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bioRxiv2016

Radical changes persist longer in the absence of sex

Harmful mutations are ubiquitous and inevitable, and the rate at which these mutations are removed from populations is a critical determinant of evolutionary fate. Closely related sexual and asexual taxa provide a particularly powerful setting to study deleterious mutation elimination because sexual reproduction should facilitate mutational clearance by reducing selective interference between sites and by allowing the production of offspring with different mutational complements than their parents. Here, we compared the rate of removal of conservative (i.e., similar biochemical properties) and radical (i.e., distinct biochemical properties) nonsynonymous mutations from mitochondrial genomes of sexual vs. asexual Potamopyrgus antipodarum, a New Zealand freshwater snail characterized by coexisting and ecologically similar sexual and asexual lineages. Our analyses revealed that radical nonsynonymous mutations are cleared at higher rates than conservative changes and that sexual lineages eliminate radical changes more rapidly than asexual counterparts. These results are consistent with reduced efficacy of purifying selection in asexual lineages allowing harmful mutations to remain polymorphic longer than in sexual lineages. Together, these data illuminate some of the population-level processes contributing to mitochondrial mutation accumulation and suggest that mutation accumulation could influence the outcome of competition between sexual and asexual lineages.

Evolutionary Biology↗

bioRxiv2016

No ′small genome attraction′ artifact: A response to Harish et al. ′Did viruses evolve as a distinct supergroup from common ancestors of cells?′

In a recent eLetter and associated preprint, Harish, Abroi, Gough and Kurland criticized our structural phylogenomic methods, which support the early cellular origin of viruses. Their claims include the argument that the rooting of our trees is artifactual and distorted by small genome (proteome) size. Here we uncover their aprioristic reasoning, which mingles with misunderstandings and misinterpretations of cladistic methodology. To demonstrate, we labeled the phylogenetic positions of the smallest proteomes in our phylogenetic trees and confirm that the smallest genomes were neither attracted towards the root nor caused any distortions in the four-supergroup tree of life. Their results therefore stem from confusing outgroups with ancestors and handpicking problematic taxa to distort tree reconstruction. In doing so, they ignored the details of our rooting method, taxa sampling rationale, the plethora of evidence given in our study supporting the ancient origin of the viral supergroup and also recent literature on viral evolution. Indeed, our tree of life uncovered many viral monophyletic groups consistent with ICTV classifications and showed remarkable evolutionary tracings of virion morphotypes onto a revealing tree topology.

Evolutionary Biology↗

bioRxiv2016

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes

Sperm cells provide crucial, if usually diminutive, ingredients to successful sexual reproduction as the source of centrioles and half the diploid genome. Despite this essential conserved function, sperm competition and coevolution with female traits can drive spectacular change in size and shape of these motile cells. Here we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Exploring potential genetic and developmental determinants of Caenorhabditis sperm size variation, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes of androdioecious species, as well as within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development, i.e. at the formation of primary spermatocytes while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter-and intraspecific sperm size differences in Caenorhabditis. Together, our results provide a novel integrative view on the developmental and evolutionary origins of Caenorhabditis sperm size variation. We hypothesize that life history and/or ecological differences among species favoured the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm, with gigantic sperm potentially providing a means of paternal care via gametic provisioning or as a potent vehicle for sexual conflict over offspring development.

Evolutionary Biology↗

bioRxiv2016

Nuclear and Plastid DNA Sequence-based Molecular Phylogeography of Salvadora oleoides (Salvadoraceae) in Punjab, India

Salvadora oleiodes is a tropical tree species belonging to the little-known family Salvadoraceae and distributed in the arid regions of Africa and Asia. Aims of our study were to trace the microevolutionary legacy of this tree species with the help of sequence-based multi-local phylogeography and to find the comparative placement of family Salvadoraceae within angiosperm clade malvids. A total 20 geographical isolates were collected from different regions of North India, covering a major part of its species range within the Indian Subcontinent. Sequence data from nuclear-encoded Internal Transcribed Spacer region (ITS1-5.8S-ITS2) and plastid-encoded trnL-F spacer region, were generated for this species for the first time in the world. ITS-based Bayesian phylogeographic analysis revealed the existence of four clades while trnL-F spacer based Bayesian analysis revealed one clade for this species distributed in the Indian subcontinent. Between these two loci, ITS revealed more distinct phylogeographic clades, indicating the phylogeographic utility of this locus for the systematics of Salvadoraceae. Phylogenetic analyzes based on trnL-F spacer suggested a synonymy of this species with Salvadora angustifolia. Maximum Likelihood gene tree based on ITS sequence data revealed that Salvadoraceae belongs to Sapindales rather than Brassicales. However, in the gene tree based on trnL-F spacer sequence, this family clustered within Brassicales. An evolutionary congruence of S. oleoides isolates across its range in North India is revealed in this study. Given the conflicting results on the relative placement of Salvadoraceae in Brassicales and Sapindales, the need for further phylogenetic analyses of malvids using supermatrix approach is highlighted.

Evolutionary Biology↗

bioRxiv2016

Urbanization drives parallel adaptive clines in plant populations

Urban areas are a new and increasingly dominant feature of terrestrial landscapes that dramatically alter environments. It is unclear whether wild populations can adapt to the unique challenges presented by urbanization. To address this problem, we sampled the frequency of a Mendelian-inherited trait--cyanogenesis--in white clover (Trifolium repens L.) plants along urbanization gradients in four large cities. Cyanogenesis protects plants from herbivores, but also reduces freezing tolerance. Plants evolved reduced cyanogenesis with increasing proximity to the urban center in three of the four cities. In an experiment, we demonstrate that gradients in herbivore pressure do not cause these clines. Instead, urban areas experience relatively cold minimum winter ground temperatures because of reduced snow cover within cities, which selects against cyanogenesis. Together, our study demonstrates that wild populations exhibit parallel adaptive evolution in response to urbanization, which likely facilitates the persistence of these plants and promotes pollinator abundance and diversity.

Evolutionary Biology↗

bioRxiv2016

Evolutionary mysteries in meiosis.

Meiosis is a key event of sexual life cycles in eukaryotes. Its mechanistic details have been uncovered in several model organisms, and most of its essential features have received various and often contradictory evolutionary interpretations. In this perspective, we present an overview of these often \"weird\" features. We discuss the origin of meiosis (origin of ploidy reduction and recombination, two-step meiosis), its secondary modifications (in polyploids or asexuals, inverted meiosis), its importance in punctuating life cycles (meiotic arrests, epigenetic resetting, meiotic asymmetry, meiotic fairness) and features associated with recombination (disjunction constraints, heterochiasmy, crossover interference and hotspots). We present the various evolutionary scenarios and selective pressures that have been proposed to account for these features, and we highlight that their evolutionary significance often remains largely mysterious. Resolving these mysteries will likely provide decisive steps towards understanding why sex and recombination are found in the majority of eukaryotes.

Evolutionary Biology↗

bioRxiv2016

How life history can sway the fixation probability of mutants

In this work, we study the effects of demographic structure on evolutionary dynamics, when selection acts on reproduction, survival, or both. In contrast with the previously discovered pattern that the fixation probability of a neutral mutant decreases while population becomes younger, we show that a mutant with constant selective advantage may have a maximum or a minimum of the fixation probability in populations with an intermediate fraction of young individuals. This highlights the importance of life history and demographic structure in studying evolutionary dynamics. We also illustrate the fundamental differences between selection on reproduction and on survival when age structure is present. In addition, we evaluate the relative importance of size and structure of the population in determining the fixation probability of the mutant. Our work lays the foundation for studying also density and frequency dependent effects in populations when demographic structures cannot be neglected.

Evolutionary Biology↗

bioRxiv2016

Ecology, molecules and colour: Multivariate species delimitation and conservation of Harlequin poison frogs

AO_SCPLOWBSTRACTC_SCPLOWWe propose a iterative protocol for delimiting species under the generalized lineage concept (GLC) based on the multivariate clustering of morphological, ecological, and genetic data. Our rationale is that the resulting groups should correspond to evolutionarily independent metapopulation lineages because they reflect the common signal of different secondary defining properties (ecological and genetic distinctiveness, morphological diagnosability, etc.), implying the existence of barriers preventing or limiting gene exchange. We applied this method to study a group of highly endangered poison frogs, the Oophaga histrionica complex. In our study case, we use next generation targeted amplicon sequencing to obtain a robust genetic dataset that we then combined with patterns of morphological and ecological divergence. Our analyses revealed the existence of at least five different species in the histrionica complex (three of them new to science) occurring in very small isolated populations outside any protected areas. More broadly, our study exemplifies how transcriptome-based reduction of genomic complexity and multivariate statistical techniques can be integrated to successfully identify species and their boundaries.\n\nIO_SCPLOWNC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWMEMORIAMC_SCPLOW\"I propose that each species has a distinctive life history, which include a series of stages that correspond to some of the named species concepts\"\n\nRichard G. Harrison\n\n1945-2016

Evolutionary Biology↗

bioRxiv2016

Homeostatic responses regulate selfish mitochondrial genome dynamics in C. elegans

Selfish genetic elements have profound biological and evolutionary consequences. Mutant mitochondrial genomes (mtDNA) can be viewed as selfish genetic elements that persist in a state of heteroplasmy despite having potentially deleterious consequences to the organism. We sought to investigate mechanisms that allow selfish mtDNA to achieve and sustain high levels. Here, we establish a large 3.1kb deletion bearing mtDNA variant uaDf5 as a bona fide selfish genome in the nematode Caenorhabditis elegans. Next, using droplet digital PCR to quantify mtDNA copy number, we show that uaDf5 mutant mtDNA replicates in addition to, not at the expense of, wildtype mtDNA. These data suggest existence of homeostatic copy number control for wildtype mtDNA that is exploited by uaDf5 to hitchhike to high frequency. We also observe activation of the mitochondrial unfolded protein response (UPRmt) in animals with uaDf5. Loss of UPRmt results in a decrease in uaDf5 frequency whereas constitutive activation of UPRmt increases uaDf5 levels. These data suggest that UPRmt allows uaDf5 levels to increase. Interestingly, the decreased uaDf5 levels in absence of UPRmt recover in parkin mutants lacking mitophagy, suggesting that UPRmt protects uaDf5 from mitophagy. We propose that cells activate two homeostatic responses, mtDNA copy number control and UPRmt, in uaDf5 heteroplasmic animals. Inadvertently, these homeostatic responses allow uaDf5 levels to be higher than they would be otherwise. In conclusion, our data suggest that homeostatic stress response mechanisms play an important role in regulating selfish mitochondrial genome dynamics.

Genetics↗

bioRxiv2016

Pyricularia graminis-tritici sp. nov., a new Pyricularia species causing wheat blast

Abstract Pyricularia oryzae is a species complex that causes blast disease on more than 50 species of poaceous plants. Pyricularia oryzae has a worldwide distribution as a rice (Oryza) pathogen and in the last 30 years emerged as an important wheat (Triticum) pathogen in southern Brazil. We conducted phylogenetic analyses using 10 housekeeping loci for 128 isolates of P. oryzae sampled from sympatric populations of grasses growing in or near wheat fields. Phylogenetic analyses grouped the isolates into three major clades. Clade 1 comprised isolates associated only with rice and corresponds to the previously described rice blast pathogen P. oryzae pathotype Oryza (PoO). Clade 2 comprised isolates associated almost exclusively with wheat and corresponds to the previously described wheat blast pathogen P. oryzae pathotype Triticum (PoT). Clade 3 contained isolates obtained from wheat as well as other Poaceae hosts. We found that Clade 3 is distinct from P. oryzae and represents a new species, Pyricularia graminis-tritici, (Pgt). No morphological differences were observed among these species, but a distinctive pathogenicity spectrum was observed. Pgt and PoT were pathogenic and highly aggressive on Triticum aestivum (wheat), Hordeum vulgare (barley), Urochloa brizantha (signal grass) and Avena sativa (oats). PoO was highly virulent on the original rice host (Oryza sativa), and also on wheat, barley, and oats, but not on signal grass. We conclude that blast disease on wheat and its associated Poaceae hosts in Brazil is caused by multiple Pyricularia species. Pyricularia graminis-tritici was recently found causing wheat blast in Bangladesh. This indicates that P. graminis-tritici represents a serious threat to wheat cultivation globally.

Evolutionary Biology↗

bioRxiv2016

Adaptively introgressed Neandertal haplotype at the OAS locus functionally impacts innate immune responses in humans.

The 2-5 oligoadenylate synthetase (OAS) locus encodes for three OAS enzymes (OAS1-3) involved in innate immune response. This region harbors high amounts of Neandertal ancestry in non-African populations; yet, strong evidence of positive selection in the OAS region is still lacking. Here we used a broad array of selection tests in concert with neutral coalescent simulations to firmly demonstrate a signal of adaptive introgression at the OAS locus. Furthermore, we characterized the functional consequences of the Neandertal haplotype in the transcriptional regulation of OAS genes at baseline and infected conditions. We found that cells from people with the Neandertal-like haplotype express lower levels of OAS3 upon infection, as well as distinct isoforms of OAS1 and OAS2. Notably, the Neandertal-introgressed haplotype reintroduced an ancestral splice variant of OAS1 encoding a more active protein, suggesting that adaptive introgression occurred as a means to resurrect adaptive variation that had been lost outside Africa.

Evolutionary Biology↗

bioRxiv2016

Consensus Phylogenetic trees of Fifteen Prokaryotic Aminoacyl-tRNA Synthetase Polypeptides based on Euclidean Geometry of All-Pairs Distances and Concatenation

BackgroundMost molecular phylogenetic trees depict the relative closeness or the extent of similarity among a set of taxa based on comparison of sequences of homologous genes or proteins. Since the tree topology for individual monogenic traits varies among the same set of organisms and does not overlap taxonomic hierarchy, hence there is a need to generate multidimensional phylogenetic trees.\n\nResultsPhylogenetic trees were constructed for 119 prokaryotes representing 2 phyla under Archaea and 11 phyla under Bacteria after comparing multiple sequence alignments for 15 different aminoacyl-tRNA synthetase polypeptides. The topology of Neighbor Joining (NJ) trees for individual tRNA synthetase polypeptides varied substantially. We use Euclidean geometry to estimate all-pairs distances in order to construct phylogenetic trees. Further, we used a novel \"Taxonomic fidelity\" algorithm to estimate clade by clade similarity between the phylogenetic tree and the taxonomic tree. We find that, as compared to trees for individual tRNA synthetase polypeptides and rDNA sequences, the topology of our Euclidean tree and that for aligned and concatenated sequences of 15 proteins are closer to the taxonomic trees and offer the best consensus. We have also aligned sequences after concatenation, and find that by changing the order of sequence joining prior to alignment, the tree topologies vary. In contrast, changing the types of polypeptides in the grouping for Euclidean trees does not affect the tree topologies.\n\nConclusionsWe show that a consensus phylogenetic tree of 15 polypeptides from 14 aminoacyl-tRNA synthetases for 119 prokaryotes using Euclidean geometry exhibits better taxonomic fidelity than trees for individual tRNA synthetase polypeptides as well as 16S rDNA. We have also examined Euclidean N-dimensional trees for 15 tRNA synthetase polypeptides which give the same topology as that constructed after amalgamating 3-dimensional Euclidean trees for groups of 3 polypeptides. Euclidean N-dimensional trees offer a reliable future to multi-genic molecular phylogenetics.

Evolutionary Biology↗

bioRxiv2016

Estimating effective population size from temporal allele frequency changes in experimental evolution

The effective population size (Ne) is a major factor determining allele frequency changes in natural and experimental populations. Temporal methods provide a powerful and simple approach to estimate short-term Ne. They use allele frequency shifts between temporal samples to calculate the standardized variance, which is directly related to Ne. Here we focus on experimental evolution studies that often rely on repeated sequencing of samples in pools (Pool-Seq). Pool-Seq is cost-effective and outperforms individual-based sequencing in estimating allele frequencies, but it is associated with atypical sampling properties: additional to sampling individuals, sequencing DNA in pools leads to a second round of sampling increasing the estimated allele frequency variance. We propose a new estimator of Ne, which relies on allele frequency changes in temporal data and corrects for the variance in both sampling steps. In simulations, we obtain accurate Ne estimates, as long as the drift variance is not too small compared to the sampling and sequencing variance. In addition to genome-wide Ne estimates, we extend our method using a recursive partitioning approach to estimate Ne locally along the chromosome. Since type I error is accounted for, our method permits the identification of genomic regions that differ significantly in Ne. We present an application to Pool-Seq data from experimental evolution with Drosophila, and provide recommendations for whole-genome data. The estimator is computationally efficient and available as an R-package at https://github.com/ThomasTaus/Nest.

Evolutionary Biology↗

bioRxiv2016

Separating spandrels from phenotypic targets of selection in adaptive molecular evolution

There are many examples of adaptive molecular evolution in natural populations, but there is no existing method to verify which phenotypic changes were directly targeted by selection. The problem is that correlations between traits make it difficult to distinguish between direct and indirect selection. A phenotype is a direct target of selection when that trait in particular was shaped by selection to better perform a function. An indirect target of selection, also known as an evolutionary spandrel, is a phenotype that changes only because it is correlated with another trait under direct selection. Studies that mutate genes and examine the phenotypic consequences are increasingly common, and these experiments could estimate the mutational accessibility of the phenotypic changes that arise during an instance of adaptive molecular evolution. Under indirect selection, we expect phenotypes to evolve toward states that are more accessible by mutation. Deviation from this null expectation (evolution toward a phenotypic state rarely produced by mutation) would be compelling evidence of adaptation, and could be used to distinguish direct selection from indirect selection on correlated traits. To be practical, this molecular test of adaptation requires phenotypic differences that are caused by changes in a small number of genes. These kinds of genetically simple traits have been observed in many empirical studies of adaptive evolution. Here we describe how to use mutational accessibility to separate spandrels from direct targets of selection and thus verify adaptive hypotheses for phenotypes that evolve by adaptive molecular changes at one or a few genes.

Evolutionary Biology↗

bioRxiv2016

From epigenetic landscape to phenotypic fitness landscape: evolutionary effect of pathogens on host traits

The epigenetic landscape illustrates how cells differentiate into different types through the control of gene regulatory networks. Numerous studies have investigated epigenetic gene regulation but there are limited studies on how the epigenetic landscape and the presence of pathogens influence the evolution of host traits. Here we formulate a multistable decision-switch model involving many possible phenotypes with the antagonistic influence of parasitism. As expected, pathogens can drive dominant (common) phenotypes to become inferior, such as through negative frequency-dependent selection. Furthermore, novel predictions of our model show that parasitism can steer the dynamics of phenotype specification from multistable equilibrium convergence to oscillations. This oscillatory behavior could explain pathogen-mediated epimutations and excessive phenotypic plasticity. The Red Queen dynamics also occur in certain parameter space of the model, which demonstrates winnerless cyclic phenotype-switching in hosts and in pathogens. The results of our simulations elucidate how epigenetic landscape is associated with the phenotypic fitness landscape and how parasitism facilitates non-genetic phenotypic diversity.

Evolutionary Biology↗

bioRxiv2016

Adaptation in isolated populations: when does it happen and when can we tell?

Isolated populations with novel phenotypes present an exciting opportunity to uncover the genetic basis of ecologically significant adaptation, and genomic scans for positive selection in such populations have often, but not always, led to candidate genes directly related to an adaptive phenotype. However, in many cases these populations were established by a severe bottleneck, which can make identifying targets of selection problematic. Here we simulate severe bottlenecks and subsequent selection on standing variation, mimicking adaptation after establishment of a new small population, such as an island or an artificial selection experiment. Using simulations of single loci under positive selection and population genetics theory, we examine how population size and age of the population isolate affects the ability of outlier scans for selection to identify adaptive alleles using both single site measures and haplotype structure. We find and explain an optimal combination of selection strength, starting frequency, and age of the adaptive allele, which we refer to as a Goldilocks zone, where adaptation is likely to occur, and yet the adaptive variants are most likely to derive from a single ancestor (a \"hard\" selective sweep); in this zone, four commonly used statistics detect selection with high power. Real-world examples of both island colonization and experimental evolution studies are discussed. Our study provides concrete considerations to be made before embarking on whole genome sequencing of differentiated populations.

Evolutionary Biology↗

bioRxiv2016

On the evolutionary origins of equity

Equity, defined as reward according to contribution, is considered a central aspect of human fairness in both philosophical debates and scientific research. Despite large amounts of research on the evolutionary origins of fairness, the evolutionary rationale behind equity is still unknown. Here, we investigate how equity can be understood in the context of the cooperative environment in which humans evolved. We model a population of individuals who cooperate to produce and divide a resource, and choose their cooperative partners based on how they are willing to divide the resource. Agent-based simulations, an analytical model, and extended simulations using neural networks provide converging evidence that equity is the best evolutionary strategy in such an environment: individuals maximize their fitness by dividing benefits in proportion to their own and their partners relative contribution. The need to be chosen as a cooperative partner thus creates a selection pressure strong enough to explain the evolution of preferences for equity. We discuss the limitations of our model, the discrepancies between its predictions and empirical data, and how interindividual and intercultural variability fit within this framework.

Evolutionary Biology↗

bioRxiv2016

Male density and rapid evolution of genital morphology in the seed beetle Callosobruchus maculatus

Male reproductive structures are known to be extremely diverse, particularly in insect taxa. Male genital structures are thought to be some of the fastest evolving traits, but the processes responsible for this pattern remain unclear. In the present study we manipulated the mating regimes of Callosobruchus maculatus, a seed beetle, to determine if male genital structures would be altered under forced monogamy and polyandry. Males in this species have an intromittent organ that contains spines that are known to puncture the female reproductive tract. We measured both testes size and genital spine length in monogamous and polyandrous treatments over seven generations. We found that testes size was not significantly different between treatments, but that genital spine length was significantly longer in the polyandrous treatment within seven generations. These results highlight the fact that evolution can occur rapidly when under strong sexual selection, a process that has been implicated in leading to morphological differences in male genitalia.

Evolutionary Biology↗