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bioRxiv2016

Quantitative, model-based estimates of variability in the serial interval of Plasmodium falciparum malaria

Background: The serial interval is a fundamentally important quantity in infectious disease epidemiology that has numerous applications to inferring patterns of transmission from case data. Many of these applications are apropos to efforts to eliminate Plasmodium falciparum (Pf) malaria from locations throughout the world, yet the serial interval for this disease is poorly understood quantitatively.\n\nResults: To obtain a quantitative estimate of the serial interval for Pf malaria, we took the sum of components of the Pf malaria transmission cycle based on a combination of mathematical models and empirical data. During this process, we identified a number of factors that account for substantial variability in the serial interval across different contexts. Treatment with antimalarial drugs roughly halves the serial interval, seasonality results in different serial intervals at different points in the transmission season, and variability in within-host dynamics results in many individuals whose serial intervals do not follow average behavior.\n\nConclusions: These results have important implications for epidemiological applications that rely on quantitative estimates of the serial interval of Pf malaria and other diseases characterized by prolonged infections and complex ecological drivers.

Epidemiology↗

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

Enhanced gene expression plasticity as a mechanism of adaptation to a variable environment in a reef-building coral

Local adaptation is ubiquitous1, but the molecular mechanisms giving rise to this ecological phenomenon remain largely unknown2. A year-long reciprocal transplant of mustard hill coral (Porites astreoides) between a highly environmentally variable inshore habitat and more stable offshore habitat3 demonstrated that both inshore and offshore populations exhibit elevated growth, protein and lipid content in their home reef environment, indicative of local adaptation 4 Here, we characterized the genomic basis of this adaptation in both coral hosts and their intracellular algal symbionts (Symbiodinium sp.) using genome-wide gene expression profiling5,6 and gene coexpression network analysis7. Inshore and offshore coral populations differ primarily in their capacity for gene expression pla ...

Genomics↗

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

DNA methylation adjusts the specificity of memories depending on the learning context and promotes relearning

The activity of the epigenetic writers DNA methyltransferases (Dnmts) after olfactory reward conditioning is important for both stimulus-specific long-term memory (LTM) formation and extinction. It, however, remains unknown which components of memory formation Dnmts regulate (e.g. associative vs. non-associative) and in what context (e.g. varying training conditions). Here we address these aspects in order to clarify the role of Dnmt-mediated DNA methylation in memory formation. We used a pharmacological Dnmt inhibitor and classical appetitive conditioning in the honeybee Apis mellifera, a well characterized model for classical conditioning. We quantified the effect of DNA methylation on naive odour and sugar responses, and on responses following olfactory reward conditioning. We show that (1) Dnmts do not influence naive odour or sugar responses, (2) Dnmts do not affect the learning of new stimuli, but (3) Dnmts influence odour-coding, i.e. 'correct' (stimulus-specific) LTM formation. Particularly, Dnmts reduce memory specificity when experience is low (one-trial training), and increase memory specificity when experience is high (multiple-trial training), generating an ecologically more useful response to learning. (4) In reversal learning conditions, Dnmts are involved in regulating both excitatory (re-acquisition) and inhibitory (forgetting) processes.

Neuroscience↗

bioRxiv2016

Modeling and experimental determination of infection bottleneck and within-host dynamics of a soil-borne bacterial plant pathogen.

In natura, many organisms face multiple infections by pathogens. The ability of a pathogen to reinfect an already-infected host affects the genetic makeup of the pathogen population at the end of the infectious cycle. Despite the likely prevalence of this situation, the population dynamics of pathogens during multiple infections over time is still poorly understood. Here we combined theoretical and empirical investigations of the founding population size, a critical driver of the evolution of pathogens, in a setting allowing for multiple and subsequent re-infections. Using the soil-borne bacterial pathogen Ralstonia solanacearum and tomato as its host, we first assessed the strength of the host infection bottleneck, and showed that both the host barrier and the immune system work additively to constrain the infection. Then, by increasing the temperature, we experimentally demonstrated that the increased pathogen proliferation within the host reduces the contribution of subsequent re-infection leading to a lower founding population size. Our study highlights the importance of within-host pathogen proliferation in determining founding population size - and thus bacterial genetic diversity during epidemics - for pathosystems where multiple re-infections occur. Under current global changes, our work notably predicts that an increased temperature provided this increase has a beneficial impact on pathogen growth, should decrease the founding population size and as a consequence potentially lower the diversity of the infecting and transmitted pathogen population.\n\nSignificance StatementFounder population size is a major determinant of pathogen evolution, yet we still have limited insights into effective populations in natural settings. Most studies have considered infection as a single event, followed by pathogen growth in the host. But, in natura, organisms typically face multiple infections by several co-exisiting pathogen strains. Therefore, effective population size will depend on the timing and relative growth rate of the different infecting strains. In this work, we predict and experimentally show that both priority effects and within-host competition determines effective founding size, with an over-contribution of fast-growing and early infecting genotypes. This work sheds a new light on the ecological and evolutionary pressures affecting infection dynamics in realistic conditions.

Plant Biology↗

bioRxiv2016

Editing of the urease gene by CRISPR-Cas in the diatom Thalassiosira pseudonana

Background: CRISPR-Cas is a recent and powerful edition to the molecular toolbox which allows programmable genome editing. It has been used to modify genes in a wide variety of organisms, but only two alga to date. Here we present a methodology to edit the genome of T. pseudonana, a model centric diatom with both ecological significance and high biotechnological potential, using CRISPR-Cas.\n\nResults: A single construct wa assembled using Golden Gate cloning. Two sgRNAs were used to introduce a precise 37nt deletion early in the coding region of the urease gene. A high percentage of bi-allelic mutations ([≤] 61.5%) were observed in clones with the CRISPR-Cas construct. Growth of bi-allelic mutants in urea led to a significant reduction in growth rate and cell size compared to growth in nitrate.\n\nConclusions: CRISPR-Cas can precisely and efficiently edit the genome of T. pseudonana. The use of Golden Gate cloning to assemble CRISPR-Cas constructs gives additional flexibility to the CRISPR-Cas method and facilitates modifications to target alternative genes or species.

Genomics↗

bioRxiv2016

Electrophysiology reveals the neural dynamics of naturalistic auditory language processing: event-related potentials reflect continuous model updates

The recent trend away from ANOVA-based analyses places experimental investigations into the neurobiology of cognition in more naturalistic and ecologically valid designs within reach. Using mixed-effects models for epoch-based regression, we demonstrate the feasibility of examining event-related potentials (ERPs), and in particular the N400, to study the neural dynamics of auditory language processing in a naturalistic setting. Despite the large variability between trials during naturalistic stimulation, we replicated previous findings from the literature: frequency, animacy, word order. This suggests a new perspective on ERPs, namely as a continuous modulation reflecting continuous model updates (cf. Friston, 2005) instead of a series of discrete and essentially sequential processes.

Animal Behavior and Cognition↗

bioRxiv2016

Awake Canine fMRI Predicts Dogs’ Preference for Praise Versus Food

Dogs are hypersocial with humans, and their integration into human social ecology makes dogs a unique model for studying cross-species social bonding. However, the proximal neural mechanisms driving dog-human social interaction are unknown. We used fMRI in 15 awake dogs to probe the neural basis for their preferences for social interaction and food reward. In a first experiment, we used the ventral caudate as a measure of intrinsic reward value and compared activation to conditioned stimuli that predicted food, praise, or nothing. Relative to the control stimulus, the caudate was significantly more active to the reward-predicting stimuli and showed roughly equal or greater activation to praise versus food in 13 of 15 dogs. To confirm that these differences were driven by the intrinsic value of social praise, we performed a second imaging experiment in which the praise was withheld on a subset of trials. The difference in caudate activation to the receipt of praise, relative to its withholding, was strongly correlated with the differential activation to the conditioned stimuli in the first experiment. In a third experiment, we performed an out-of-scanner choice task in which the dog repeatedly selected food or owner in a Y-maze. The relative caudate activation to food-and praise-predicting stimuli in Experiment 1 was a strong predictor of each dogs sequence of choices in the Y-maze. Analogous to similar neuroimaging studies of individual differences in human social reward, our findings demonstrate a neural mechanism for preference in domestic dogs that is stable within, but variable between, individuals. Moreover, the individual differences in the caudate responses indicate the potentially higher value of social than food reward for some dogs and may help to explain the apparent efficacy of social interaction in dog training.

Animal Behavior and Cognition↗

bioRxiv2016

Origins of pandemic clones from environmental gene pools

Some microbes can transition from an environmental lifestyle to a pathogenic one1-3. This ecological switch typically occurs through the acquisition of horizontally acquired virulence genes4,5. However, the genomic features that must be present in a population prior to the acquisition of virulence genes and emergence of pathogenic clones remain unknown. We hypothesized that virulence adaptive polymorphisms (VAPs) circulate in environmental populations and are required for this transition. We developed a comparative genomic framework for identifying VAPs, using Vibrio cholerae as a model. We then characterized several environmental VAP alleles to show that, while some of them reduced the ability of clinical strains to colonize a mammalian host, other alleles conferred efficient host colonization. These results show that VAPs are present in environmental bacterial populations prior to the emergence of virulent clones. We propose a scenario in which VAPs circulate in the environment, they become selected and enriched under certain ecologicalconditions, and finally a genomic background containing several VAPs acquires virulence factors that allows for its emergence as a pathogenic clone.

Microbiology↗

bioRxiv2016

Strategic adjustment of parental care: life-history trade-offs and the role of glucocorticoids

Life history theory predicts that optimal strategies of parental investment will depend on ecological and social factors such as current brood value and offspring need. Parental care strategies are also likely to be mediated in part by the hypothalamic-pituitary-adrenal (HPA) axis and glucocorticoid hormones. Here we present an experiment in tree swallows (Tachycineta bicolor), a biparental songbird with wide geographic distribution, asking whether parental care is strategically adjusted in response to signals of offspring need and brood value and whether glucocorticoids are involved in these adjustments. Using an automated playback system, we carried out playbacks of nestling begging calls specifically to females in two populations differing in their brood value: a northern population in Ontario, Canada (relatively high brood value) and a southern population in North Carolina, USA (lower brood value). We quantified female offspring provisioning rates before and during playbacks and plasma corticosterone levels (cort) once during late incubation and once immediately after playbacks. Females in both populations increased feeding rates temporarily during the first two hours of playback but the increase was not sustained for the entire duration of playback (six hours). Cort levels from samples at the end of the playback did not differ between control females and females that received playbacks. However, females that had higher increases in cort between the incubation and nestling period had greater fledging success. These results suggest that females are able to strategically respond to offspring need, although the role of glucocorticoids in this strategic adjustment remains unclear.

Animal Behavior and Cognition↗

bioRxiv2016

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

Admixture--the mixing of genomes from divergent populations--is increasingly appreciated as a central process in evolution. To characterize and quantify patterns of admixture across the genome, a number of methods have been developed for local ancestry inference. However, existing approaches have a number of shortcomings. First, all local ancestry inference methods require some prior assumption about the expected ancestry tract lengths. Second, existing methods generally require genotypes, which is not feasible to obtain for many next-generation sequencing projects. Third, many methods assume samples are diploid, however a wide variety of sequencing applications will fail to meet this assumption. To address these issues, we introduce a novel hidden Markov model for estimating local ancestry that models the read pileup data, rather than genotypes, is generalized to arbitrary ploidy, and can estimate the time since admixture during local ancestry inference. We demonstrate that our method can simultaneously estimate the time since admixture and local ancestry with good accuracy, and that it performs well on samples of high ploidy--i.e. 100 or more chromosomes. As this method is very general, we expect it will be useful for local ancestry inference in a wider variety of populations than what previously has been possible. We then applied our method to pooled sequencing data derived from populations of Drosophila melanogaster on an ancestry cline on the east coast of North America. We find that regions of local recombination rates are negatively correlated with the proportion of African ancestry, suggesting that selection against foreign ancestry is the least efficient in low recombination regions. Finally we show that clinal outlier loci are enriched for genes associated with gene regulatory functions, consistent with a role of regulatory evolution in ecological adaptation of admixed D. melanogaster populations. Our results illustrate the potential of local ancestry inference for elucidating fundamental evolutionary processes.\n\nAuthor SummaryWhen divergent populations hybridize, their offspring obtain portions of their genomes from each parent population. Although the average ancestry proportion in each descendant is equal to the proportion of ancestors from each of the ancestral populations, the contribution of each ancestry type is variable across the genome. Estimating local ancestry within admixed individuals is a fundamental goal for evolutionary genetics, and here we develop a method for doing this that circumvents many of the problems associated with existing methods. Briefly, our method can use short read data, rather than genotypes and can be applied to samples with any number of chromosomes. Furthermore, our method simultaneously estimates local ancestry and the number of generations since admixture--the time that the two ancestral populations first encountered each other. Finally, in applying our method to data from an admixture zone between ancestral populations of Drosophila melanogaster, we find many lines of evidence consistent with natural selection operating to against the introduction of foreign ancestry into populations of one predominant ancestry type. Because of the generality of this method, we expect that it will be useful for a wide variety of existing and ongoing research projects.

Evolutionary Biology↗

bioRxiv2016

Towards robust evolutionary inference with integral projection models

Integral projection models (IPMs) are extremely flexible tools for ecological and evolutionary inference. IPMs track the distribution of phenotype in populations through time, using functions describing phenotype-dependent development, inheritance, survival and fecundity. For evolutionary inference, two important features of any model are the ability to (i) characterize relationships among traits (including values of the same traits across ages) within individuals, and (ii) characterize similarity between individuals and their descendants. In IPM analyses, the former depends on regressions of observed trait values at each age on values at the previous age (development functions), and the latter on regressions of offspring values at birth on parent values as adults (inheritance functions). We show analytically that development functions, characterized this way, will typically underestimate covariances of trait values across ages, due to compounding of regression to the mean across projection steps. Similarly, we show that inheritance, characterized this way, is inconsistent with a modern understanding of inheritance, and underestimates the degree to which relatives are phenotypically similar. Additionally, we show that the use of a constant biometric inheritance function, particularly with a constant intercept, is incompatible with evolution. Consequently, current implementations of IPMs will predict little or no phenotypic evolution, purely as artifacts of their construction. We present alternative approaches to constructing development and inheritance functions, based on a quantitative genetic approach, and show analytically and through an empirical example on a population of bighorn sheep how they can potentially recover patterns that are critical to evolutionary inference.

Evolutionary Biology↗

bioRxiv2016

Flexibility of co-evolutionary patterns in ectoparasite populations: genetic structure and diversity in Apodemus mice and their lice.

Host-parasite co-evolution belongs among the major processes governing evolution of biodiversity on the global scale. Numerous studies performed at inter-specific level revealed variety of patterns from strict co-speciation to lack of co-divergence and frequent host-switching, even in species tightly linked to their hosts. To explain these observations and formulate ecological hypotheses, we need to acquire better understanding to parasites population genetics and dynamics, and their main determinants. Here, we analyse the impact of co-evolutionary processes on genetic diversity and structure of parasite populations, using a model composed of the louse Polyplax serrata and its hosts, mice of the genus Apodemus, collected from several dozens of localities across Europe. We use mitochondrial DNA sequences and microsatellite data to describe the level of genealogical congruence between hosts and parasites and to assess genetic diversity of the populations. We also explore links between the genetic assignment of the parasite and its host affiliation, and test the prediction that populations of the parasite possessing narrower host specificity show deeper pattern of population structure and lower level of genetic diversity as a result of limited dispersal and smaller effective population size. We demonstrate an overall complexity of the co-evolutionary processes and their variability even among closely related lineages of the parasites. In the analysis of several sympatric parasite populations, we find strong evidence for the link between the width of host specificity and genetic diversity of parasites.

Evolutionary Biology↗

bioRxiv2016

High Phylogenetic Utility of an Ultraconserved Element Probe Set Designed for Arachnida

Arachnida is an ancient, diverse, and ecologically important animal group that contains a number of species of interest for medical, agricultural, and engineering applications. Despite this applied importance, many aspects of the arachnid tree of life remain unresolved, hindering comparative approaches to arachnid biology. Biologists have made considerable efforts to resolve the arachnid phylogeny; yet, limited and challenging morphological characters, as well as a dearth of genetic resources, have confounded these attempts. Here, we present a genomic toolkit for arachnids featuring hundreds of conserved DNA regions (ultraconserved elements or UCEs) that allow targeted sequencing of any species in the arachnid tree of life. We used recently developed capture probes designed from conserved genomic regions of available arachnid genomes to enrich a sample of loci from 32 diverse arachnids. Sequence capture returned an average of 487 UCE loci for all species, with a range from 170 to 722. Phylogenetic analysis of these UCEs produced a highly resolved arachnid tree with relationships largely consistent with recent transcriptome-based phylogenies. We also tested the phylogenetic informativeness of UCE probes within the spider, scorpion, and harvestman orders, demonstrating the utility of these markers at shallower taxonomic scales, even down to the level of species differences. This probe set will open the door to phylogenomic and population genomic studies across the arachnid tree of life, enabling systematics, species delimitation, species discovery, and conservation of these diverse arthropods.

Genomics↗

bioRxiv2016

Rewired RNAi-Mediated Genome Surveillance in House Dust Mites

House dust mites are common pests with an unusual evolutionary history, being descendants of a parasitic ancestor. Transition to parasitism is frequently accompanied by genome rearrangements, possibly to accommodate the genetic change needed to access new ecology. Transposable element (TE) activity is a source of genomic instability that can trigger large-scale genomic alterations. Eukaryotes have multiple transposon control mechanisms, one of which is RNA interference (RNAi). Investigation of the dust mite genome failed to identify a major RNAi pathway: the Piwi-associated RNA (piRNA) pathway, which has been replaced by a novel small-interfering RNAs (siRNAs)-like pathway. Co-opting of piRNA function by dust mite siRNAs is extensive, including establishment of TE control master loci that produce siRNAs. Interestingly, other members of the Acari have piRNAs indicating loss of this mechanism in dust mites is a recent event. Flux of RNAi-mediated control of TEs provides a mechanism for unusual arc of dust mite evolution.

Genomics↗

bioRxiv2016

Origin and phylogenetic status of the local Ashanti Dwarf pig (ADP) of Ghana based 1 on evidence from mtDNA analysis, MC1R, and Y-chromosome haplotypes

The Ashanti Dwarf Pig (ADP) of Ghana is an endangered pig breed with hardy and disease resistant traits. Characterisation of animal genetic resources provides relevant data for their conservation and sustainable use for food security and economic development. We investigated the origin and phylogenetic status of the local ADP of Ghana and their crosses with modern commercial breeds based on mtDNA, MC1R and Y-chromosome sequence polymorphisms, as well as genome-wide SNP genotyping.\n\nThe study involved 164 local pigs sampled from the three agro-ecological zones of Ghana. Analyses of the mitochondrial D-loop region and Y-chromosome sequences revealed both European and Asian genetic signatures, with differences between the geographical zones. Black coat colour is the most predominant within the breed, with dominant black MC1R alleles of both Asian and European origin contributing. European alleles for spotting are present at a low frequency in the sample set, and may account for the occurrence of spotted piglets in some APD litters. PCA analysis of SNP data revealed a strong location and breed effect on clustering of local Ghanaian pigs. On a global level, Ghanaian local pigs cluster closely with European pigs of commercial origin, such as the Large White.\n\nThe presence of both European and Asian contributions, with differences between geographical zones probably reflects trading and colonial influences.. Understanding the effects of admixture on important adaptive and economic traits of the ADP and other local breeds in Africa is critical for developing sustainable conservation programmes to prevent the decline of these genetic resources.

Genomics↗