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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↗

bioRxiv2016

DIVERGENT IMMUNE PRIMING RESPONSES ACROSS FLOUR BEETLE LIFE STAGES AND POPULATIONS

Growing evidence shows that low doses of pathogens may prime the immune response in many insects, conferring subsequent protection against infection in the same developmental stage (within life stage priming), across life stages (ontogenic priming), or to offspring (trans-generational priming). Recent work also suggests that immune priming is a costly response. Thus, depending on host and pathogen ecology and evolutionary history, tradeoffs with other fitness components may constrain the evolution of priming. However, the relative impacts of priming at different life stages and across natural populations remain unknown. We quantified immune priming responses of 10 natural populations of the red flour beetle Tribolium castaneum, primed and infected with the natural insect pathogen Bacillus thuringiensis. We found that priming responses were highly variable both across life stages and populations, ranging from no detectable response to a 13-fold survival benefit. Comparing across stages, we found that ontogenic immune priming at the larval stage conferred maximum protection against infection. Finally, we found that various forms of priming showed sex-specific associations that may represent tradeoffs or shared mechanisms. These results suggest that sex-, life stage-, and pathogen-specific selective pressures can cause substantial divergence in priming responses even within a species. Our work highlights the necessity of further work to understand the mechanistic basis of this variability.

Evolutionary Biology↗

bioRxiv2016

Efficient Maximum-Likelihood Inference For The Isolation-With-Initial-Migration Model With Potentially Asymmetric Gene Flow

The isolation-with-migration (IM) model is commonly used to make inferences about gene flow during speciation, using polymorphism data. However, Becquet and Przeworski (2009) report that the parameter estimates obtained by fitting the IM model are very sensitive to the model's assumptions (including the assumption of constant gene flow until the present). This paper is concerned with the isolation-with-initial-migration (IIM) model of Wilkinson-Herbots (2012), which drops precisely this assumption. In the IIM model, one ancestral population divides into two descendant subpopulations, between which there is an initial period of gene flow and a subsequent period of isolation. We derive a very fast method of fitting an extended version of the IIM model, which also allows for asymmetric gene flow and unequal population sizes. This is a maximum-likelihood method, applicable to data on the number of segregating sites between pairs of DNA sequences from a large number of independent loci. In addition to obtaining parameter estimates, our method can also be used to distinguish between alternative models representing different evolutionary scenarios, by means of likelihood ratio tests. We illustrate the procedure on pairs of Drosophila sequences from approximately 30,000 loci. The computing time needed to fit the most complex version of the model to this data set is only a couple of minutes. The R code to fit the IIM model can be found in the supplementary files of this paper.

Evolutionary Biology↗

bioRxiv2016

The last common ancestor of most bilaterian animals possessed at least 9 opsins

The opsin gene family encodes key proteins animals use to sense light and has expanded dramatically since it originated early in animal evolution. Understanding the origins of opsin diversity can offer clues to how separate lineages of animals have repurposed different opsin paralogs for different light-detecting functions. However, the more we look for opsins outside of eyes and from additional animal phyla, the more opsins we uncover, suggesting we still do not know the true extent of opsin diversity, nor the ancestry of opsin diversity in animals. To estimate the number of opsin paralogs present in both the last common ancestor of the Nephrozoa (bilaterians excluding Xenoacoelomorpha), and the ancestor of Cnidaria + Bilateria, we reconstructed a reconciled opsin phylogeny using sequences from 14 animal phyla, especially the traditionally poorly-sampled echinoderms and molluscs. Our analysis strongly supports a repertoire of at least nine opsin paralogs in the bilaterian ancestor and at least four opsin paralogs in the last common ancestor of Cnidaria + Bilateria. Thus, the kernels of extant opsin diversity arose much earlier in animal history than previously known. Further, opsins likely duplicated and were lost many times, with different lineages of animals maintaining different repertoires of opsin paralogs. This phylogenetic information can inform hypotheses about the functions of different opsin paralogs and be used to understand how and when opsins were incorporated into complex traits like eyes and extraocular sensors.

Evolutionary Biology↗

bioRxiv2016

Soft selective sweeps in evolutionary rescue

Evolutionary rescue occurs when a population that is declining in size because of an environmental change is rescued by genetic adaptation. Evolutionary rescue is an important phenomenon at the intersection of ecology and population genetics. While most population genetic models of evolutionary rescue focus on estimating the probability of rescue, we focus on whether one or more adaptive lineages contribute to evolutionary rescue. We find that when evolutionary rescue is likely, it is often driven by soft selective sweeps where multiple adaptive mutations spread through the population simultaneously. We give full analytic results for the probability of evolutionary rescue and the probability that evolutionary rescue occurs via soft selective sweeps in our model. We expect that these results will find utility in understanding the genetic signatures associated with various evolutionary rescue scenarios in large populations, such as the evolution of drug resistance in viral, bacterial, or eukaryotic pathogens.

Evolutionary Biology↗

bioRxiv2016

Resource limitation reveals a twofold benefit of eusociality

Explaining the evolution and maintenance of cooperative breeding or eusociality remains a challenge. Surprisingly, fundamental ecological factors, specifically competition for limited resources and resource variance, are frequently ignored in models of animal sociality. We here develop a mathematical model that includes density-dependent population growth and quantify the influence of cooperative foraging on resource use efficiency. We derive optimal resource sharing strategies, ranging from egalitarian to cooperatively breeding and eusocial groups. We find that, while egalitarian resource sharing is a risk-reducing foraging strategy, eusociality yields additional benefits: like egalitarian strategies, eusocial groups can reduce their members starvation risk by reducing resource variance. Additionally, eusocial groups increase their reproductive output by increasing intra-group variance in resources allocated to reproduction. This allows reproduction even when resources are so scarce that solitary animals would not be able to reproduce. In a majority of environmental situations and life-histories, this twofold benefit of eusociality increased resource use efficiency and led to supersaturation, that is, to a strong increase in carrying capacity. Supersaturation provides indirect benefits to group members even for low intra-group relatedness and represents one potential explanation for the evolution and maintenance of eusociality and cooperative breeding.

Evolutionary Biology↗

bioRxiv2016

Seed size and its rate of evolution correlate with species diversification across angiosperms

Species diversity varies greatly across the different taxonomic groups that comprise the Tree of Life (ToL). This imbalance is particularly conspicuous within angiosperms, but is largely unexplained. Seed mass is one trait that may help clarify why some lineages diversify more than others because it confers adaptation to different environments, which can subsequently influence speciation and extinction. The rate at which seed mass changes across the angiosperm phylogeny may also be linked to diversification by increasing reproductive isolation and allowing access to novel ecological niches. However, the magnitude and direction of the association between seed mass and diversification has not been assessed across the angiosperm phylogeny. Here, we show that absolute seed size and the rate of change in seed size are both associated with variation in diversification rates. Based on the largest available angiosperm phylogenetic tree, we found that smaller-seeded plants had higher rates of diversification, possibly due to improved colonisation potential. The rate of phenotypic change in seed size was also strongly positively correlated with speciation rates, providing rare, large-scale evidence that rapid morphological change is associated with species divergence. Our study now reveals that variation in morphological traits and, importantly, the rate at which they evolve can contribute to explaining the extremely uneven distribution of diversity across the ToL.

Evolutionary Biology↗

bioRxiv2016

The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. Alternatively, genome-wide hybridization resulting from hybrid swarm may be the trigger. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.

Evolutionary Biology↗

bioRxiv2016

Corticosteroid and progesterone transactivation of mineralocorticoid receptors from Amur sturgeon and tropical gar

The response to a panel of steroids by the mineralocorticoid receptor (MR) from Amur sturgeon and tropical gar, two basal ray-finned fish, expressed in HEK293 cells was investigated. Half-maximal responses (EC50s) for transcriptional activation of sturgeon MR by 11-deoxycorticosterone, corticosterone, 11-deoxycortisol, cortisol and aldosterone, and progesterone were between 13 pM and 150 pM. For gar MR, EC50s were between 8 pM and 55 pM. Such low EC50s support physiological regulation by these steroids of the MR in sturgeon and gar. Companion studies with human MR and zebrafish MR found higher EC50s compared to EC50s for sturgeon and gar MR, with EC50s for zebrafish MR closer to gar and sturgeon MR than was human MR. For zebrafish MR, EC50s were between 75 pM and 740 pM; for human MR, EC50s were between 65 pM and 2 nM. In addition to progesterone, spironolactone and 19nor-progesterone were agonists for all three fish MRs, in contrast to their antagonist activity for human MR, which is hypothesized to involve serine-810 in human MR because all three steroids are agonists for a mutant human Ser810Leu-MR. Paradoxically, sturgeon, gar and zebrafish MRs contain a serine corresponding to serine-810 in human MR. Our data suggests alternative mechanism(s) for progesterone, spironolactone and 19nor-progesterone as MR agonists in these three ray-finned fishes and the need for caution in applying data for progesterone signaling in zebrafish to human physiology.

Evolutionary Biology↗