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bioRxiv2015

Ancestral chromatin configuration constrains chromatin evolution on differentiating sex chromosomes in Drosophila

Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. In Drosophila, the dosage-compensated X becomes enriched for hyperactive chromatin in males (mediated by H4K16ac), while the Y chromosome acquires silencing heterochromatin (enriched for H3K9me2/3). Drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatin-like milieu (enriched for H3K9me2/3) that permits the normal expression of dot-linked genes, but which is different from typical pericentric heterochromatin. In Drosophila busckii, the dot chromosomes have fused to the ancestral sex chromosomes, creating a pair of neo-sex chromosomes. Here we collect genomic, transcriptomic and epigenomic data from D. busckii, to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional. Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes. Despite rampant neo-Y degeneration, we find that the neo-X is deficient for the canonical histone modification mark of dosage compensation (H4K16ac), relative to autosomes or the compensated ancestral X chromosome, possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X. Our data show that Y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes, and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration.\n\nAuthor SummaryDNA is packaged with proteins into two general types of chromatin: the transcriptionally active euchromatin and repressive heterochromatin. Sex chromosomes typically evolve from a pair of euchromatic autosomes. The Y chromosome of Drosophila is gene poor and almost entirely heterochromatic; the X chromosome, in contrast, has evolved a hyperactive euchromatin structure and globally up-regulates its gene expression, to compensate for loss of activity from the homologous genes on the Y chromosome. The evolutionary trajectory along which sex chromosomes evolve such opposite types of chromatin configurations remains unclear, as most sex chromosomes are ancient and no longer contain signatures of their transitions. Here we investigate a pair of unusual young sex chromosomes (termed neo-Y and neo-X chromosomes) in D. busckii, which formed through fusions of a largely heterochromatic autosome (the dot chromosome) to the ancestral sex chromosomes. We show that nearly 60% of the neo-Y genes have already become non-functional within only 1 million years of evolution. Gene expression is lower on the neo-Y than on the neo-X, which is associated with a higher level of binding of a silencing heterochromatin mark. The neo-X, on the other hand, shows no evidence of evolving hyperactive chromatin for dosage compensation. Our results show that the Y chromosome can degenerate quickly, but the tempo and mode of chromatin evolution on the sex chromosomes may be constrained by the ancestral chromatin configuration.

Evolutionary Biology↗

bioRxiv2015

Endorsing Darwin – Global biogeography of the epipelagic goose barnacles Lepas spp. (Cirripedia, Lepadomorpha) proves cryptic speciation

AimWe studied different species of gooseneck barnacles from the globally distributed rafting genus Lepas to examine whether the most widespread species are true cosmopolitans and to explore the factors influencing the phylogeny and biogeography of these epipelagic rafters.\n\nLocationTemperate and tropical parts of the Atlantic, Pacific, and Indic oceans.\n\nMethodsWe used a phylogenetic approach based on mitochondrial 16S and coI sequences, and the nuclear 18S gene to elucidate patterns of inter- and intra-species divergence. Altogether, five species of Lepas from 18 confined regions of the Atlantic, Pacific and Indic oceans were analyzed.\n\nResultsA combination of nuclear and mitochondrial sequences provided robust phylogenetic signals for biogeographic classification of subgroups in Lepas species. Lepas australis, restricted to cold-temperate waters of the southern hemisphere shows two separate populations in the southern hemisphere (coastal Chile, other circum-Antarctic sampling sites) most probably related to temperature differences in the southern Pacific current systems. A more complex differentiation is seen for the cosmopolitan L. anatifera that thrives in warmer waters. In total, it is differentiated in four regional subgroups (coastal Chile, Oregon, Indopacific in general, Atlantic) and a global group, which might be either an ancient stemgroup, but more probably is an anthropogenic artefact. Separation into subgroups likely reflect geological vicariance effects. For Lepas, these were closure of the Isthmus of Panama, installation of the cool Benguela Current in the later Miocene including its persistence into the Present, Pleistocene current systems in the western Pacific differing from today, and in general lowered Pleistocene temperatures, and finally present-day current systems. The extreme ecological generalists L. anserifera and L. pectinata are not differentated according to available data and might represent true global species. Data for L. testudinata remain ambiguous.\n\nMain conclusionsOur data indicate cryptic speciation in some but not all species of the cosmopolitan epipelagic genus Lepas. Regional distribution of genetically different populations rely on a wealth of in part interacting inherited geological factors and modern traits. Controlling factors differ between species according to their ecospace limits and demonstrate the need for studies on species level to avoid unjustified generalizations. Data indicate that allopatric speciation is the main mode of divergence. True global species, if existent at all, need to be extreme ecological generalists, like Lepas pectinata and L. anserifera.

Evolutionary Biology↗

bioRxiv2015

A new idea on the evolution of biodiversity

The understanding of the mechanisms that allow the origin of species has shed light on many processes such as speciation, adaptation and extinction, but how to explain the existence of such a huge diversity of species on Earth still remains a mystery. Many theories and evidence have corroborated the processes that allow species to evolve or become extinct. Currently there are different hypotheses but no clear demonstrations of the factors that maintain the species diversity of ecosystems. Those based on competitive principles have been criticized from both theoretical and empirical approaches. Only by studying biodiversity in the context of evolution, natural history and ecology (taking into consideration the avoidance of competition and dispersal abilities, the phenotypic plasticity, the heterogeneous landscape, the facilitation and the endogenosymbiosis) we can understand values and gaps of past theories trying to provide a broader understanding of life on Earth towards a Unified Theory of Biodiversity.

Evolutionary Biology↗

bioRxiv2015

Origins of major archaeal clades do not correspond to gene acquisitions from bacteria

In a recent articxle, Nelson-Sathi et al. [NS] report that the origins of Major Archaeal Lineages [MAL] correspond to massive group-specific gene acquisitions via horizontal gene transfer (HGT) from bacteria (Nelson-Sathi et al., 2015, Nature 517(7532):77-80). If correct, this would have fundamental implications for the process of diversification in microbes. However, a re-examination of these data and results shows that the methodology used by NS systematically inflates the number of genes acquired at the root of each MAL, and incorrectly assumes bacterial origins for these genes. A re-analysis of their data with appropriate phylogenetic models accounting for the dynamics of gene gain and loss between lineages supports the continuous acquisition of genes over long periods in the evolution of Archaea.

Evolutionary Biology↗

bioRxiv2015

General formulation of Luria-Delbrück distribution of the number of mutants

The Luria-Delbruck experiment is a cornerstone of evolutionary theory, demonstrating the randomness of mutations before selection. The distribution of the number of mutants in this experiment has been the subject of intense investigation during the last 70 years. Despite this considerable effort, most of the results have been obtained under the assumption of constant growth rate, which is far from the experimental condition. We derive here the properties of this distribution for arbitrary growth function, for both the deterministic and stochastic growth of the mutants. The derivation we propose is surprisingly simple and versatile, allowing many generalizations to be taken easily into account.

Evolutionary Biology↗

bioRxiv2015

Stable eusociality via maternal manipulation when resistance is costless

In many eusocial species, queens use pheromones to influence offspring to express worker phenotypes. While evidence suggests that queen pheromones are honest signals of the queens reproductive health, here I show that queens honest signaling can result from ancestral maternal manipulation. I develop a mathematical model to study the coevolution of maternal manipulation, offspring resistance to manipulation, and maternal resource allocation. I assume that (1) maternal manipulation causes offspring to be workers against offsprings interests; (2) offspring can resist at no direct cost, as is thought to be the case with pheromonal manipulation; and (3) the mother chooses how much resource to allocate to fertility and maternal care. In the coevolution of these traits, I find that maternal care decreases, thereby increasing the benefit that offspring obtain from help, which in the long run eliminates selection for resistance. Consequently, ancestral maternal manipulation yields stable eusociality despite costless resistance. Additionally, ancestral manipulation in the long run becomes honest signaling that induces offspring to help. These results indicate that both eusociality and its commonly associated queen honest signaling can be likely to originate from ancestral manipulation.

Evolutionary Biology↗

bioRxiv2015

A Bayesian Approach for Detecting Mass-Extinction Events When Rates of Lineage Diversification Vary

The paleontological record chronicles numerous episodes of mass extinction that severely culled the Tree of Life. Biologists have long sought to assess the extent to which these events may have impacted particular groups. We present a novel method for detecting mass-extinction events from phylogenies estimated from molecular sequence data. We develop our approach in a Bayesian statistical framework, which enables us to harness prior information on the frequency and magnitude of mass-extinction events. The approach is based on an episodic stochastic-branching process model in which rates of speciation and extinction are constant between rate-shift events. We model three types of events: (1) instantaneous tree-wide shifts in speciation rate; (2) instantaneous tree-wide shifts in extinction rate, and; (3) instantaneous tree-wide mass-extinction events. Each of the events is described by a separate compound Poisson process (CPP) model, where the waiting times between each event are exponentially distributed with event-specific rate parameters. The magnitude of each event is drawn from an event-type specific prior distribution. Parameters of the model are then estimated using a reversible-jump Markov chain Monte Carlo (rjMCMC) algorithm. We demonstrate via simulation that this method has substantial power to detect the number of mass-extinction events, provides unbiased estimates of the timing of mass-extinction events, while exhibiting an appropriate (i.e., below 5%) false discovery rate even in the case of background diversification rate variation. Finally, we provide an empirical application of this approach to conifers, which reveals that this group has experienced two major episodes of mass extinction. This new approach--the CPP on Mass Extinction Times (CoMET) model--provides an effective tool for identifying mass-extinction events from molecular phylogenies, even when the history of those groups includes more prosaic temporal variation in diversification rate.

Evolutionary Biology↗

bioRxiv2015

Sequence capture of ultraconserved elements from bird museum specimens

New DNA sequencing technologies are allowing researchers to explore the genomes of the millions of natural history specimens collected prior to the molecular era. Yet, we know little about how well specific next-generation sequencing (NGS) techniques work with the degraded DNA typically extracted from museum specimens. Here, we use one type of NGS approach, sequence capture of ultraconserved elements (UCEs), to collect data from bird museum specimens as old as 120 years. We targeted approximately 5,000 UCE loci in 27 Western Scrub-Jays (Aphelocoma californica) representing three evolutionary lineages, and we collected an average of 3,749 UCE loci containing 4,460 single nucleotide polymorphisms (SNPs). Despite older specimens producing fewer and shorter loci in general, we collected thousands of markers from even the oldest specimens. More sequencing reads per individual helped to boost the number of UCE loci we recovered from older specimens, but more sequencing was not as successful at increasing the length of loci. We detected contamination in some samples and determined contamination was more prevalent in older samples that were subject to less sequencing. For the phylogeny generated from concatenated UCE loci, contamination led to incorrect placement of some individuals. In contrast, a species tree constructed from SNPs called within UCE loci correctly placed individuals into three monophyletic groups, perhaps because of the stricter analytical procedures we used for SNP calling. This study and other recent studies on the genomics of museums specimens have profound implications for natural history collections, where millions of older specimens should now be considered genomic resources.

Evolutionary Biology↗

bioRxiv2015

Phylodynamics of H5N1 Highly Pathogenic Avian Influenza in Europe, 2005–2010: Potential for Molecular Surveillance of New Outbreaks

Previous Bayesian phylogeographic studies of H5N1 highly pathogenic avian influenza viruses (HPAIVs) explored the origin and spread of the epidemic from China into Russia, indicating that HPAIV circulated in Russia prior to its detection there in 2005. In this study, we extend this research to explore the evolution and spread of HPAIV within Europe during the 2005-2010 epidemic, using all available sequences of the HA and NA gene regions that were collected in Europe and Russia during the outbreak. We use discrete-trait phylodynamic models within a Bayesian statistical framework to explore the evolution of HPAIV. Our results indicate that the genetic diversity and effective population size of HPAIV peaked between mid-2005 and early 2006, followed by drastic decline in 2007, which coincides with the end of the epidemic in Europe. Our results also suggest that domestic birds were the most likely source of the spread of the virus from Russia into Europe. Additionally, estimates of viral dispersal routes indicate that Russia, Romania, and Germany were key epicenters of these outbreaks. Our study quantifies the dynamics of a major European HPAIV pandemic and substantiates the ability of phylodynamic models to improve molecular surveillance of novel AIVs.

Evolutionary Biology↗

bioRxiv2015

Evolution of ecological dominance of yeast species in high-sugar environments

In budding yeasts, fermentation in the presence of oxygen evolved around the time of a whole genome duplication (WGD) and is thought to confer dominance in high-sugar environments because ethanol is toxic to many species. While there are many fermentative yeast species, only Saccharomyces cerevisiae consistently dominates wine fermentations. In this study, we use co-culture experiments and intrinsic growth rate assays to examine the relative fitness of non-WGD and WGD yeast species across environments to assess when S. cerevisiaes ability to dominate high-sugar environments arose. We show that S. cerevisiae dominates nearly all other non-WGD and WGD species except for its sibling species S. paradoxus in both grape juice and a high-sugar rich medium. Of the species we tested, S. cerevisiae and S. paradoxus have evolved the highest ethanol tolerance and intrinsic growth rate in grape juice. However, the ability of S. cerevisiae and S. paradoxus to dominate certain species depends on the temperature and the type of high-sugar environment. Our results indicate that dominance of high-sugar environments evolved much more recently than the WGD, most likely just prior to or during the differentiation of Saccharomyces species, and that evolution of multiple traits contributes to S. cerevisiaes ability to dominate wine fermentations.

Evolutionary Biology↗

bioRxiv2015

Bayesian co-estimation of selfing rate and locus-specific mutation rates for a partially selfing population

We present a Bayesian method for characterizing the mating system of populations reproducing through a mixture of self-fertilization and random outcrossing. Our method uses patterns of genetic variation across the genome as a basis for inference about pure hermaphroditism, androdioecy, and gynodioecy. We extend the standard coalescence model to accommodate these mating systems, accounting explicitly for multilocus identity disequilibrium, inbreeding depression, and variation in fertility among mating types. We incorporate the Ewens Sampling Formula (ESF) under the infinite-alleles model of mutation to obtain a novel expression for the likelihood of mating system parameters. Our Markov chain Monte Carlo (MCMC) algorithm assigns locus-specific mutation rates, drawn from a common mutation rate distribution that is itself estimated from the data using a Dirichlet Process Prior model. Among the parameters jointly inferred are the population-wide rate of self-fertilization, locus-specific mutation rates, and the number of generations since the most recent outcrossing event for each sampled individual.

Evolutionary Biology↗

bioRxiv2015

The Nature, Extent, and Consequences of Genetic Variation in the opa Repeats of Notch in Drosophila

Polyglutamine (pQ) tracts are abundant in many proteins co-interacting on DNA. The lengths of these pQ tracts can modulate their interaction strengths. However, pQ tracts > 40 residues are pathologically prone to amyloidogenic self-assembly. Here, we assess the extent and consequences of variation in the pQ-encoding opa repeats of Notch (N) in Drosophila melanogaster. We use Sanger sequencing to genotype opa sequences (50-CAX repeats), which have resisted assembly using short sequence reads. While the majority of N sequences pertain to reference opa31 (Q13HQ17) and opa32 (Q13HQ18) allelic classes, several rare alleles encode tracts > 32 residues: opa33a (Q14HQ18), opa33b (Q15HQ17), opa34 (Q16HQ17), opa35a1/opa35a2 (Q13HQ21), opa36 (Q13HQ22), and opa37 (Q13HQ23). Only one rare allele encodes a tract < 31 residues: opa23 (Q13-Q10). This opa23 allele shortens the pQ tract while simultaneously eliminating the interrupting histidine. Homozygotes for the short and long opa alleles have defects in sensory bristle organ specification, abdominal patterning, and embryonic survival. Inbred stocks with wild-type opa31 alleles become more viable when outbred, while an inbred stock with the longer opa35 becomes less viable after outcrossing to different backgrounds. In contrast, an inbred stock with the short opa23 allele is semi-viable in both inbred and outbred genetic backgrounds. This opa23 Notch allele also produces notched wings when recombined out of the X chromosome. Importantly, wa-linked X balancers carry the N allele opa33b and suppress AS-C insufficiency caused by the sc8 inversion. Our results demonstrate potent pQ variation and epistatic sensitivity for the N locus, and the need for long read genotyping of key repeat variables underlying gene regulatory networks.

Evolutionary Biology↗

bioRxiv2015

MERS-CoV recombination: implications about the reservoir and potential for adaptation

Recombination is a process that unlinks neighbouring loci allowing for independent evolutionary trajectories within genomes of many organisms. If not properly accounted for, recombination can compromise many evolutionary analyses. In addition, when dealing with organisms that are not obligately sexually reproducing, recombination gives insight into the rate at which distinct genetic lineages come into contact. Since June, 2012, Middle East respiratory syndrome coronavirus (MERS-CoV) has caused 1106 laboratory-confirmed infections, with 421 MERS-CoV associated deaths as of April 16, 2015. Although bats are considered as the likely ultimate source of zoonotic betacoronaviruses, dromedary camels have been consistently implicated as the source of current human infections in the Middle East. In this paper we use phylogenetic methods and simulations to show that MERS-CoV genome has likely undergone numerous recombinations recently. Recombination in MERS-CoV implies frequent co-infection with distinct lineages of MERS-CoV, probably in camels given the current understanding of MERS-CoV epidemiology.

Evolutionary Biology↗

bioRxiv2015

Evolution and coexistence in response to a key innovation in a long-term evolution experiment with Escherichia coli

Evolution of a novel function can greatly alter the effects of an organism on its environment. These environmental changes can, in turn, affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following evolution of a novel function in the long-term evolution experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to consume citrate aerobically. However, that ability evolved in one of the LTEE populations. In this population, citrate-utilizing bacteria (Cit+) coexisted stably with another clade of bacteria that lacked the capacity to utilize citrate (Cit-). This coexistence was shaped by the evolution of a cross-feeding relationship in which Cit+ cells released the dicarboxylic acids succinate, fumarate, and malate into the medium, and Cit- cells evolved improved growth on these carbon sources, as did the Cit+ cells. Thus, the evolution of citrate consumption led to a flask-based ecosystem that went from a single limiting resource, glucose, to one with five resources either shared or partitioned between two coexisting clades. Our findings show how evolutionary novelties can change environmental conditions, thereby facilitating diversity and altering both the structure of an ecosystem and the evolutionary trajectories of coexisting organisms.\n\nEvolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one.\n\n-Francois Jacob

Evolutionary Biology↗

bioRxiv2015

Environmental fluctuations do not select for increased variation or population-based resistance in Escherichia coli

Little is known about the mechanisms that enable organisms to cope with unpredictable environments. To address this issue, we used replicate populations of Escherichia coli selected under complex, randomly changing environments. Under four novel stresses that had no known correlation with the selection environments, individual cells of the selected populations had significantly lower lag and greater yield compared to the controls. More importantly, there were no outliers in terms of growth, thus ruling out the evolution of population-based resistance. We also assayed the standing phenotypic variation of the selected populations, in terms of their growth on 94 different substrates. Contrary to expectations, there was no increase in the standing variation of the selected populations, nor was there any significant divergence from the ancestors. This suggested that the greater fitness in novel environments is brought about by selection at the level of the individuals, which restricts the suite of traits that can potentially evolve through this mechanism. Given that day-to-day climatic variability of the world is rising, these results have potential public health implications. Our results also underline the need for a very different kind of theoretical approach to study the effects of fluctuating environments.

Evolutionary Biology↗

bioRxiv2015

Machine Learning Biogeographic Processes from Biotic Patterns: A New Trait-Dependent Dispersal and Diversification Model with Model-Choice By Simulation-Trained Discriminant Analysis

Current statistical biogeographical analysis methods are limited in the ways ecology can be related to the processes of diversification and geographical range evolution, requiring conflation of geography and ecology, and/or assuming ecologies that are uniform across all lineages and invariant in time. This precludes the possibility of studying a broad class of macro-evolutionary biogeographical theories that relate geographical and species histories through iineage-specific ecological and evolutionary dynamics, such as taxon cycle theory. Here we present a new model that generates phylogenies under a complex of superpositioned geographical range evolution, trait evolution, and diversification processes that can communicate with each other. This means that, under our model, the diversification and transition of the states of a lineage through geographical space is separate from, yet is conditional on, the state of the lineage in trait space (or vice versa). We present a likelihood-free method of inference under our model using discriminant analysis of principal components of summary statistics calculated on phylogenies, with the discriminant functions trained on data generated by simulations under our model. This approach of model classification is shown to be efficient, robust, and performant over a broad range of parameter space defined by the relative rates of dispersal, trait evolution, and diversification processes. We apply our method to a case study of the taxon cycle, i.e. testing for habitat and trophic-level constraints in the dispersal regimes of the Wallacean avifaunal radiation.

Evolutionary Biology↗

bioRxiv2015

Evolution of organismal stoichiometry in a 50,000-generation experiment with Escherichia coli

Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, little is known about rates and directions of evolutionary changes in elemental composition in response to nutrient limitation. We measured carbon, nitrogen, and phosphorus content of Escherichia coli evolved under controlled carbon-limited conditions for 50,000 generations. The bacteria evolved higher relative nitrogen and phosphorus content, consistent with selection for increased use of the more abundant elements. Total carbon assimilated also increased, indicating more efficient use of the limiting element. Altogether, our study shows that stoichiometry evolved over a relatively short time-period, and that it did so in a predictable direction given the carbon-limiting environment.

Evolutionary Biology↗

bioRxiv2015

Stochastic evolutionary games in dynamic populations

Frequency dependent selection and demographic fluctuations play important roles in evolutionary and ecological processes. Under frequency dependent selection, the average fitness of the population may increase or decrease based on interactions between individuals within the population. This should be reflected in fluctuations of the population size even in constant environ ments. Here, we propose a stochastic model, which naturally combines these two evolutionary ingredients by assuming frequency dependent competition between different types in an individual-based model. In contrast to previous game theoretic models, the carrying capacity of the population and thus the population size is determined by pairwise competition of individuals mediated by evolutionary games and demographic stochasticity. In the limit of infinite population size, the averaged stochastic dynamics is captured by the deterministic competitive LotkaVolterra equations. In small populations, demographic stochasticity may instead lead to the extinction of the entire population. As the population size is driven by the fitness in evolutionary games, a population of cooperators is less prone to go extinct than a population of defectors, whereas in the usual systems of fixed size, the population would thrive regardless of its average payoff.

Evolutionary Biology↗