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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↗

bioRxiv2017

Extensive Copy Number Variation in Fermentation-Related Genes among Saccharomyces cerevisiae Wine Strains

Due to the importance of Saccharomyces cerevisiae in wine-making, the genomic variation of wine yeast strains has been extensively studied. One of the major insights stemming from these studies is that wine yeast strains harbor low levels of genetic diversity in the form of single nucleotide polymorphisms (SNPs). Genomic structural variants, such as copy number (CN) variants, are another major type of variation segregating in natural populations. To test whether genetic diversity in CN variation is also low across wine yeast strains, we examined genome-wide levels of CN variation in 132 whole-genome sequences of S. cerevisiae wine strains. We found an average of 97.8 CN variable regions (CNVRs) affecting ~4% of the genome per strain. Using two different measures of CN diversity, we found that gene families involved in fermentation-related processes such as copper resistance (CUP), flocculation (FLO), and glucose metabolism (HXT), as well as the SNO gene family whose members are expressed before or during the diauxic shift showed substantial CN diversity across the 132 strains examined. Importantly, these same gene families have been shown, through comparative transcriptomic and functional assays, to be associated with adaptation to the wine fermentation environment. Our results suggest that CN variation is a substantial contributor to the genomic diversity of wine yeast strains and identify several candidate loci whose levels of CN variation may affect the adaptation and performance of wine yeast strains during fermentation.

evolutionary biology↗

bioRxiv2017

Environmental correlates of internal coloration in anurans vary throughout space and lineages

Internal organs of ectotherms have melanin-containing cells. Several studies analyzed their developmental origin, role in immunity, and hormonal regulation. However, little is known about how environmental variables influence the distribution and quantity of organ coloration. Here, we addressed how environmental variables (temperature, UV, and photoperiod) influence the internal coloration of amphibians after controlling for spatial and phylogenetic autocorrelations. Coloration in all organs was correlated with phylogeny. However, the coloration of the heart, kidneys, and rectum of hylids, R. schneideri, some Leptodactylus, and Proceratophrys were influenced by temperature and photoperiod, whereas that of the testicle, lumbar parietal peritoneum, lungs, and mesenterium of Leiuperinae, Hylodidae, Adenomera, most Leptodactylus were influenced by UVB and temperature variation. Therefore, the amount of internal melanin seems to be a key trait influencing species distribution of frogs throughout space, since it can protect internal organs against the deleterious effect of high UV-B, temperature variation, and photoperiod.\n\nSignificanceThe functions of internal coloration in fishes and frogs are little known. Internal pigmentation is commonly altered in fish and the degree of response is correlated with body transparency levels, suggesting possible adaptive functions. Here, we assume that internal melanin has protective functions against UV-B, temperature variation, and photoperiod. Thus it could influence frogs species distribution throughout space. The melanin coloration of each organ was influenced by distinct environmental variables depending on the lineages of species. Our results could direct further studies about the functions of internal coloration.

evolutionary biology↗

bioRxiv2017

Genetic analysis reveals efficient sexual spore dispersal at a fine spatial scale in Armillaria ostoyae, the causal agent of root-rot disease in conifers

Armillaria ostoyae (sometimes named A. solidipes) is a fungal species causing root diseases in numerous coniferous forests of the northern hemisphere. The importance of sexual spores for the establishment of new disease centers remains unclear, particularly in the large maritime pine plantations of southwestern France. An analysis of the genetic diversity of a local fungal population distributed over 500 ha in this French forest showed genetic recombination between genotypes to be frequent, consistent with regular sexual reproduction within the population. The estimated spatial genetic structure displayed a significant pattern of isolation by distance, consistent with the dispersal of sexual spores mostly at the spatial scale studied. Using these genetic data, we inferred an effective density of reproductive individuals of 0.1 to 0.3 individuals/ha, and a second moment of parent-progeny dispersal distance of 130 to 800 m, compatible with the main models of fungal spore dispersal. These results contrast with those obtained for studies of A. ostoyae over larger spatial scales, suggesting that inferences about mean spore dispersal may be best performed at fine spatial scales (i.e. a few kilometers) for most fungal species.

evolutionary biology↗

bioRxiv2017

North Andean origin and diversification of the largest ithomiine butterfly genus

The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification here remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.

evolutionary biology↗

bioRxiv2017

Bayesian molecular dating as a "doubly intractable" problem

1This study focuses on a conceptual issue with Bayesian inference of divergence times using Markov chain Monte Carlo. The influence of fossil data on the probabilistic distribution of trees is the crux of the matter considered here. More specifically, among all the phylogenies that a tree model (e.g., the birth-death process) generates, only a fraction of them \"agree\" with the fossil data at hands. Bayesian inference of divergence times using Markov Chain Monte Carlo requires taking this fraction into account. Yet, doing so is challenging and most Bayesian samplers have simply overlooked this hurdle so far, thereby providing approximate estimates of divergence times and tree process parameters. A generic solution to this issue is presented here. This solution relies on an original technique, the so-called exchange algorithm, dedicated to drawing samples from \"doubly intractable\" distributions. A small example illustrates the problem of interest and the impact of the approximation aforementioned on tree parameter estimates. The analysis of land plant sequences and multiple fossils further illustrates the importance of proper mathematical handling of calibration data in order to derive accurate estimates of node age.

evolutionary biology↗

bioRxiv2017

Approximate Bayesian Computation Algorithms for Estimating Network Model Parameters

Studies on Approximate Bayesian Computation (ABC) replacing the intractable likelihood function in evaluation of the posterior distribution have been developed for several years. However, their field of application has to date essentially been limited to inference in population genetics. Here, we propose to extend this approach to estimating the structure of transmission networks of viruses in human populations. In particular, we are interested in estimating the transmission parameters under four very general network structures: random, Watts-Strogatz, Barabasi-Albert and an extension that incorporates aging. Estimation was evaluated under three approaches, based on ABC, ABC-Markov chain Monte Carlo (ABC-MCMC) and ABC-Sequential Monte Carlo (ABC-SMC) samplers. We show that ABC-SMC samplers outperform both ABC and ABC-MCMC, achieving high accuracy and low variance in simulations. This approach paves the way to estimating parameters of real transmission networks of transmissible diseases.

evolutionary biology↗

bioRxiv2017

Strong purifying selection on codon usage bias

1Codon usage bias (CUB), where certain codons are used more frequently than expected by chance, is a ubiquitous phenomenon and occurs across the tree of life. The dominant paradigm is that the proportion of preferred codons is set by weak selection. While experimental changes in codon usage have at times shown large phenotypic effects in contrast to this paradigm, genome-wide population genetic estimates have supported the weak selection model. Here we use deep genomic sequencing of two Drosophila melanogaster populations to measure selection on synonymous sites in a way that allowed us to estimate the prevalence of both weak and strong selection. We find that selection in favor of preferred codons ranges from weak (|Nes| [~] 1) to strong (|Nes| > 10). While previous studies indicated that selection at synonymous sites could be strong, this is the first study to detect and quantify strong selection specifically at the level of CUB. We suggest that the level of CUB in the genome is determined by the proportion of synonymous sites under no, weak, and strong selection. This model challenges the standard Li-Bulmer model and explains some of the longest-standing puzzles in the field.

evolutionary biology↗

bioRxiv2017

Evolution of the α2-adrenoreceptors in vertebrates: ADRA2D is absent in mammals and crocodiles

Evolutionary studies of genes that have been functionally characterized and whose variation has been associated with pathological conditions represent an opportunity to understand the genetic basis of pathologies. 2-adrenoreceptors (ADRA2) are a class of G protein-coupled receptors that regulate several physiological processes including blood pressure, platelet aggregation, insulin secretion, lipolysis, and neurotransmitter release. This gene family has been extensively studied from a molecular/physiological perspective, yet much less is known about its evolutionary history. Accordingly, the goal of this study was to investigate the evolutionary history of 2-adrenoreceptors (ADRA2) in vertebrates. Our results show that in addition to the three well-recognized 2-adrenoreceptor genes (ADRA2A, ADRA2B and ADRA2C), we recovered a clade that corresponds to the fourth member of the 2-adrenoreceptor gene family (ADRA2D). We also recovered a clade that possesses two ADRA2 sequences found in two lamprey species. Furthermore, our results show that mammals and crocodiles are characterized by possessing three 2-adrenoreceptor genes, whereas all other vertebrate groups possess the full repertoire of 2-adrenoreceptor genes. Among vertebrates ADRA2D seems to be a dispensable gene, as it was lost two independent times during the evolutionary history of the group. Additionally, we found that most examined species possess the most common alleles described for humans; however, there are cases in which non-human mammals possess the alternative variant.

evolutionary biology↗

bioRxiv2017

Hitchhiking and epistasis give rise to cohort dynamics in adapting populations

Beneficial mutations are the driving force of adaptive evolution. In asexual populations, the identification of beneficial alleles is confounded by the presence of genetically-linked hitchhiker mutations. Parallel evolution experiments enable the recognition of common targets of selection, yet these targets are inherently enriched for genes of large target size and mutations of large effect. A comprehensive study of individual mutations is necessary to create a realistic picture of the evolutionarily significant spectrum of beneficial mutations. Here we utilize a bulk-segregant approach to identify the beneficial mutations across 11 lineages of experimentally-evolved yeast populations. We report that most genome sequence evolution is non-adaptive: nearly 80% of detected mutations have no discernable effects on fitness and less than 1% are deleterious. We determine the distribution of driver and hitchhiker mutations in 31 mutational cohorts, groups of up to ten mutations that arise synchronously from low frequency and track tightly with one another. Surprisingly, we find that one-third of cohorts lack identifiable driver mutations. In addition, we identify intra-cohort synergistic epistasis between mutations in hsl7 and kel1, which arose together in a low frequency lineage.

evolutionary biology↗

bioRxiv2017

Re-evaluating inheritance in genome evolution: widespread transfer of LINEs between species

Transposable elements (TEs) are mobile DNA sequences, colloquially known as jumping genes because of their ability to replicate to new genomic locations. Given a vector of transfer (e.g. tick or virus), TEs can jump further: between organisms or species in a process known as horizontal transfer (HT). Here we propose that LINE-1 (L1) and Bovine-B (BovB), the two most abundant TE families in mammals, were initially introduced as foreign DNA via ancient HT events. Using a 503-genome dataset, we identify multiple ancient L1 HT events in eukaryotes and provide evidence that L1s infiltrated the mammalian lineage after the monotreme-therian split. We also extend the BovB paradigm by increasing the number of estimated transfer events compared to previous studies, finding new potential blood-sucking parasite vectors and occurrences in new lineages (e.g. bats, frog). Given that these TEs make up nearly half of the genome sequence in todays mammals, our results provide the first evidence that HT can have drastic and long-term effects on the new host genomes. This revolutionizes our perception of genome evolution to consider external factors, such as the natural introduction of foreign DNA. With the advancement of genome sequencing technologies and bioinformatics tools, we anticipate our study to be the first of many large-scale phylogenomic analyses exploring the role of HT in genome evolution.\n\nSignificance statementLINE-1 (L1) elements occupy about half of most mammalian genomes (1), and they are believed to be strictly vertically inherited (2). Mutagenic L1 insertions are thought to account for approximately 1 of every 1000 random, disease-causing insertions in humans (4-7). Our research indicates that the very presence of L1s in humans, and other therian mammals, is due to an ancient transfer event - which has drastic implications for our perception of genome evolution. Using a machina analyses over 503 genomes, we trace the origins of L1 and BovB retrotransposons across the tree of life, and provide evidence of their long-term impact on eukaryotic evolution.

evolutionary biology↗

bioRxiv2017

Recent Regulatory Changes Shaped the Human Facial and Vocal Anatomy

SummaryRegulatory changes are broadly accepted as key drivers of phenotypic divergence. However, identifying regulatory changes that underlie human-specific traits has proven very challenging. Here, we use 63 DNA methylation maps of ancient and present-day humans, as well as of six chimpanzees, to detect differentially methylated regions that emerged in modern humans after the split from Neanderthals and Denisovans. We show that genes affecting the face and vocal tract went through particularly extensive methylation changes. Specifically, we identify widespread hypermethylation in a network of face- and voice-affecting genes (SOX9, ACAN, COL2A1, NFIX and XYLT1). We propose that these repression patterns appeared after the split from Neanderthals and Denisovans, and that they might have played a key role in shaping the modern human face and vocal tract.View Full Text

evolutionary biology↗