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bioRxiv2016

The genetic architecture of local adaptation II: The QTL landscape of water-use efficiency for foxtail pine (Pinus balfouriana Grev. & Balf.)

Water availability is an important driver of the geographic distribution of many plant species, although its importance relative to other climatic variables varies across climate regimes and species. A common indirect measure of water-use efficiency (WUE) is the ratio of carbon isotopes ({delta}13C) fixed during photosynthesis, especially when analyzed in conjunction with a measure of leaf-level resource utilization ({delta}15N). Here, we test two hypotheses about the genetic architecture of WUE for foxtail pine (Pinus balfouriana Grev. & Balf.) using a novel mixture of double digest restriction site associated DNA sequencing, species distribution modeling, and quantitative genetics. First, we test the hypothesis that water availability is an important determinant of the geographical range of foxtail pine. Second, we test the hypothesis that variation in {delta}13C and {delta}15N is genetically based, differentiated between regional populations, and has genetic architectures that include loci of large effect. We show that precipitation-related variables structured the geographical range of foxtail pine, climate-based niches differed between regional populations, and {delta}13C and {delta}15N were heritable with moderate signals of differentiation between regional populations. A set of large-effect QTLs (n = 11 for {delta}13C; n = 10 for {delta}15N) underlying {delta}13C and {delta}15N variation, with little to no evidence of pleiotropy, was discovered using multiple-marker, half-sibling regression models. Our results represent a first approximation to the genetic architecture of these phenotypic traits, including documentation of several patterns consistent with {delta}13C being a fitness-related trait affected by natural selection.

Evolutionary Biology↗

bioRxiv2016

Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

Speciation usually proceeds in a continuum from intensively hybridizing populations until the formation of irreversibly isolated species. Restriction of interspecific gene flow may often be achieved by gradual accumulation of intrinsic postzygotic incompatibilities with hybrid infertility typically evolving more rapidly than inviability. A reconstructed history of speciation in European loaches (Cobitis) reveals that accumulation of postzygotic reproductive incompatibilities may take an alternative, in the literature largely neglected, pathway through initiation of hybrids asexuality rather than through a decrease in hybrids fitness. Combined evidence shows that contemporary Cobitis species readily hybridize in hybrid zones, but their gene pools are isolated as hybridization produces infertile males and fertile but clonally reproducing females that cannot mediate introgressions. Nevertheless, coalescent analyses indicated intensive historical gene flow during earlier stages of Cobitis diversification, suggesting that non-clonal hybrids must have existed in the past. The revealed patterns imply that during the initial stages of speciation, hybridization between little diverged species produced recombinant hybrids mediating gene flow, but growing divergence among species caused disrupted meiosis in hybrids resulting in their clonality, which acts as a barrier to gene flow. Comparative analysis of published data on other fish hybrids corroborated the generality of our findings; the species pairs producing asexual hybrids were more genetically diverged than those pairs producing fertile sexual hybrids but less diverged than species pairs producing infertile hybrids. Hybrid asexuality therefore appears to evolve at lower divergence than other types of postzygotic barriers and might thus represent a primary reproductive barrier in many taxa.

Evolutionary Biology↗

bioRxiv2016

How transposons drive evolution of virulence in a fungal pathogen

Genomic plasticity enables adaptation to changing environments, which is especially relevant for pathogens that engage in arms races with their hosts. In many pathogens, genes mediating aggressiveness cluster in highly variable, transposon-rich, physically distinct genomic compartments. However, understanding of the evolution of these compartments, and the role of transposons therein, remains limited. We now show that transposons are the major driving force for adaptive genome evolution in the fungal plant pathogen Verticillium dahliae. Highly variable genomic regions evolved by frequent segmental duplications mediated by erroneous homologous recombination, often utilizing transposons, leading to genetic material that is free to diverge. Intriguingly, the duplicated regions are enriched in active transposons that further contribute to local genome plasticity. Thus, we provide evidence for genome shaping by transposons, both in an active and passive manner, which impacts the evolution of pathogen aggressiveness.

Evolutionary Biology↗

bioRxiv2016

Sequence amplification via cell passaging creates spurious signals of positive adaptation in influenza H3N2 hemagglutinin

Clinical influenza A isolates are frequently not sequenced directly. Instead, a majority of these isolates (~70% in 2015) are first subjected to passaging for amplification, most commonly in non-human cell culture. Here, we find that this passaging leaves distinct signals of adaptation in the viral sequences, which can confound evolutionary analyses of the viral sequences. We find distinct patterns of adaptation to Madin-Darby (MDCK) and monkey cell culture absent from unpassaged hemagglutinin sequences. These patterns also dominate pooled datasets not separated by passaging type, and they increase in proportion to the number of passages performed. By contrast, MDCK-SIAT1 passaged sequences seem mostly (but not entirely) free of passaging adaptations. Contrary to previous studies, we find that using only internal branches of the influenza phylogenetic trees is insufficient to correct for passaging artifacts. These artifacts can only be safely avoided by excluding passaged sequences entirely from subsequent analysis. We conclude that future influenza evolutionary analyses should appropriately control for potentially confounding effects of passaging adaptations.

Evolutionary Biology↗

bioRxiv2016

Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi

Although cell cycle control is an ancient, conserved, and essential process, some core animal and fungal cell cycle regulators share no more sequence identity than non-homologous proteins. Here, we show that evolution along the fungal lineage was punctuated by the early acquisition and entrainment of the SBF transcription factor through horizontal gene transfer. Cell cycle evolution in the fungal ancestor then proceeded through a hybrid network containing both SBF and its ancestral animal counterpart E2F, which is still maintained in many basal fungi. We hypothesize that a virally-derived SBF may have initially hijacked cell cycle control by activating transcription via the cis-regulatory elements targeted by the ancestral cell cycle regulator E2F, much like extant viral oncogenes. Consistent with this hypothesis, we show that SBF can regulate promoters with E2F binding sites in budding yeast.

Evolutionary Biology↗

bioRxiv2016

Skew in ovarian activation depends on domicile size in a facultatively social thrips

Costs and benefits of group living are a fundamental topic in behavioural ecology. Resource availability affects individuals breeding prospects alone and in groups, as well as how reproduction is distributed within groups (\"reproductive skew\"). Here, we provide correlational evidence in facultatively social thrips that breeding resources are associated with (1) whether solitary or social living is favoured, and (2) the degree of ovarian skew.\n\nDunatothrips aneurae (Thysanoptera, Phlaeothripidae) cooperatively build silk \"domiciles\" on Australian Acacias, feeding exclusively from internal phyllode surfaces. Per capita productivity scaled differently with group size depending on domicile volume - females in small domiciles did better alone than in groups, whereas in large domiciles single and group-nesting females did equally well. Ovarian dissections revealed that in small domiciles some females were nonreproductive, indicating ovarian (i.e. reproductive) skew. Skew increased as domicile size decreased and group size increased. Breeders had smaller oocyte volume in smaller domiciles, especially those containing nonreproductives.\n\nThese findings suggest group formation and reproductive skew in D. aneurae may be influenced by reproductive competition for breeding resources. Nonreproductive females in small domiciles may be reproductively suppressed, subfertile, or waiting to reproduce. We speculate they may avoid eviction by contributing as \"helpers\" to domicile maintenance.

Evolutionary Biology↗

bioRxiv2016

Phenotypic plasticity promotes balanced polymorphism in periodic environments by a genomic storage effect

Phenotypic plasticity is known to evolve in perturbed habitats, where it alleviates the deleterious effects of selection. But the effects of plasticity on levels of genetic polymorphism, an important precursor to adaptation in temporally varying environments, are unclear. Here we develop a haploid, two-locus population-genetic model to describe the interplay between a plasticity modifier locus and a target locus subject to periodically varying selection. We find that the interplay between these two loci can produce a \"genomic storage effect\" that promotes balanced polymorphism over a large range of parameters, in the absence of all other conditions known to maintain genetic variation. The genomic storage effect arises as recombination allows alleles at the two loci to escape more harmful genetic backgrounds and associate in haplotypes that persist until environmental conditions change. Using both Monte Carlo simulations and analytical approximations we quantify the strength of the genomic storage effect across a range of selection pressures, recombination rates, plasticity modifier effect sizes, and environmental periods.

Evolutionary Biology↗

bioRxiv2016

Evolutionary games of multiplayer cooperation on graphs

There has been much interest in studying evolutionary games in structured populations, often modelled as graphs. However, most analytical results so far have only been obtained for two-player or linear games, while the study of more complex multiplayer games has been usually tackled by computer simulations. Here we investigate evolutionary multiplayer games on graphs updated with a Moran death-Birth process. For cycles, we obtain an exact analytical condition for cooperation to be favored by natural selection, given in terms of the payoffs of the game and a set of structure coefficients. For regular graphs of degree three and larger, we estimate this condition using a combination of pair approximation and diffusion approximation. For a large class of cooperation games, our approximations suggest that graph-structured populations are stronger promoters of cooperation than populations lacking spatial structure. Computer simulations validate our analytical approximations for random regular graphs and cycles, but show systematic differences for graphs with many loops such as lattices. In particular, our simulation results show that these kinds of graphs can even lead to more stringent conditions for the evolution of cooperation than well-mixed populations. Overall, we provide evidence suggesting that the complexity arising from many-player interactions and spatial structure can be captured by pair approximation in the case of random graphs, but that it need to be handled with care for graphs with high clustering.\n\nAuthor SummaryCooperation can be defined as the act of providing fitness benefits to other individuals, often at a personal cost. When interactions occur mainly with neighbors, assortment of strategies can favor cooperation but local competition can undermine it. Previous research has shown that a single coefficient can capture this trade-off when cooperative interactions take place between two players. More complicated, but also more realistic models of cooperative interactions involving multiple players instead require several such coefficients, making it difficult to assess the effects of population structure. Here, we obtain analytical approximations for the coefficients of multiplayer games in graph-structured populations. Computer simulations show that, for particular instances of multiplayer games, these approximate coefficients predict the condition for cooperation to be promoted in random graphs well, but fail to do so in graphs with more structure, such as lattices. Our work extends and generalizes established results on the evolution of cooperation on graphs, but also highlights the importance of explicitly taking into account higher-order statistical associations in order to assess the evolutionary dynamics of cooperation in spatially structured populations.

Evolutionary Biology↗

bioRxiv2016

The stasis that wasn’t: Adaptive evolution goes against phenotypic selection in a wild rodent population

In natural populations, quantitative trait dynamics often do not appear to follow evolutionary predictions: Despite abundant examples of natural selection acting on heritable traits, conclusive evidence for contemporary adaptive evolution remains rare for wild vertebrate populations, and phenotypic stasis seems to be the norm. This so-called stasis paradox highlights our inability to predict evolutionary change, which is especially concerning within the context of rapid anthropogenic environmental change. While the causes underlying the stasis paradox are hotly debated, comprehensive attempts aiming at a resolution are lacking. Here we apply a quantitative genetic framework to individual-based long-term data for a wild rodent population and show that despite a positive association between body mass and fitness, there has been a genetic change towards lower body mass. The latter represents an adaptive response to viability selection favouring juveniles growing up to become relatively small adults, i.e. with a low potential adult mass, which presumably complete their development earlier. This selection is particularly strong towards the end of the snow-free season, and it has intensified in recent years, coinciding which a change in snowfall patterns. Importantly, neither the negative evolutionary change, nor the selective pressures that drive it, are apparent on the phenotypic level, where they are masked by phenotypic plasticity and a non-causal (i.e. non-genetic) positive association between body mass and fitness, respectively. Estimating selection at the genetic level thereby enabled us to uncover adaptive evolution in action, and to identify the corresponding phenotypic selective pressure. We thereby demonstrate that natural populations can show a rapid and adaptive evolutionary response to a novel selective pressure, and that explicitly (quantitative) genetic models are able to provide us with an understanding of the causes and consequences of selection that is superior to purely phenotypic estimates of selection and evolutionary change.

Evolutionary Biology↗

bioRxiv2016

Combining Shigella Tn-seq data with Gold-standard E. coli Gene Deletion Data Suggests Rare Transitions between Essential and Non-essential Gene Functionality

Gene essentiality - whether or not a gene is necessary for cell growth - is a fundamental component of gene function. It is not well established how quickly gene essentiality can change, as few studies have compared empirical measures of essentiality between closely related organisms. Here we present the results of a Tn-seq experiment designed to detect essential protein coding genes in the bacterial pathogen Shigella flexneri 2a 2457T on a genome-wide scale. Superficial analysis of this data suggested that 451 protein-coding genes in this Shigella strain are critical for robust cellular growth on rich media. Comparison of this set of genes with a gold-standard data set of essential genes in the closely related Escherichia coli K12 BW25113 suggested that an excessive number of genes appeared essential in Shigella but non-essential in E. coli. Importantly, and in converse to this comparison, we found no genes that were essential in E. coli and non-essential in Shigella, suggesting that many genes were artefactually inferred as essential in Shigella. Controlling for such artefacts resulted in a much smaller set of discrepant genes. Among these, we identified three sets of functionally related genes, two of which have previously been implicated as critical for Shigella growth, but which are dispensable for E. coli growth. The data presented here highlight the small number of protein coding genes for which we have strong evidence that their essentiality status differs between the closely related bacterial taxa E. coli and Shigella. A set of genes involved in acetate utilization provides a canonical example. These results leave open the possibility of developing strain-specific antibiotic treatments targeting such differentially essential genes, but suggest that such opportunities may be rare in closely related bacteria.

Evolutionary Biology↗

bioRxiv2016

No evidence for the positive relationship between genetic correlations and heritabilities

Quantitative genetics predicts, that traits subjected to strong selection should show low heritability and may yield biased estimates of genetic correlations (rg). Similar pattern may also appear if genetic sources of variation are confounded with non-genetic sources. Thus, a positive relationship between genetic correlations and heritabilities (h2) of underlying traits might be observed. Here we test this prediction using a large dataset of published estimates of genetic correlations and employing a powerful meta-analytical approach. We considered both between-traits and cross-sex genetic correlations. We failed to find support for the prediction about a positive rg - h2 relationship: our analysis based on nearly 1000 published estimates of genetic parameters indicates that the predicted relationship is weak and statistically non-significant. Thus, low heritability does not preclude the possibility of detecting substantial genetic correlations. Our meta-analysis indicates that published estimates of genetic parameters coming from various experimental designs and obtained using different statistical techniques are not significantly biased in case of weakly-heritable traits.

Evolutionary Biology↗

bioRxiv2016

Inferring the frequency spectrum of derived variants to quantify adaptive molecular evolution in protein-coding genes of Drosophila melanogaster

Many approaches for inferring adaptive molecular evolution analyze the unfolded site frequency spectrum (SFS), a vector of counts of sites with different numbers of copies of derived alleles in a sample of alleles from a population. Accurate inference of the high copy number elements of the SFS is difficult, however, because of misassignment of alleles as derived versus ancestral. This is a known problem with parsimony using outgroup species. Here, we show that the problem is particularly serious if there is variation in the substitution rate among sites brought about by variation in selective constraint levels. We present a new method for inferring the SFS using one or two outgroups, which attempts to overcome the problem of misassignment. We show that two outgroups are required for accurate estimation of the SFS if there is substantial variation in selective constraints, which is expected to be the case for nonsynonymous sites of protein-coding genes. We apply the method to estimate unfolded SFSs for synonymous and nonsynonymous sites from Phase 2 of the Drosophila Population Genomics Project. We use the unfolded spectra to estimate the frequency and strength of advantageous and deleterious mutations, and estimate that {small tilde}50% of amino acid substitutions are positively selected, but that less than 0.5% of new amino acid mutations are beneficial, with a scaled selection strength of Nes {approx} 12.

Evolutionary Biology↗

bioRxiv2016

Social selection maintains honesty of a dynamic visual signal in cichlid fish

How honest signals evolve is a question that has been hotly debated by animal communication theoreticians and for which empirical evidence has been difficult to obtain. Theory predicts that, due to strong conflicts of interest, communication in aggressive contexts should be under strong selection for clear and reliable signaling. On the other hand, context-dependent signaling increases cheating opportunities, depending on how senders and receivers use, acquire and process signal information. Using animal signaling theory, theoretical visual models and behavioral experimentation, we characterize and determine proximate honesty mechanisms of the facial coloration in the Princess of Burundi cichlid, Neolamprologus brichardi, a species with complex social interactions. We show that this facial color pattern evolved stable chromatic conspicuousness for efficient transmission in the aquatic environment, while context-dependent plasticity in luminance of the horizontal black stripe element is used to signal switches in aggressive intent. Importantly, using experimental signal manipulation we demonstrate that social selection by receiver retaliation is the mechanism responsible for maintaining signal honesty. We suggest that by affecting the evolution of pigmentation patterns in sexually monochromatic cichlid species, social selection can have potential impacts on diversification dynamics.

Evolutionary Biology↗

bioRxiv2016

Evolution of HIV virulence in response to widespread scale up of antiretroviral therapy: a modeling study

There are global increases in the use of HIV antiretroviral therapy (ART), guided by clinical benefits of early ART initiation, and the efficacy of treatment as prevention of transmission. Separately, it has been shown theoretically and empirically that HIV virulence can evolve over time. Observed virulence levels may reflect an adaptive balance between infected lifespan and per-contact transmission rate. Critically, the potential effects of widespread ART on HIV virulence are unknown. To predict these effects, we used an agent-based stochastic model to simulate changes in HIV virulence, using set point viral load as a virulence proxy. We calibrated our epidemic model to the prevalence and incidence trends of South Africa. We repeated our analysis using a separate calibration, as a sensitivity analysis, and found that predicted impact of ART on virulence was relatively insensitive to calibration. We explored two ART scenarios, at increasing coverage : ART initiation based on patients reaching a CD4 cell count threshold, or based on time elapsed since infection (a scenario that mimics the \"universal testing and treatment\" aspirations). We found that HIV virulence is generally unchanged in scenarios of CD4-based initiation. However, with ART initiation based on time since infection, virulence can increase moderately within several years of ART rollout, under high coverage and early treatment initiation, albeit within the context of rapidly shrinking epidemics. Our modeling study suggests that increasing virulence driven by universal test and treat is likely not a major public health concern, but could be monitored in sentinel surveillance, in a manner similar to transmitted drug resistance.

Evolutionary Biology↗

bioRxiv2016

Craniofacial shape transition across the house mouse hybrid zone: implications for the genetic architecture and evolution of between-species differences

Craniofacial shape differences between taxa have often being linked to environmental adaptation, e.g. to new food sources, or have been studied in the context of domestication. Evidence for the genetic basis of such phenotypic differences to date suggests that within- as well as between-species variation has an oligogenic basis, i.e. few loci of large effect explain most of the variation. In mice, it has been shown that within-population craniofacial variation has a highly polygenic basis, but there are no data regarding the genetic basis of between-species differences. Here, we address this question using a phenotype-focused approach. Using 3D geometric morphometrics, we phenotyped a panel of mice derived from a natural hybrid zone between M. m. domesticus and M. m. musculus, and quantify the transition of craniofacial shape along the hybridization gradient. We find a continuous shape transition along the hybridization gradient, and unaltered developmental stability associated with hybridization. This suggests that the morphospace between the two subspecies is continuous despite reproductive isolation and strong barriers to gene flow. We show that quantitative changes in genome composition generate quantitative changes in craniofacial shape; this supports a highly polygenic basis for between-species craniofacial differences in the house mouse. We discuss our findings in the context of oligogenic versus polygenic models of the genetic architecture of morphological traits.

Evolutionary Biology↗

bioRxiv2016

The infinitesimal model

Our focus here is on the infinitesimal model. In this model, one or several quantitative traits are described as the sum of a genetic and a non-genetic component, the first being distributed as a normal random variable centred at the average of the parental genetic components, and with a variance independent of the parental traits. We first review the long history of the infinitesimal model in quantitative genetics. Then we provide a definition of the model at the phenotypic level in terms of individual trait values and relationships between individuals, but including different evolutionary processes: genetic drift, recombination, selection, mutation, population structure, ... We give a range of examples of its application to evolutionary questions related to stabilising selection, assortative mating, effective population size and response to selection, habitat preference and speciation. We provide a mathematical justification of the model as the limit as the number M of underlying loci tends to infinity of a model with Mendelian inheritance, mutation and environmental noise, when the genetic component of the trait is purely additive. We also show how the model generalises to include epistatic effects. In each case, by conditioning on the pedigree relating individuals in the population, we incorporate arbitrary selection and population structure. We suppose that we can observe the pedigree up to the present generation, together with all the ancestral traits, and we show, in particular, that the genetic components of the individual trait values in the current generation are indeed normally distributed with a variance independent of ancestral traits, up to an error of order [Formula]. Simulations suggest that in particular cases the convergence may be as fast as 1/M.

Evolutionary Biology↗

bioRxiv2016

A tradeoff between the ecological and evolutionary stabilities of public goods genes in microbial populations

Microbial populations often rely on the cooperative production of extracellular \"public goods\" molecules. The cooperative nature of public good production may lead to minimum viable population sizes, below which populations collapse. In addition, \"cooperator\" public goods producing cells face evolutionary competition from non-producing mutants, or \"freeloaders\". Thus, public goods cooperators have to be stable not only to the invasion of freeloaders, but also to ecological perturbations that may push their numbers too small to be sustainable. Through a combination of experiments with microbial populations and mathematical analysis of the Ecological Public Goods Game, we show that game parameters and experimental conditions that improve the evolutionary stability of cooperators also lead to a low ecological stability of the cooperator population. Complex regulatory strategies mimicking those used by microbes in nature may allow cooperators to beat this eco-evolutionary stability tradeoff and become resistant to freeloaders while at the same time maximizing their ecological stability. Our results thus identify the coupled eco-evolutionary stability as being key for the long-term viability of microbial public goods cooperators.

Evolutionary Biology↗

bioRxiv2016

Into the tropics: phylogenomics and evolutionary dynamics of a contrarian clade of ants

AimThe standard latitudinal diversity gradient (LDG), in which species richness decreases from equator to pole, is a pervasive pattern observed in most groups of organisms. Despite its commonness, an increasing number of non-conforming lineages have been identified, presenting a challenge for general explanations of the standard LDG. Although problematic, documenting and studying these contrarian groups can help us to better understand LDGs generally. To that end we identify the ant tribe Stenammini, a diverse lineage with over 400 species, as a contrarian clade, and we attempt to explain the groups atypical diversity pattern using a historical approach. We evaluate the following alternative hypotheses: time-for-speciation/center-of-origin (TFS/COO), niche conservatism, and differences in diversification rate.\n\nLocationGlobal.\n\nMethodsWe examine the shape of the LDG in Stenammini by plotting latitudinal midpoints for all extant species. We then infer a robust phylogeny using a phylogenomic approach that employs ultraconserved element loci and we use the phylogeny to estimate divergence dates, biogeographic history, and ancestral habitats. We also test for diversification rate heterogeneity across the tree and among lineages within the tribe.\n\nResultsStenammini has a skewed inverse latitudinal diversity gradient with an extratropical richness peak in the northern temperate zone. Our phylogenomic approach resulted in a robust phylogeny revealing five major clades and several instances of non-monophyly among genera (Goniomma, Aphaenogaster). The tribe and most major lineages originated in the temperate zone and inhabited temperate niches. Crown Stenammini dates to 52 Ma (Eocene Climatic Optimum) and most major lineages appeared soon after during a period of global cooling. Despite its temperate origin, the group invaded the tropics at least six times, but failed to diversify greatly there. Across the tree diversification increased from 17.2-1.9 Ma following the Mid-Miocene Climatic Optimum, and among lineages there was a rate increase in Holarctic Aphaenogaster + Messor just prior to 17.2 Ma.\n\nMain ConclusionsOur results suggest that time, niche conservatism, and increased diversification have all contributed to the inverse latitudinal gradient in Stenammini. Among these processes, niche conservatism may be less important given that the tribe has dispersed to the tropics multiple times.

Evolutionary Biology↗