The analytical results allow calculation of univariate and multivariate directional, quadratic, and correlational selection gradients from log-linear and log-quadratic models.\nC_LIO_LIThe results should be quite generally applicable in selection analysis. They apply to any generalised linear model with a log link function. Furthermore, we show how they apply to some situations including inference of selection from (molecular) paternity data, capture-mark-recapture analysis, and survival analysis. Finally, the results may bridge some gaps between typical approaches in empirical and theoretical studies of natural selection.\nC_LI

Evolutionary Biology↗

bioRxiv2016

Bayesian Inference of the Evolution of a Phenotype Distribution on a Phylogenetic Tree

The distribution of a phenotype on a phylogenetic tree is often a quantity of interest. Many phenotypes have imperfect heritability, so that a measurement of the phenotype for an individual can be thought of as a single realisation from the phenotype distribution of that individual. If all individuals in a phylogeny had the same phenotype distribution, measured phenotypes would be randomly distributed on the tree leaves. This is however often not the case, implying that the phenotype distribution evolves over time. Here we propose a new model based on this principle of evolving phenotype distribution on the branches of a phylogeny, which is different from ancestral state reconstruction where the phenotype itself is assumed to evolve. We develop an efficient Bayesian inference method to estimate the parameters of our model and to test the evidence for changes in the phenotype distribution. We use multiple simulated datasets to show that our algorithm has good sensitivity and specificity properties. Since our method identifies branches on the tree on which the phenotype distribution has changed, it is able to break down a tree into components for which this distribution is unique and constant. We present two applications of our method, one investigating the association between HIV genetic variation and human leukocyte antigen, and the other studying host range distribution in a lineage of Salmonella enterica, and we discuss many other potential applications. All the methods described in this paper are implemented in a software package called TreeBreaker which is freely available for download at https://github.com/ansariazim/TreeBreaker

Evolutionary Biology↗

bioRxiv2016

Natural selection driven by DNA binding proteins shapes genome-wide motif statistics

Ectopic DNA binding by transcription factors and other DNA binding proteins can be detrimental to cellular functions and ultimately to organismal fitness. The frequency of protein-DNA binding at non-functional sites depends on the global composition of a genome with respect to all possible short motifs, or k-mer words. To determine whether weak yet ubiquitous protein-DNA interactions could exert significant evolutionary pressures on genomes, we correlate in vitro measurements of binding strengths on all 8-mer words from a large collection of transcription factors, in several different species, against their relative genomic frequencies. Our analysis reveals a clear signal of purifying selection to reduce the large number of weak binding sites genome-wide. This evolutionary process, which we call global selection, has a detectable hallmark in that similar words experience similar evolutionary pressure, a consequence of the biophysics of protein-DNA binding. By analyzing a large collection of genomes, we show that global selection exists in all domains of life, and operates through tiny selective steps, maintaining genomic binding landscapes over long evolutionary timescales.

Evolutionary Biology↗

bioRxiv2016

Generation of mutation hotspots in ageing bacterial colonies

How do ageing bacterial colonies generate adaptive mutants? Over a period of two months, we isolated on ageing colonies outgrowing mutants able to use a new carbon source, and sequenced their genomes. This allowed us to uncover exquisite details on the molecular mechanism behind their adaptation: most mutations were located in just a few hotspots in the genome and over time, mutations increasingly originated from 8-oxo-guanosine, formed exclusively on the transcribed strand.

Evolutionary Biology↗

bioRxiv2016

Pollinator specialization imposes stronger evolutionary constraints on flower shape

Flowers show important structural variation as reproductive organs but the evolutionary forces underlying this diversity are still poorly understood. In animal-pollinated species, flower shape is strongly fashioned by selection imposed by pollinators, which is expected to vary according to guilds of effective pollinators. Using the Antillean subtribe Gesneriinae (Gesneriaceae), we tested the hypothesis that pollination specialists pollinated by one functional type of pollinator have maintained more similar corolla shapes through time due to stronger selection constraints compared to species with more generalist pollination strategies. Using geometric morphometrics and evolutionary models, we showed that the corolla of hummingbird specialists, bat specialists, and species with a mixed-pollination strategy (pollinated by hummingbirds and bats; thus a more generalist strategy) have distinct shapes and that these shapes have evolved under evolutionary constraints. However, we did not find support for smaller disparity in corolla shape for hummingbird specialists compared to more generalist species. This could be because the corolla shape of more generalist species in subtribe Gesneriinae, which has evolved multiple times, is finely adapted to be effectively pollinated by both bats and hummingbirds. These results suggest that pollination generalization is not necessarily associated with relaxed selection constraints.

Evolutionary Biology↗

bioRxiv2016

Species Identification by Bayesian Fingerprinting: A Powerful Alternative to DNA Barcoding

A number of methods have been developed to use genetic sequence data to identify and delineate species. Some methods are based on heuristics, such as DNA barcoding which is based on a sequence-distance threshold, while others use Bayesian model comparison under the multispecies coalescent model. Here we use mathematical analysis and computer simulation to demonstrate large differences in statistical performance of species identification between DNA barcoding and Bayesian inference under the multispecies coalescent model as implemented in the BPP program. We show that a fixed genetic-distance threshold as used in DNA barcoding is problematic for delimiting species, even if the threshold is \"optimized\", because different species have different population sizes and different divergence times, and therefore display different amounts of intra-species versus inter-species variation. In contrast, BPP can reliably delimit species in such situations with only one locus and rarely supports a wrong assignment with high posterior probability. While under-sampling or rare specimens may pose problems for heuristic methods, BPP can delimit species with high power when multi-locus data are used, even if the species is represented by a single specimen. Finally we demonstrate that BPP may be powerful for delimiting cryptic species using specimens that are misidentified as a single species in the barcoding library.

Evolutionary Biology↗

bioRxiv2016

Sporulation, bacterial cell envelopes, and the origin of life

Four recent papers from our group exploiting the power of electron cryotomography to produce 3-D reconstructions of intact cells in a near-native state have led to the proposal that an ancient sporulation-like event gave rise to the second membrane in diderm bacteria. Here we review the images of sporulating monoderm and diderm cells which show how sporulation leads to diderm cells. We also review the images of Gram-negative and Gram-positive cell walls that show they are more closely related than previously thought, and explain how this provides critical support for the hypothesis. Mapping the distribution of cell envelope architectures onto the most recent phylogenetic tree of life then leads to the conclusion that the diderm cell plan, and therefore the sporulation-like event that gave rise to it, must be very ancient. One explanation for the biogeologic record is that during the cataclysmic transitions of early Earth, cellular evolution may have gone through a bottleneck where only spores survived (LUCA was a spore).

Evolutionary Biology↗

bioRxiv2016

Trait Heritability in Major Transitions

A crucial component of major transitions theory is that after the transition, adaptation occurs primarily at the level of the new, higher-level unit. For collective-level adaptations to occur, though, collective-level traits must be heritable. Since collective-level trait values are functions of lower-level trait values, collective-level heritability is related to particle-level heritability. However, the nature of this relationship has rarely been explored in the context of major transitions. We examine relationships between particle-level heritability and collective-level heritability for several functions that express collective-level trait value in terms of particle-level trait values. When a collective-level trait value is a linear function of particle-level trait values, the heritability of a collective-level trait is never less than that of the corresponding particle-level trait and is higher under most conditions. For more complicated functions, collective-level heritability is higher under most conditions, but can be lower when the function relating particle to cell-level trait values is sensitive to small fluctuations in the state of the particles within the collective. Rather than being an impediment to major transitions, we show that collective-level heritability superior to that of the lower-level units can often arise for free, simply as a byproduct of collective formation.

Evolutionary Biology↗

bioRxiv2016

Measuring epistasis in fitness landscapes: the correlation of fitness effects of mutations

Genotypic fitness landscapes are constructed by assessing the fitness of all possible combinations of a given number of mutations. In the last years, several experimental fitness landscapes have been completely resolved. As fitness landscapes are high-dimensional, simple measures of their structure are used as statistics in empirical applications. Epistasis is one of the most relevant features of fitness landscapes. Here we propose a new natural measure of the amount of epistasis based on the correlation of fitness effects of mutations. This measure has a natural interpretation, captures well the interaction between mutations and can be obtained analytically for most landscape models. We discuss how this measure is related to previous measures of epistasis (number of peaks, roughness/slope, fraction of sign epistasis, Fourier-Walsh spectrum) and how it can be easily extended to landscapes with missing data or with fitness ranks only. Furthermore, the dependence of the correlation of fitness effects on mutational distance contains interesting information about the patterns of epistasis. This dependence can be used to uncover the amount and nature of epistatic interactions in a landscape or to discriminate between different landscape models.

Evolutionary Biology↗

bioRxiv2016

Core Genes Evolve Rapidly in the Long-term Evolution Experiment with Escherichia coli

Bacteria can evolve rapidly under positive selection owing to their vast numbers, allowing their genes to diversify by adapting to different environments. We asked whether the same genes that are fast evolving in the long-term evolution experiment with Escherichia coli (LTEE) have also diversified extensively in nature. We identified ~2000 core genes shared among 60 E. coli strains. During the LTEE, core genes accumulated significantly more nonsynonymous mutations than flexible (i.e., noncore) genes. Furthermore, core genes under positive selection in the LTEE are more conserved in nature than the average core gene. In some cases, adaptive mutations appear to fine-tune protein functions, rather than merely knocking them out. The LTEE conditions are novel for E. coli, at least in relation to the long sweep of its evolution in nature. The constancy and simplicity of the environment likely favor the complete loss of some unused functions and the fine-tuning of others.\n\nCompeting Interests StatementWe, the authors, declare that we have no conflicts of interest.

Evolutionary Biology↗

bioRxiv2016

Evolution in Eggs and Phases: experimental evolution of fecundity and reproductive timing in Caenorhabditis elegans

To examine the role of natural selection on fecundity in a variety of Caenorhabditis elegans genetic backgrounds, we used an experimental evolution protocol to evolve 14 distinct genetic strains over 15-20 generations. Beginning with three founder worms for each strain, we were able to generate 790 distinct genealogies, which provided information on both the effects of natural selection and the evolvability of each strain. Among these genotypes are a wildtype (N2) and a collection of mutants with targeted mutations in the daf-c, daf-d, and AMPK pathways. The overarching goal of our analysis is two-fold: to observe differences in reproductive fitness and observe related changes in reproductive timing. This yields two outcomes. The first is that the majority of selective effects on fecundity occur during the first few generations of evolution, while the negative selection for reproductive timing occurs on longer timescales. The second finding reveals that positive selection on fecundity results in positive and negative selection on reproductive timing, both of which are strain-dependent. Using a derivative of population size per generation called the reproductive carry-over (RCO) measure, it is found that the fluctuation and shape of the probability distribution may be informative in terms of developmental selection. While these consist of general patterns that transcend mutations in a specific gene, changes in the RCO measure may nevertheless be products of selection. In conclusion, we discuss the broader implications of these findings, particularly in the context of genotype-fitness maps and the role of uncharacterized mutations in individual variation and evolvability.

Evolutionary Biology↗

bioRxiv2016

Assortative mating can impede or facilitate fixation of underdominant alleles

Although underdominant mutations have undoubtedly fixed between divergent species, classical models of population genetics suggest underdominant alleles should be purged quickly, except in small or subdivided populations. Here we study the fixation of underdominant alleles at loci that also influence mate choice, such as loci encoding coloration patterns visible to mates and predators alike. We analyze a mechanistic model of positive assortative mating in which individuals have n chances to sample compatible mates. This one-parameter model naturally spans the two classical extremes of random mating (n = 1) and complete assortment (n [->] {infty}), and yet it produces a complex form of sexual selection that depends non-monotonically on the number of mating opportunities, n. The resulting interaction between viability selection and sexual selection can either inhibit or facilitate fixation of underdominant alleles, compared to random mating. As the number of mating opportunities increases, underdominant alleles can fix at rates that even approach the neutral substitution rate. This result is counterintuitive because sexual selection and underdominance each suppress rare alleles in this model, and yet in combination they can promote the fixation of rare alleles. This phenomenon constitutes a new mechanism for the fixation of underdominant alleles in large populations, and it illustrates how incorporating life history characteristics can alter the predictions of population-genetic models for evolutionary change.

Evolutionary Biology↗

bioRxiv2016

Transposable Element Evolution in the Allotetraploid Capsella bursa-pastoris

Premise of the studyShifts in ploidy affect the evolutionary dynamics of genomes in a myriad of ways. Population genetic theory predicts that transposable element (TE) proliferation may follow because the genome wide efficacy of selection should be reduced and the increase in gene copies may mask the deleterious effects of TE insertions. Moreover, in allopolyploids TEs may further accumulate because of hybrid breakdown of TE silencing. However, to date the evidence of TE proliferation following an increase in ploidy is mixed, and the relative importance of relaxed selection vs. silencing breakdown remains unclear.\n\nMethodsWe used high-coverage whole genome sequence data to evaluate the abundance, genomic distribution, and population frequencies of TEs in the self-fertilizing recent allotetraploid Capsella bursa-pastoris (Brassicaceae). We then compared the C. bursa-pastoris TE profile with that of its two parental diploid species, outcrossing C. grandiflora and self-fertilizing C. orientalis.\n\nKey resultsWe found no evidence that C. bursa-pastoris has experienced a large genome wide proliferation of TEs relative to its parental species. However, when centromeric regions are excluded, we find evidence of significantly higher abundance of retrotransposons in C. bursa-pastoris along the gene-rich chromosome arms, compared to C.grandiflora and C. orientalis.\n\nConclusionsThe lack of a genome-wide effect of allopolyploidy on TE abundance, combined with the increases TE abundance in gene-rich regions suggest that relaxed selection rather than hybrid breakdown of host silencing explains the TE accumulation in C. bursa-pastoris

Evolutionary Biology↗