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bioRxiv2017

A hierarchical Bayesian approach to estimate endosymbiont infection rates

Endosymbionts may play an important role in the evolution of the Insecta. Bacteria such as Wolbachia, Cardinium, and Rickettsia are known to manipulate host reproduction to facilitate their own. Indeed, there are many documented cases where Wolbachia (Alphaproteobacteria: Rickettsiaceae) induces one of four manipulative phenotypes (cytoplasmic incompatibility, male killing, feminization, and parthenogenesis). The scale of infection among species has been a major subject of investigation, but quantification has been difficult because various approaches have yielded different estimates. One under-appreciated aspect of this problem arises when multiple--yet independent--samples are taken within a taxon. When independent samples within a taxon are treated as levels of a hierarchy, the problem is greatly simplified because data are partially pooled according to taxon. Here, we present a hierarchical Bayesian approach to estimate infection frequency where multiple independent samples were collected across several taxonomic levels. We apply this model to estimate the rates of infection for Wolbachia in the Lepidoptera, and then extend the model to account for phylogenetic non-independence. In addition, we highlight the current knowledge regarding Wolbachia and its effects within Lepidoptera. Our model estimates that the rate of endosymbiont infection for the Lepidoptera is approximately 12%. Given our limited knowledge regarding the phenotypes induced by these endosymbionts and the low infection rate, we urge caution when extrapolating the results of positive assays.

evolutionary biology↗

bioRxiv2017

Density-dependent selection in evolutionary genetics: a lottery model of Grime’s triangle

Selection is commonly described by assigning constant relative fitness values to genotypes. Yet population density is often regulated by crowding. Relative fitness may then depend on density, and selection can change density when it acts on a density-regulating trait. When strong density-dependent selection acts on a density-regulating trait, selection is no longer describable by density-independent relative fitnesses, even in demographically stable populations. These conditions are met in most previous models of density-dependent selection (e.g. \"K-selection\" in the logistic and Lotka-Volterra models), suggesting that density-independent relative fitnesses must be replaced with more ecologically explicit absolute fit-nesses unless selection is weak. Here we show that density-independent relative fitnesses can also accurately describe strong density-dependent selection under some conditions. We develop a novel model of density-regulated population growth with three ecologically intuitive traits: fecundity, mortality, and competitive ability. Our model, unlike the logistic or Lotka-Volterra, incorporates a density-dependent juvenile \"reproductive excess\", which largely decouples density-dependent selection from the regulation of density. We find that density-independent relative fitnesses accurately describe strong selection acting on any one trait, even fecundity, which is both density-regulating and subject to density-dependent selection. Pleiotropic interactions between these traits recovers the familiar K-selection behavior. In such cases, or when the population is maintained far from demographic equilibrium, our model offers a possible alternative to relative fitness.

evolutionary biology↗

bioRxiv2017

The role of gene expression in the recent evolution of resistance in a model host parasite system

Damage by parasites is a perpetual challenge for hosts, often leading to the evolution of elaborate mechanisms of avoidance, immunity, or tolerance. Host resistance can evolve via changes in immune protein coding and/or expression. Heritable population differences in gene expression following infection can reveal mechanisms of immune evolution. We compared gene expression in infected and uninfected threespine stickleback (Gasterosteus aculeatus) from two natural populations that differ in their resistance to a native cestode parasite, Schistocephalus solidus. Genes in both the innate and adaptive immune system were differentially expressed as a function of host population, infection status, and their interaction. These genes were enriched for loci controlling immune functions that we independently verified differ between host populations, or in response to infection. For instance, populations differ strongly in reactive oxygen (ROS) production, and we observed corresponding differences in expression of ROS-affecting loci. Differentially expressed genes also were involved in fibroblast activation, B-cell activation, and leukocyte trafficking. Coexpression network analysis identified two distinct immune processes contributing to stickleback resistance; several modules of genes are correlated with parasite survival while a different set of modules are correlated with suppression of cestode growth. Comparison of networks between populations showed resistant fish have a dynamic expression profile while susceptible fish are static. In summary, recent evolutionary divergence between two vertebrate populations has generated population-specific gene expression responses to parasite infection, which reveal a few immune modules likely to separately affect cestode establishment, and growth.

evolutionary biology↗

bioRxiv2017

The genomic basis of adaptation to the deep water ‘twilight zone’ in Lake Malawi cichlid fishes

Deep water environments are characterized by low levels of available light at increasingly narrow spectra, great hydrostatic pressure and reduced dissolved oxygen - conditions predicted to exert highly specific selection pressures. In Lake Malawi over 800 cichlid species have evolved, and this adaptive radiation extends into the \"twilight zone\" below 100 metres. We use population-level RAD-seq data to investigate whether four endemic deep water species (Diplotaxodon spp.) have experienced divergent selection within this environment. We identify candidate genes including regulators of photoreceptor function, photopigments, lens morphology and haemoglobin, many not previously implicated in cichlid adaptive radiations. Co-localization of functionally linked genes suggests co-adapted \"supergene\" complexes. Comparisons of Diplotaxodon to the broader Lake Malawi radiation using genome resequencing data revealed functional substitutions in candidate genes. Our data provide unique insights into genomic adaptation to life at depth, and suggest genome-level specialisation for deep water habitat as an important process in cichlid radiation.

evolutionary biology↗

bioRxiv2017

Resolution of conflict between parental genomes in a hybrid species

The development of reproductive barriers against parent species is crucial during hybrid speciation, and post-zygotic isolation can be important in this process. Genetic incompatibilities that normally isolate the parent species can become sorted in hybrids to form reproductive barriers towards either parent. However, the extent to which this sorting process is systematically biased and therefore predictable in which loci are involved and which alleles are favored is largely unknown. Theoretically, reduced fitness in hybrids due to the mixing of differentiated genomes can be resolved through rapid evolution towards allelic combinations ancestral to lineage-splitting of the parent species, as these alleles have successfully coexisted in the past. However, for each locus, this effect may be influenced by its chromosomal location, function, and interactions with other loci. We use the Italian sparrow, a homoploid hybrid species that has developed post-zygotic barriers against its parent species, to investigate this prediction. We show significant bias towards fixation of the ancestral allele among 57 nuclear intragenic SNPs, particularly those with a mitochondrial function whose ancestral allele came from the same parent species as the mitochondria. Consistent with increased pleiotropy leading to stronger fitness effects, genes with more protein-protein interactions were more biased in favor of the ancestral allele. Furthermore, the number of protein-protein interactions was especially low among candidate incompatibilities still segregating within Italian sparrows, suggesting that low pleiotropy allows steep intraspecific clines in allele frequencies to form. Finally, we report evidence for pervasive epistatic interactions within one Italian sparrow population, particularly involving loci isolating the two parent species but not hybrid and parent. However there was a lack of classic incompatibilities and no admixture linkage disequilibrium. This suggests that parental genome admixture can continue to constrain evolution and prevent genome stabilization long after incompatibilities have been purged.

evolutionary biology↗

bioRxiv2017

Inferring the Joint Demographic History of Multiple Populations: Beyond the Diffusion Approximation

Understanding variation in allele frequencies across populations is a central goal of population genetics. Classical models for the distribution of allele frequencies, using forward simulation, coalescent theory, or the diffusion approximation, have been applied extensively for demographic inference, medical study design, and evolutionary studies. Here we propose a tractable model of ordinary differential equations for the evolution of allele frequencies that is closely related to the diffusion approximation but avoids many of its limitations and approximations. We show that the approach is typically faster, more numerically stable, and more easily generalizable than the state-of-the-art software implementation of the diffusion approximation. We present a number of applications to human sequence data, including demographic inference with a five-population joint frequency spectrum and a discussion of the transferability of demographic histories across populations.

evolutionary biology↗

bioRxiv2017

Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices

Adaptation to human-induced environmental change has the potential to profoundly influence the genomic architecture of affected species. This is particularly true in agricultural ecosystems, where anthropogenic selection pressure is strong. Heliothis virescens feeds on cotton in its larval stages and US populations have been declining since the widespread planting of transgenic cotton, which endogenously express proteins derived Bacillus thuringiensis (Bt). No physiological adaptation to Bt toxin has been found in the field, so adaptation to this altered environment could involve: 1) shifts in host plant selection mechanisms to avoid cotton, 2) changes in detoxification mechanisms required for cotton-feeding versus feeding on other host plants, or 3) loss of resistance to previously used management practices including insecticides. Here we begin to address the question of whether such changes occurred in H. virescens populations between the years 1997 and 2012. As part of our study, we produced an H. virescens genome assembly and used this in concert with a ddRAD-seq enabled genome scan to identify loci with significant allele frequency changes over the 15 year period after Bt crops became widespread in the agricultural landscape. Confirmation that a known genetic change at a previously described H. virescens target of selection was detectable in our genome scan increased our confidence in this methodology. We quantified the strength of selection required to elicit the observed allele frequency changes at loci under selection. Potential contributions of genes near the loci under selection to adaptive phenotypes in the H. virescens cotton system are discussed.

evolutionary biology↗

bioRxiv2017

The mitochondrial genomes of the acoelomorph wormsParatomella rubra and Isodiametra pulchra

Acoels are small, ubiquitous, but understudied, marine worms with a very simple body plan. Their internal phylogeny is still in parts unresolved, and the position of their proposed phylum Xenacoelomorpha (Xenoturbella+Acoela) is still debated.\n\nHere we describe mitochondrial genome sequences from two acoel species: Paratomella rubra and Isodiametra pulchra. The 14,954 nucleotide-long P. rubra sequence is typical for metazoans in size and gene content. The larger I. pulchra mitochondrial genome contains both ribosomal genes, 21 tRNAs, but only 11 protein-coding genes. We find evidence suggesting a duplicated sequence in the I. pulchra mitochondrial genome.\n\nMitochondrial sequences for both P. rubra and I. pulchra have a unique genome organisation in comparison to other published metazoan mitochondrial genomes. We found a large degree of protein-coding gene and tRNA overlap in P. rubra, with little non-coding sequence making the genome compact. Conversely, the I. pulchra mitochondrial genome has many long non-coding sequences between genes, likely driving the genome size expansion. Phylogenetic trees inferred from concatenated alignments of mitochondrial genes grouped the fast-evolving Acoela and Tunicata, almost certainly due to the systematic error of long branch attraction: a reconstruction artefact that is probably compounded by the fast substitution rate of mitochondrial genes in this taxon.

evolutionary biology↗

bioRxiv2017

Experimental evidence that thermal selection has shaped the latitudinal distribution of mitochondrial haplotypes in Australian fruit flies

Cellular metabolism is regulated by enzyme complexes within the mitochondrion, the function of which are sensitive to the prevailing temperature. Such thermal sensitivity, coupled with the observation that population frequencies of mitochondrial haplotypes tend to associate with latitude, altitude or climatic regions across species distributions, led to the hypothesis that thermal selection has played a role in shaping standing variation in the mitochondrial DNA (mtDNA) sequence. This hypothesis, however, remains controversial, and requires evidence that the distribution of haplotypes observed in nature corresponds with the capacity of these haplotypes to confer differences in thermal tolerance. Specifically, haplotypes predominating in tropical climates are predicted to encode increased tolerance to heat stress, but decreased tolerance to cold stress. We present direct evidence for these predictions, using mtDNA haplotypes sampled from the Australian distribution of Drosophila melanogaster. We show that the ability of flies to tolerate extreme thermal challenges is affected by sequence variation across mtDNA haplotypes, and that the thermal performance associated with each haplotype corresponds with its latitudinal prevalence. The haplotype that predominates at low (subtropical) latitudes confers greater resilience to heat stress, but lower resilience to cold stress, than haplotypes predominating at higher (temperate) latitudes. We explore molecular mechanisms that might underlie these responses, presenting evidence that the effects are in part regulated by SNPs that do not change the protein sequence. Our findings suggest that standing variation in the mitochondrial genome can be shaped by thermal selection, and could therefore contribute to evolutionary adaptation under climatic stress.

evolutionary biology↗

bioRxiv2017

High GC Content Causes De Novo Created Proteins to be Intrinsically Disordered

De novo creation of protein coding genes involves the formation of short ORFs from noncoding regions; some of these ORFs might then become fixed in the populationThese orphan proteins need to, at the bare minimum, not cause serious harm to the organism, meaning that they should for instance not aggregate. Therefore, although the creation of short ORFs could be truly random, the fixation should be subjected to some selective pressure. The selective forces acting on orphan proteins have been elusive, and contradictory results have been reported. In Drosophila young proteins are more disordered than ancient ones, while the opposite trend is present in yeast. To the best of our knowledge no valid explanation for this difference has been proposed.\n\nTo solve this riddle we studied structural properties and age of proteins in 187 eukaryotic organisms. We find that, with the exception of length, there are only small differences in the properties between proteins of different ages. However, when we take the GC content into account we noted that it could explain the opposite trends observed for orphans in yeast (low GC) and Drosophila (high GC). GC content is correlated with codons coding for disorder promoting amino acids. This leads us to propose that intrinsic disorder is not a strong determining factor for fixation of orphan proteins. Instead these proteins largely resemble random proteins given a particular GC level. During evolution the properties of a protein change faster than the GC level causing the relationship between disorder and GC to gradually weaken.\n\nAuthor SummaryWe show that the GC content of a genome is of great importance for the properties of an orphan protein. GC content affects the frequency of the codons and this affects the probability for each amino acid to be included in a de novo created protein. The codons encoding for Ala, Pro and Gly contain 80% GC, while codons for Lys, Phe, Asn, Tyr and Ile contain 20% or less. The three high GC amino acids are all disorder promoting, while Phe, Tyr and Ile are order promoting. Therefore, random protein sequences at a high GC will be more disordered than the ones created at a low GC. The structural properties of the youngest proteins match to a large degree the properties of random proteins when the GC content is taken into account. In contrast, structural properties of ancient proteins only show a weak correlation with GC content. This suggests that even after fixation in the population, proteins largely resemble random proteins given a certain GC content. Thereafter, during evolution the correlation between structural properties and GC weakens.

evolutionary biology↗

bioRxiv2017

Joint estimation of relatedness coefficients and allele frequencies from ancient samples

We develop and test a method to address whether DNA samples sequenced from a group of fossil hominin bone or teeth fragments originate from the same individual or from closely related individuals. Our method assumes low amounts of retrievable DNA, significant levels of sequencing error and contamination from one or more present-day humans. We develop and implement a maximum likelihood method that estimates levels of contamination, sequencing error rates and pairwise relatedness co-efficients in a set of individuals. We assume there is no reference panel for the ancient population to provide allele and haplotype frequencies. Our approach makes use of single nucleotide polymorphisms and does not make assumptions about the underlying demographic model. By artificially mating individual genomes from the 1000 Genomes Project, we determine the numbers of individuals at a given genomic coverage that are required to detect different levels of genetic relatedness with confidence.

evolutionary biology↗

bioRxiv2017

Multilevel And Sex-Specific Selection On Competitive Traits In North American Red Squirrels

Individuals often interact more closely with some members of the population (e.g. offspring, siblings or group members) than they do with other individuals. This structuring of interactions can lead to multilevel natural selection, where traits expressed at the group-level influence fitness alongside individual-level traits. Such multilevel selection can alter evolutionary trajectories, yet is rarely quantified in the wild, especially for species that do not interact in clearly demarcated groups. We quantified multilevel natural selection on two traits, postnatal growth rate and birth date, in a population of North American red squirrels (Tamiasciurus hudsonicus). The strongest level of selection was typically within-acoustic social neighbourhoods (within 130m of the nest), where growing faster and being born earlier than nearby litters was key, while selection on growth rate was also apparent both within-litters and within-study areas. Higher population densities increased the strength of selection for earlier breeding, but did not influence selection on growth rates. Females experienced especially strong selection on growth rate at the within-litter level, possibly linked to the biased bequeathal of the maternal territory to daughters. Our results demonstrate the importance of considering multilevel and sex-specific selection in wild species, including those that are territorial and sexually monomorphic.\n\nData archival: the data set is archived on Dryad (info XXX), with a five-year embargo from the date of publication.

evolutionary biology↗

bioRxiv2017

Bounds to Parapatric Speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes and mitochondria

We investigate the conditions for the origin and maintenance of postzygotic isolation barriers, so called (Bateson-)Dobzhansky-Muller incompatibilities or DMIs, among populations that are connected by gene flow. Specifically, we compare the relative stability of pairwise DMIs among autosomes, X chromosomes, and mitochondrial genes. In an analytical approach based on a continent-island framework, we determine how the maximum permissible migration rates depend on the genomic architecture of the DMI, on sex bias in migration rates, and on sex-dependence of allelic and epistatic effects, such as dosage compensation. Our results show that X-linkage of DMIs can enlarge the migration bounds relative to autosomal DMIs or autosome-mitochondrial DMIs, in particular in the presence of dosage compensation. The effect is further strengthened with male-biased migration. This mechanism might contribute to a higher density of DMIs on the X chromosome (large X-effect) that has been observed in several species clades. Furthermore, our results agree with empirical findings of higher introgression rates of autosomal compared to X-linked loci.

evolutionary biology↗

bioRxiv2017

Genome-wide signatures of genetic variation within and between populations - a comparative perspective

Genome-wide screens of genetic variation can reveal signatures of population-specific selection implicated in adaptation and speciation. Yet, unrelated processes such as linked selection arising as a consequence of genome architecture can generate comparable signatures across taxa. To investigate prevalence and phylogenetic stability of linked selection, we took a comparative approach utilizing population-level data from 444 re-sequenced genomes of three avian clades spanning 50 million years of evolution. Levels of nucleotide diversity ({pi}),population-scaled recombination rate ({rho}), genetic differentiation (FST, PBS) and sequence divergence (Dxy) were remarkably similar in syntenic genomic regions across clades. Elevated local genetic differentiation was associated with inferred centromere and sub-telomeric regions. Our results support a role of linked selection shaping genome-wide heterogeneity in genetic diversity within and between clades. The long-term conservation of diversity landscapes and stable association with genomic features make the outcome of this evolutionary process in part predictable.

evolutionary biology↗

bioRxiv2017

Network analysis of the hominin origin of Herpes Simplex virus 2 from fossil data

Herpes simplex virus 2 is a human herpesvirus found worldwide that causes genital lesions and more rarely causes encephalitis. This pathogen is most common in Africa, and particularly in central and east Africa, an area of particular significance for the evolution of modern humans. Unlike HSV1, HSV2 has not simply co-speciated with humans from their last common ancestor with primates. HSV2 jumped the species barrier between 1.4 and 3 MYA, most likely through an intermediate but unknown hominin species.\n\nIn this paper, we use probability-based network analysis to determine the probable path between intermediate hosts of HSV2, from chimpanzees to modern humans, using paleoenvironmental data on the distribution of African tropical rainforest over the last 3 million years and data on the age and distribution of fossil species of hominin present in Africa between 1.4 and 3 MYA. Our model identifies Homo rudolfensis as the most likely intermediate host of HSV2

evolutionary biology↗

bioRxiv2017

Genetic equidistance at the nucleotide level

The genetic equidistance phenomenon was first discovered in 1963 by Margoliash and shows complex taxa to be all approximately equidistant to a less complex species in amino acid percentage identity. The result has been mis-interpretated by the ad hoc universal molecular clock hypothesis, and the much overlooked mystery was finally solved by the maximum genetic diversity hypothesis (MGD). Here, we studied 15 proteomes and their coding DNA sequences (CDS) to see if the equidistance phenomenon also holds at the CDS level. We performed DNA alignments for a total of 5 groups with 3 proteomes per group and found that in all cases the outgroup taxon was equidistant to the two more complex taxa species at the DNA level. Also, when two sister taxa (snake and bird) were compared to human as the outgroup, the more complex taxon bird was closer to human, confirming species complexity rather than time to be the primary determinant of MGD. Finally, we found the fraction of overlap sites where coincident substitutions occur to be inversely correlated with CDS conservation, indicating saturation to be more common in less conserved DNAs. These results establish the genetic equidistance phenomenon to be universal at the DNA level and provide additional evidence for the MGD theory.

evolutionary biology↗

bioRxiv2017

Effects of Historical Coinfection on Host Shift Abilities of Exploitative and Competitive Viruses

Rapid evolution contributes to frequent emergence of RNA viral pathogens on novel hosts. However, accurately predicting which viral genotypes will emerge has been elusive. Prior work with lytic RNA bacteriophage f6 (family Cystoviridae) suggested that evolution under low multiplicity of infection (MOI; proportion of viruses to susceptible cells) selected for greater host exploitation, while evolution under high MOI selected for better intracellular competition against co-infecting viruses. We predicted that phage genotypes that experienced 300 generations of low MOI ecological history would be relatively advantaged in growth on two novel hosts. We inferred viral growth through changes in host population density, specifically by analyzing five attributes of growth curves of infected bacteria. Despite equivalent growth of evolved viruses on the original host, low MOI evolved clones were generally advantaged relative to high MOI clones in exploiting novel hosts. We also observed genotype-specific differences in clone infectivity: High fitness genotypes on the original host also performed better on novel hosts. Our results indicated that traits allowing greater exploitation of the original host correlated positively with performance on novel hosts. Based on infectivity differences of viruses from high versus low MOI histories, we suggest that prior MOI selection can later affect emergence potential.

evolutionary biology↗

bioRxiv2017

Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting-edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 82-88%, over the 12-18% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell-intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non-senescence, or negative senescence. We end by discussing whether similar levels of non-genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.\n\nData depositionThe processed image analysis data, R code, as well as the Leslie matrices will be archived at Dryad.org.

evolutionary biology↗