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bioRxiv2016

Haplotype block dynamics in hybrid populations

When species originate through hybridization, the genomes of the ancestral species are blended together. Over time genomic blocks that originate from either one of the ancestral species accumulate in the hybrid genome through genetic recombination. Modeling the accumulation of ancestry blocks can elucidate processes and patterns of genomic admixture. However, previous models have ignored ancestry block dynamics for chromosomes that consist of a discrete, finite number of chromosomal elements. Here we present an analytical treatment of the dynamics of the mean number of blocks over time, for continuous and discrete chromosomes, in finite and infinite populations. We describe the mean number of haplotype blocks as a universal function dependent on population size, the number of genomic elements per chromosome, the number of recombination events, and the initial relative frequency of the ancestral species.

Evolutionary Biology↗

bioRxiv2016

Gene-tree reconciliation with MUL-trees to resolve polyploidy events

Polyploidy can have a huge impact on the evolution of species, and it is a common occurrence, especially in plants. The two types of polyploids - autopolyploids and allopolyploids - differ in the level of divergence between the genes that are brought together in the new polyploid lineage. Because allopolyploids are formed via hybridization, the homoeologous copies of genes within them are at least as divergent as orthologs in the parental species that came together to form them. This means that common methods for estimating the parental lineages of allopolyploidy events are not accurate, and can lead to incorrect inferences about the number of gene duplications and losses. Here, we have adapted an algorithm for topology-based gene-tree reconciliation to work with multi-labeled trees (MUL-trees). By definition, MUL-trees have some tips with identical labels, which makes them a natural representation of the genomes of polyploids. Using this new reconciliation algorithm we can: accurately place allopolyploidy events on a phylogeny, identify the parental lineages that hybridized to form allopolyploids, distinguish between allo-, auto-, and (in most cases) no polyploidy, and correctly count the number of duplications and losses in a set of gene trees. We validate our method using gene trees simulated with and without polyploidy, and revisit the history of polyploidy in data from the clades including both bakers yeast and bread wheat. Our re-analysis of the yeast data confirms the allopolyploid origin and parental lineages previously identified for this group. The method presented here should find wide use in the growing number of genomes from species with a history of polyploidy.

Evolutionary Biology↗

bioRxiv2016

Evolution of resistance against CRISPR/Cas9 gene drive

The idea of driving genetically modified alleles to fixation in a population has fascinated scientists for over 40 years1,2. Potential applications are broad and ambitious, including the eradication of disease vectors, the control of pest species, and the preservation of endangered species from extinction3. Until recently, these possibilities have remained largely abstract due to the lack of an effective drive mechanism. CRISPR/Cas9 gene drive (CGD) now promise a highly adaptable approach for driving even deleterious alleles to high population frequency, and this approach was recently shown to be effective in small laboratory populations of insects4-7. However, it remains unclear whether CGD will also work in large natural populations in the face of potential resistance mechanisms. Here we show that resistance against CGD will inevitably evolve unless populations are small and repair of CGD-induced cleavage via nonhomologous end joining (NHEJ) can be effectively suppressed, or resistance costs are on par with those of the driver. We specifically calculate the probability that resistance evolves from variants at the target site that are not recognized by the driver's guide RNA, either because they are already present when the driver allele is introduced, arise by de novo mutation, or are created by the driver itself when NHEJ introduces mutations at the target site. Our results shed light on strategies that could facilitate the engineering of a successful drive by lowering resistance potential, as well as strategies that could promote resistance as a possible mechanism for controlling a drive. This study highlights the need for careful modeling of CGD prior to the actual release of a driver construct into the wild.

Evolutionary Biology↗

bioRxiv2016

Deciphering the wisent demographic and adaptive histories from individual whole-genome sequences

As the largest European herbivore, the wisent (Bison bonasus) is emblematic of the continent wildlife but has unclear origins. Here, we infer its demographic and adaptive histories from two individual whole genome sequences via a detailed comparative analysis with bovine genomes. We estimate that the wisent and bovine species diverged from 1.7x106 to 850,000 YBP through a speciation process involving an extended period of limited gene flow. Our data further support the occurrence of more recent secondary contacts, posterior to the Bos taurus and Bos indicus divergence (ca. 150,000 YBP), between the wisent and (European) taurine cattle lineages. Although the wisent and bovine population sizes experienced a similar sharp decline since the Last Glacial Maximum, we find that the wisent demography remained more fluctuating during the Pleistocene. This is in agreement with a scenario in which wisents responded to successive glaciations by habitat fragmentation rather than southward and eastward migration as for the bovine ancestors.\n\nWe finally detect 423 genes under positive selection between the wisent and bovine lineages, which shed a new light on the genome response to different living conditions (temperature, available food resource and pathogen exposure) and on the key gene functions altered by the domestication process.

Evolutionary Biology↗

bioRxiv2016

Lazarus effects: the frequency and genetic causes of Escherichia coli population recovery under lethal heat stress

Sometimes populations crash and yet recover before being lost completely. Such recoveries have been observed incidentally in evolution experiments using Escherichia coli, and this phenomenon has been termed the \"Lazarus effect.\" To investigate how often recovery occurs and the genetic changes that drive it, we evolved ~300 populations of E. coli at lethally high temperatures (43.0{degrees}) for five days and sequenced the genomes of recovered populations. Our results revealed that the Lazarus effect is uncommon, but frequent enough, at ~9% of populations, to be a potent source of evolutionary innovation. Population sequencing uncovered a set of mutations adaptive to lethal 43.0{degrees}C that were mostly distinct from those that were beneficial at a high but nonlethal temperature (42.2{degrees}). Mutations within two operons--the heat shock hslUV operon and the RNA polymerase rpoBC operon--drove adaptation to lethal temperature. Mutations in hslUV exhibited little antagonistic pleiotropy at 37.0{degrees}C and may have arisen neutrally prior to subjection to lethal temperature. In contrast, rpoBC mutations provided greater fitness benefits than hslUV mutants, but were less prevalent and caused stronger fitness tradeoffs at lower temperatures. Recovered populations fixed mutations in only one operon or the other, but not both, indicating that epistatic interactions between beneficial mutations were important even at the earliest stages of adaptation.

Evolutionary Biology↗

bioRxiv2016

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Temporal collinearity is often regarded as the force preserving Hox clusters in vertebrate genomes. Studies that combine genomic and gene expression data in invertebrates would allow generalizing this observation across all animals, but are scarce, particularly within Lophotrochozoa (e.g., snails and segmented worms). Here, we use two brachiopod species -Terebratalia transversa, Novocrania anomala- to characterize the complement, cluster and expression of their Hox genes. T. transversa has an ordered, split cluster with ten genes (lab, pb, Hox3, dfd, scr, lox5, antp, lox4, post2, post1), while N. anomala has nine (missing post1). Our in situ hybridization, qPCR and stage specific transcriptomic analyses show that brachiopod Hox genes are neither strictly temporally nor spatially collinear; only pb (in T. transversa), Hox3 and dfd (in both brachiopods) show staggered mesodermal expression. The spatial expression of the Hox genes in both brachiopod species correlates with their morphology and demonstrates cooption of Hox genes in the chaetae and shell fields, two major lophotrochozoan morphological novelties. The shared and specific expression of a subset of Hox genes, Arx and Zic orthologs in chaetae and shell-fields between brachiopods, mollusks, and annelids supports the deep conservation of the molecular basis forming these lophotrochozoan hallmarks. Our findings challenge that collinearity alone preserves lophotrochozoan Hox clusters, indicating that additional genomic traits need to be considered in understanding Hox evolution.

Evolutionary Biology↗

bioRxiv2016

A logic approach to modeling nomenclatural change

We utilize an Answer Set Programming (ASP) approach to show that the principles of nomenclature are tractable in computational logic. To this end we design a hypothetical, 20 nomenclatural taxon use case with starting conditions that embody several overarching principles of the International Code of Zoological Nomenclature; including Binomial Nomenclature, Priority, Coordination, Homonymy, Typification, and the structural requirement of Gender Agreement. The use case ending conditions are triggered by the reinterpretation of the diagnostic features of one of 12 type specimens anchoring the corresponding species-level names. Permutations of this child-to-parent reassignment action lead to 36 alternative scenarios, where each scenario requires 1-14 logically contingent nomenclatural emendations. We show that an ASP transition system approach can correctly infer the Code-mandated changes for each scenario, and visually output the ending conditions. The results provide a foundation for further developing logic-based nomenclatural change optimization and compliance verification services, which could be applied in globally coordinated nomenclatural registries. More generally, logic explorations of nomenclatural and taxonomic change scenarios provide a novel means of assessing design biases inherent in the principles of nomenclature, and thus may inform the design of future, big data-compatible identifier systems for systematic products that recognize and mitigate these constraints.

Evolutionary Biology↗

bioRxiv2016

A genomic view of the peopling of the Americas

Whole-genome studies have documented that most Native American ancestry stems from a single population that diversified within the continent more than twelve thousand years ago. However, this shared ancestry hides a more complex history whereby at least four distinct streams of Eurasian migration have contributed to present-day and prehistoric Native American populations. Whole genome studies enhanced by technological breakthroughs in ancient DNA now provide evidence of a sequence of events involving initial migration from a structured Northeast Asian source population, followed by a divergence into northern and southern Native American lineages. During the Holocene, new migrations from Asia introduced the Saqqaq/Dorset Paleoeskimo population to the North American Arctic ~4,500 years ago, ancestry that is potentially connected with ancestry found in Athabaskan-speakers today. This was then followed by a major new population turnover in the high Arctic involving Thule-related peoples who are the ancestors of present-day Inuit. We highlight several open questions that could be addressed through future genomic research.

Evolutionary Biology↗

bioRxiv2016

Programmed cell death can increase the efficacy of microbial bet-hedging

Programmed cell death (PCD) occurs in both unicellular and multicellular organisms. While PCD plays a key role in the development and maintenance of multicellular organisms, explaining why single-celled organisms would evolve to actively commit suicide has been far more challenging. Here, we explore the potential for PCD to act as an accessory to microbial bet-hedging strategies that utilize stochastic phenotype switching. We consider organisms that face unpredictable and recurring disasters, in which fitness depends on effective phenotypic diversification. We show that when reproductive opportunities are limited by carrying capacity, PCD drives population turnover, providing increased opportunities for phenotypic diversification through stochastic phenotype switching. The main cost of PCD, providing resources for growth to a PCD(-) competitor, is ameliorated by genetic assortment driven by population spatial structure. Using three dimensional agent based simulations, we explore how basic demographic factors, namely cell death and clonal reproduction, can create populations with sufficient spatial structure to favor the evolution of high PCD rates.

Evolutionary Biology↗

bioRxiv2016

Bayesian inference of ancestral recombination graphs for bacterial populations

Homologous recombination is a central feature of bacterial evolution, yet confounds traditional phylogenetic methods. While a number of methods specific to bacterial evolution have been developed, none of these permit joint inference of a bacterial recombination graph and associated parameters. In this paper, we present a new method which addresses this shortcoming. Our method uses a novel Markov chain Monte Carlo algorithm to perform phylogenetic inference under the ClonalOrigin model of Didelot et al. (Genetics, 2010). We demonstrate the utility of our method by applying it to rMLST data sequenced from pathogenic and non-pathogenic Escherichia coli serotype O157 and O26 isolates collected in rural New Zealand. The method is implemented as an open source BEAST 2 package, Bacter, which is available via the project web page at http://tgvaughan.github.io/bacter.

Evolutionary Biology↗

bioRxiv2016

Monogamy promotes worker sterility in insect societies

Inclusive-fitness theory highlights monogamy as a key driver of altruistic sib-rearing. Accordingly, monogamy should promote the evolution of worker sterility in social insects when sterile workers make for better helpers. However, a recent population-genetics analysis (Olejarz et al. 2015) found no clear effect of monogamy on worker sterility. Here, we revisit this analysis. First, we relax genetic assumptions, considering not only alleles of extreme effect--encoding either no sterility or complete sterility--but also alleles with intermediate worker-sterility effects. Second, we broaden the stability analysis--which focused on the invasibility of populations where either all workers are fully-sterile or all workers are fully-reproductive--to identify where intermediate pure or mixed evolutionarily-stable states may occur. Finally, we consider additional, demographically-explicit ecological scenarios relevant to worker non-reproduction. This extended analysis demonstrates that an exact population-genetics approach strongly supports the prediction of inclusive-fitness theory that monogamy promotes sib-directed altruism in social insects.

Evolutionary Biology↗

bioRxiv2016

The Evolutionary Trade-off between Stem Cell Niche Size, Aging, and Tumorigenesis

Many epithelial tissues within large multicellular organisms are continually replenished by small independent populations of stem cells. These stem cells divide within their niches and differentiate into the constituent cell types of the tissue, and are largely responsible for maintaining tissue homeostasis. Mutations can accumulate in stem cell niches and change the rate of stem cell division and differentiation, contributing to both aging and tumorigenesis. Here, we create a mathematical model of the intestinal stem cell niche, crypt system, and epithelium. We calculate the expected effect of fixed mutations in stem cell niches and their expected effect on tissue homeostasis throughout the intestinal epithelium over the lifetime of an organism. We find that, due to the small population size of stem cell niches, fixed mutations are expected to accumulate via genetic drift and decrease stem cell fitness, leading to niche and tissue attrition, and contributing to organismal aging. We also explore mutation accumulation at various stem cell niche sizes, and demonstrate that an evolutionary trade-off exists between niche size, tissue aging, and the risk of tumorigenesis; where niches exist at a size that minimizes the probability of tumorigenesis, at the expense of accumulating deleterious mutations due to genetic drift. Finally, we show that the probability of tumorigenesis and the extent of aging trade-off differently depending on whether mutational effects confer a selective advantage, or not, in the stem cell niche.

Evolutionary Biology↗

bioRxiv2016

Shedding light on the grey zone of speciation along a continuum of genomic divergence

Speciation results from the progressive accumulation of mutations that decrease the probability of mating between parental populations, or reduce the fitness of hybrids - the so-called species barriers. The speciation genomic literature, however, is mainly a collection of case studies, each with its own approach and specificities, such that a global view of the gradual process of evolution from one to two species is currently lacking. Of primary importance is the prevalence of gene flow between diverging entities, which is central in most species concepts, and has been widely discussed in recent years. Here we explore the continuum of speciation thanks to a comparative analysis of genomic data from 61 pairs of populations/species of animals with variable levels of divergence. Gene flow between diverging gene pools is assessed under an Approximate Bayesian Computation (ABC) framework. We show that the intermediate \"grey zone\" of speciation, in which taxonomy is often controversial, spans from 0.5% to 2% of net synonymous divergence, irrespective of species life-history traits or ecology. Thanks to appropriate modeling of among-loci variation in genetic drift and introgression rate, we clarify the status of the majority of ambiguous cases and uncover a number of cryptic species. Our analysis also reveals the high incidence in animals of semi-isolated species, when some but not all loci are affected by barriers to gene flow, and highlights the intrinsic difficulty, both statistical and conceptual, of delineating species in the grey zone of speciation.

Evolutionary Biology↗

bioRxiv2016

Temperature-induced transcriptional responses of the deep-biosphere bacterium, Kosmotoga olearia, illuminate its adaptation to growth from 20 ° to 79°

Temperature is one of the defining parameters of an ecological niche. Most organisms thrive within a temperature range that rarely exceeds [~] 30{degrees}C, but the deep subsurface bacterium Kosmotoga olearia can grow over a temperature range of 59{degrees}C (20{degrees}C -79{degrees}C). To identify genes correlated with this flexible phenotype, we compared transcriptomes of K. olearia cultures grown at its optimal 65{degrees}C to those at 30{degrees}C, 40{degrees}C, and 77{degrees}C. The temperature treatments affected expression of 573 of 2,224 K. olearia genes. Notably, this transcriptional response elicits re-modeling of the cellular membrane and changes in metabolism, with increased expression of genes involved in energy and carbohydrate metabolism at high temperatures and up-regulation of amino acid metabolism at lower temperatures. At sub-optimal temperatures, many transcriptional changes were similar to those observed in mesophilic bacteria at physiologically low temperatures, including up-regulation of typical cold stress genes and ribosomal proteins. Comparative genomic analysis of additional Thermotogae genomes, indicate that one of K. olearia's strategies for low temperature growth is increased copy number of some typical cold response genes through duplication and/or lateral acquisition. At 77{degrees}C one third of the up-regulated genes are of hypothetical function, indicating that many features of high temperature growth are unknown.

Evolutionary Biology↗

bioRxiv2016

Cryptic genetic differentiation of the sex-determining chromosome in the mosquito Aedes aegypti

Mechanisms and evolutionary dynamics of sex-determination systems are of particular interest in insect vectors of human pathogens like mosquitoes because novel control strategies aim to convert pathogen-transmitting females into non-biting males, or rely on accurate sexing for the release of sterile males. In Aedes aegypti, the main vector of dengue and Zika viruses, sex determination is governed by a dominant male-determining locus, previously thought to reside within a small, non-recombining, sex-determining region (SDR) of an otherwise homomorphic sex chromosome. Here, we provide evidence that sex chromosomes in Ae. aegypti are genetically differentiated between males and females over a region much larger than the SDR. Our linkage mapping intercrosses failed to detect recombination between X and Y chromosomes over a 123-Mbp region (40% of their physical length) containing the SDR. This region of reduced male recombination overlapped with a smaller 63-Mbp region (20% of the physical length of the sex chromosomes) displaying high male-female genetic differentiation in unrelated wild population from Brazil and Australia and in a reference laboratory strain originating from Africa. In addition, the sex-differentiated genomic region was associated with a significant excess of male-to-female heterozygosity and contained a small cluster of loci consistent with Y-specific null alleles. We demonstrate that genetic differentiation between sex chromosomes is sufficient to assign individuals to their correct sex with high accuracy. We also show how data on allele frequency differences between sexes can be used to estimate linkage disequilibrium between loci and the sex-determining locus. Our discovery of large-scale genetic differentiation between sex chromosomes in Ae. aegypti lays a new foundation for mapping and population genomic studies, as well as for mosquito control strategies targeting the sex-determination pathway.

Evolutionary Biology↗

bioRxiv2016

High virulence does not necessarily impede viral adaptation to a new host: A case study using a plant RNA virus

BackgroundWhen between-host selection pressures predominate, theory suggests that high virulence could hinder between-host transmission of microparasites, and that virulence therefore will evolve to lower levels that optimize between-host transmission. Highly virulent microparasites could also curtail host development, thereby limiting both the host resources available to them and their own within-host effective population size. High virulence might therefore curtail the mutation supply rate and increase the strength with which genetic drift acts on microparasite populations, thereby limiting the potential to adapt to the host and ultimately perhaps the ability to evolve lower virulence. As a first exploration of this hypothesis, we evolved Tobacco etch virus carrying an eGFP fluorescent marker in two semi-permissive host species, Nicotiana benthamiana and Datura stramonium, for which it has a large difference in virulence. We compared the results to those previously obtained in the typical host, Nicotiana tabacum, where we have shown that carriage of eGFP has a high fitness cost and its loss serves as a real-time indicator of adaptation.\n\nResultsAfter over half a year of evolution, we sequenced the genomes of the evolved lineages and measured their fitness. During the evolution experiment, marker loss leading to viable virus variants was only observed in one lineage of the host for which the virus has low virulence, D. stramonium. This result was consistent with the observation that there was a fitness cost of eGFP in this host, while surprisingly no fitness cost was observed in the host for which the virus has high virulence, N. benthamiana. Furthermore, in both hosts we observed few lineages with increases in viral fitness, and host-specific convergent evolution at the genomic level was only found in N. benthamiana.\n\nConclusionsThe results of this study do not lend support to the hypothesis that high virulence impedes microparasites evolution. Rather, they exemplify that jumps between host species can be game changers for evolutionary dynamics. When considering the evolution of genome architecture, host species jumps might play a very important role, by allowing evolutionary intermediates to be competitive.

Evolutionary Biology↗

bioRxiv2016

Evolutionary genomics of peach and almond domestication

The domesticated almond [Prunus dulcis (L.) Batsch] and peach [P. persica (Mill.) D. A. Webb] originate on opposite sides of Asia and were independently domesticated approximately 5000 years ago. While interfertile, they possess alternate mating systems and differ in a number of morpholog-ical and physiological traits. Here we evaluated patterns of genome-wide diversity in both almond and peach to better understand the impacts of mating system, adaptation, and domestication on the evolution of these taxa. Almond has [~]7X the genetic diversity of peach, and high genome-wide FST values support their status as separate species. We estimated a divergence time of approximately 8 Mya, coinciding with an active period of uplift in the northeast Tibetan Plateau and subsequent Asian climate change. We see no evidence of bottleneck during domestication of either species, but identify a number of regions showing signatures of selection during domestication and a significant overlap in candidate regions between peach and almond. While we expected gene expression in fruit to overlap with candidate selected regions, instead we find enrichment for loci highly differentiated between the species, consistent with recent fossil evidence suggesting fruit divergence long preceded domestication. Taken together this study tells us how closely related tree species evolve and are domesticated, the impact of these events on their genomes, and the utility of genomic information for long-lived species. Further exploration of this data will contribute to the genetic knowledge of these species and provide information regarding targets of selection for breeding application and further the understanding of evolution in these species.

Evolutionary Biology↗

bioRxiv2016

The fitness effects of spontaneous mutations nearly unseen by selection in a bacterium with multiple chromosomes

Mutation accumulation (MA) experiments employ the strategy of minimizing the population size of evolving lineages to greatly reduce effects of selection on newly arising mutations. Thus, most mutations fix within MA lines independently of their fitness effects. This approach, more recently combined with genome sequencing, has detailed the rates, spectra, and biases of different mutational processes. However, a quantitative understanding of the fitness effects of mutations virtually unseen by selection has remained an untapped opportunity. Here, we analyzed the fitness of 43 sequenced MA lines of the multi-chromosome bacterium Burkholderia cenocepacia that had each undergone 5554 generations of MA and accumulated an average of 6.73 spontaneous mutations. Most lineages exhibited either neutral or deleterious fitness in three different environments in comparison with their common ancestor. The only mutational class that was significantly overrepresented in lineages with reduced fitness was the loss of the plasmid, though nonsense mutations, missense mutations, and coding insertion-deletion mutations were also overrepresented in MA lineages whose fitness had significantly declined. Although the overall distribution of fitness effects was similar between the three environments, the magnitude and even the sign of the fitness of a number of lineages changed with the environment, demonstrating that the fitness of some genotypes was environmentally dependent. These results present an unprecedented picture of the fitness effects of spontaneous mutations in a bacterium with multiple chromosomes and provide greater quantitative support of the theory that the vast majority of spontaneous mutations are neutral or deleterious.

Evolutionary Biology↗