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bioRxiv2017

phydms: Software for phylogenetic analyses informed by deep mutational scanning

BackgroundThe evolution of protein-coding genes can be quantitatively modeled using phylogenetic methods. Recently, it has been shown that high-throughput experimental measurements of mutational effects made via deep mutational scanning can inform site-specific phylogenetic substitution models of gene evolution. However, there is currently no software tailored for such analyses.\n\nResultsWe describe software that efficiently performs phylogenetic analyses with substitution models informed by deep mutational scanning. This software, phydms, is [~]100-fold faster than existing programs that accommodate such substitution models. It can be used to compare the results of deep mutational scanning experiments to the selection on genes in nature. For instance, phydms enables rigorous comparison of how well different experiments on the same gene describe natural selection. It also enables the re-scaling of deep mutational scanning data to account for differences in the stringency of selection in the lab and nature. Finally, phydms can identify sites that are evolving differently in nature than expected from experiments in the lab.\n\nConclusionsThe phydms software makes it easy to use phylogenetic substitution models informed by deep mutational scanning experiments. As data from such experiments becomes increasingly widespread, phydms will facilitate quantitative comparison of the experimental results to the actual selection pressures shaping evolution in nature.

evolutionary biology↗

bioRxiv2017

Genetic costs of domestication and improvement

The cost of domestication hypothesis posits that the process of domesticating wild species can result in an increase in the number, frequency, and/or proportion of deleterious genetic variants that are fixed or segregating in the genomes of domesticated species. This cost may limit the efficacy of selection and thus reduce genetic gains in breeding programs for these species. Understanding when and how deleterious mutations accumulate can also provide insight into fundamental questions about the interplay of demography and selection. Here we describe the evolutionary processes that may contribute to deleterious variation accrued during domestication and improvement, and review the available evidence for the cost of domestication in animal and plant genomes. We identify gaps and explore opportunities in this emerging field, and finally offer suggestions for researchers and breeders interested in understanding or avoiding the consequences of an increased number or frequency of deleterious variants in domesticated species.

evolutionary biology↗

bioRxiv2017

Mitochondrial genome variation affects the mutation rate of the nuclear genome in Drosophila melanogaster

Mutations are the raw material for evolutionary change. While the mutation rate has been thought constant between individuals, recent research has shown that poor genetic condition can elevate the mutation rate. Mitonuclear genetic conflict is a potential source of poor genetic condition, and considering the high mutation rate of mitochondrial genomes, there should be ample scope for mitochondrial mutations to interfere with genetic condition, with concomitant effects on the nuclear mutation rate. Moreover, because theory suggests mitochondrial genetic effects will often be male-biased, such effects could be more strongly felt in males than females. Here, by mating irradiated male Drosophila melanogaster to isogenic females bearing six distinct mitochondrial haplotypes, we tested whether mitochondrial genetic variation affects DNA repair capacity, and whether effects of mutation load on reproductive function are shaped by interactions between sex and mitochondrial haplotype. We found mitochondrial genetic effects on DNA repair, and that the mutational variance of reproductive fitness was higher in males bearing haplotypes characterized by high female fitness. These results suggest that mitochondrial genome variation may affect the mutation rate, and that induced mutations interact more strongly with male than female reproductive function. The potential for haplotype-specific effects on the nuclear mutation rate has broad implications for evolutionary dynamics, such as the accumulation of genetic load, adaptive potential, and the evolution of sexual dimorphism.

evolutionary biology↗

bioRxiv2017

Draft genome of the Heterotardigrade Milnesium tardigradum sheds light on ecdysozoan evolution

Tardigrades are among the most stress tolerant animals and survived even unassisted exposure to space in low earth orbit. Still, the adaptations leading to these unusual physiological features remain unclear. Even the phylogenetic position of this phylum within the Ecdysozoa is unclear. Complete genome sequences might help to address these questions as genomic adaptations can be revealed and phylogenetic reconstructions can be based on new markers. Here, we present a first draft genome of a species from the family Milnesiidae, namely Milnesium tardigradum. We consistently place M. tardigradum and the two previously sequenced Hypsibiidae species, Hypsibius dujardini and Ramazzottius varieornatus, as sister group of the nematodes with the arthropods as outgroup. Based on this placement, we identify a massive gene loss thus far attributed to the nematodes which predates their split from the tardigrades. We provide a comprehensive catalog of protein domain expansions linked to stress response and show that previously identified tardigrade-unique proteins are erratically distributed across the genome of M. tardigradum. We further suggest alternative pathways to cope with high stress levels that are yet unexplored in tardigrades and further promote the phylum Tardigrada as a rich source of stress protection genes and mechanisms.

evolutionary biology↗

bioRxiv2017

On reciprocal causation in the evolutionary process

Recent calls for a revision of standard evolutionary theory (SET) are based in part on arguments about the reciprocal causation. Reciprocal causation means that cause-effect relationships are obscured, as a cause could later become an effect and vice versa. Such dynamic cause-effect relationships raise questions about the distinction between proximate and ultimate causes, as originally formulated by Ernst Mayr. They have also motivated some biologists and philosophers to argue for an Extended Evolutionary Synthesis (EES). The EES will supposedly expand the scope of the Modern Synthesis (MS) and Standard Evolutionary Theory (SET), which has been characterized as gene-centred, relying primarily on natural selection and largely neglecting reciprocal causation. I critically examine these claims, with a special focus on the last conjecture and conclude - on the contrary- that reciprocal causation has long been recognized as important both in SET and in the MS tradition, although it remains underexplored. Numerous empirical examples of reciprocal causation in the form of positive and negative feedbacks are now well known from both natural and laboratory systems. Reciprocal causation have also been explicitly incorporated in mathematical models of coevolutionary arms races, frequency-dependent selection, eco-evolutionary dynamics and sexual selection. Such dynamic feedbacks were already recognized by Richard Levins and Richard Lewontin, well before the recent call for an EES. Reciprocal causation and dynamic feedbacks is one of the few contributions of dialectical thinking and Marxist philosophy in evolutionary theory, and should be recognized as such. I discuss some promising empirical and analytical tools to study reciprocal causation and the implications for the EES. While reciprocal causation have helped us to understand many evolutionary processes, I caution against uncritical extension of dialectics towards heredity and constructive development, particularly if such extensions involves attempts to restore Lamarckian or \"soft inheritance\".

evolutionary biology↗

bioRxiv2017

Rate Of Fixation Of Rare Variants In A Population

The process of molecular evolution has been dominated by the Kimura paradigm for nearly 60 years; mutations arise at a certain rate in the population and they go to fixation with a probability given by Kimuras classic formula, which assumes there are no further mutations that interfere with the fixation process. An alternative view is that rare variants exist in the population in a mutation-drift-selection balance and rise to fixation through a combination of chance (genetic drift), selection and mutation. When mutations increase in strength, but still in the weak regime, we would expect the Kimura rate approximation to be an overestimate, as a rare variant which grows in frequency will suffer a greater backward flux of mutations, slowing progress to fixation. However, to date calculating important quantities for a general model of selection and mutation, like the rate of fixation of these rare variants has not been tractable in the conventional diffusion approximation of population genetics. Here, we use Fishers angular transformation to convert the frequency-dependent diffusion inherent in population genetics to simple diffusion in an effective potential, which describes the forces of selection, drift and mutation. Once this potential is defined it is simple to show that the mean first passage time is given by a double integral which relate to populations at the barrier. Exact numerical integration shows excellent agreement with discrete Wright-Fisher simulations, which do show a slowing down of the fixation of mutants at higher mutation rates and for strong positive selection, compared to the Kimura prediction. We then seek a closed-form analytical expression for the rate of fixation of mutants, by adapting Kramers approximation for the mean first passage time. This overall gives an accurate approximation, but however, does not improve on the Kimura rate.

evolutionary biology↗

bioRxiv2017

Pairwise Hybrid Incompatibilities Dominate During Allopatric Speciation For A Simple Genotype-Phenotype Map Of Embryonic Spatial Patterning

Developmental system drift is a likely mechanism for the origin of hybrid incompatibilities between closely related species. We examine here the detailed mechanistic basis of hybrid incompatibilities for a genotype-phenotype map for developmental system drift under stabilising selection, where the organismal phenotype is conserved, but the underlying molecular phenotypes and genotype can drift. This leads to number of emergent phenomenon not obtainable by modelling genotype or phenotype alone. Our results show that: 1) speciation is more rapid at smaller population sizes with a characteristic, Orr-like, power law, but at large population sizes slow, characterised by a sub-diffusive growth law; 2) the molecular phenotypes under weakest selection contribute to the earliest incompatibilities; and 3) pairwise incompatibilities dominate over higher order, contrary to previous predictions that the latter should dominate. Our results indicate that biophysics and population size provide a much stronger constraint to speciation than suggested by previous models.

evolutionary biology↗

bioRxiv2017

Temporal Niche Expansion In Mammals From A Nocturnal Ancestor After Dinosaur Extinction

Most modern mammals, including strictly diurnal species, exhibit sensory adaptations to nocturnal activity, thought to be the result of a prolonged nocturnal phase or bottleneck during early mammalian evolution. Nocturnality may have allowed mammals to avoid antagonistic interactions with diurnal dinosaurs during the Mesozoic. However, understanding the evolution of mammalian activity patterns is hindered by scant and ambiguous fossil evidence. While ancestral reconstructions of behavioural traits from extant species have the potential to elucidate these patterns, existing studies have been limited in taxonomic scope. Here, we use an extensive behavioural dataset for 2415 species from all extant orders to reconstruct ancestral activity patterns across Mammalia. We find strong support for the nocturnal origin of mammals and the Cenozoic appearance of diurnality, although cathemerality (mixed diel periodicity) may have appeared in the late Cretaceous. Simian primates are among the earliest mammals to exhibit strict diurnal activity, some 52-33Mya. Our study is consistent with the hypothesis that temporal partitioning between early mammals and dinosaurs during the Mesozoic led to a mammalian nocturnal bottleneck, but also demonstrates the need for improved phylogenetic estimates for Mammalia.

evolutionary biology↗

bioRxiv2017

Progressive Multiple Sequence Alignment With The Poisson Indel Process

Sequence alignment lies at the heart of many evolutionary and comparative genomics studies. However, the optimal alignment of multiple sequences is NP-hard, so that exact algorithms become impractical for more than a few sequences. Thus, state of the art alignment methods employ progressive heuristics, breaking the problem into a series of pairwise alignments guided by a phylogenetic tree. Changes between homologous characters are typically modelled by a continuous-time Markov substitution model. In contrast, the dynamics of insertions and deletions (indels) are not modelled explicitly, because the computation of the marginal likelihood under such models has exponential time complexity in the number of taxa. Recently, Bouchard-Cote and Jordan [PNAS (2012) 110(4):1160-1166] have introduced a modification to a classical indel model, describing indel evolution on a phylogenetic tree as a Poisson process. The model termed PIP allows to compute the joint marginal probability of a multiple sequence alignment and a tree in linear time. Here, we present an new dynamic programming algorithm to align two multiple sequence alignments by maximum likelihood in polynomial time under PIP, and apply it a in progressive algorithm. To our knowledge, this is the first progressive alignment method using a rigorous mathematical formulation of an evolutionary indel process and with polynomial time complexity.

evolutionary biology↗

bioRxiv2017

Rational Design Of A Novel Pollinator Interaction

Diversification of the ca. 250,000 extant flowering plant species has been driven in large part by coevolution with animal pollinators. A recurring pattern of pollinator shifts from hummingbird to hawkmoth pollination has characterized plant speciation in many western North American plant taxa, but in the genus Mimulus (monkeyflowers) section Erythranthe the evolution of hawkmoth pollination from hummingbird-pollinated ancestors has not occurred. We manipulated two flower color loci and tested the attractiveness of the resulting four color phenotypes (red, yellow, pink, white) to naive hawkmoths. Hawkmoths strongly prefer derived colors (yellow, pink, white) over the ancestral red, and prefer the two-locus change (white) to either of the single-locus changes (yellow, pink). The simple flower color genetics underlying this innate pollinator preference suggests a potential path for speciation into an unfilled hawkmoth-pollinated niche, and the deliberate design of a hawkmoth-pollinated flower demonstrates a new, predictive method for studying pollination syndrome evolution.

evolutionary biology↗

bioRxiv2017

Phylogenetic Conflict In Bears Identified By Automated Discovery Of Transposable Element Insertions In Low Coverage Genomes

Compared to sequence analyses, phylogenetic reconstruction from transposable elements (TEs) offers an additional perspective to study evolutionary processes. However, detecting phylogenetically informative TE insertions requires tedious experimental work, limiting the power of phylogenetic inference. Here, we analyzed the genomes of seven bear species using high throughput sequencing data to detect thousands of TE insertions. The newly developed pipeline for TE detection called TeddyPi (TE detection and discovery for Phylogenetic Inference) obtained 150,513 high-quality TE insertions in the genomes of ursine and tremarctine bears. By integrating different TE insertion callers and using a stringent filtering approach, the TeddyPi pipeline produced highly reliable TE insertion calls, which were confirmed by extensive in vitro validation experiments. Screening for single nucleotide substitutions in the flanking regions of the TEs show that these substitutions correlate with the phylogenetic signal from the TE insertions. Our phylogenomic analyses show that TEs are a major driver of genomic variation in bears and enabled phylogenetic reconstruction of a well-resolved species tree, even with strong signals for incomplete lineage sorting and introgression. The analyses show that the Asiatic black, sun and sloth bear form a monophyletic clade. TeddyPi is open source and can be adapted to various TE and structural variation callers. The pipeline makes it easy to confidently extract thousands of TE insertions even from low coverage genomes of non-model organisms, opening new possibilities for biologists to study phylogenies, evolutionary processes as well as rates and patterns of (retro-)transposition and structural variation.

evolutionary biology↗

bioRxiv2017

Diversity Predicts Ability Of Bacterial Consortia To Mitigate A Lethal Wildlife Pathogen

Symbiotic bacterial communities can protect their hosts from infection by pathogens. Treatment of wild individuals with protective bacteria isolated from hosts can combat the spread of emerging infectious diseases, but it is unclear whether the degree of bacterially-mediated host protection is uniform across multiple isolates of globally-distributed pathogens. Here we use the lethal amphibian fungal pathogen Batrachochytrium dendrobatidis as a model to investigate the traits predicting broad-scale in vitro inhibitory capabilities of both individual bacteria and multiple-bacterial consortia. We show that inhibition of multiple pathogen isolates is rare, with no clear phylogenetic signal at the genus level. Bacterial consortia offer stronger protection against B. dendrobatidis compared to single isolates, but critically this was only true for consortia containing multiple genera, and this pattern was not uniform across all B. dendrobatidis isolates. These novel insights have important implications for the effective design of bacterial probiotics to mitigate emerging infectious diseases.

evolutionary biology↗

bioRxiv2017

Regulatory Divergence In Wound-Responsive Gene Expression In Domesticated And Wild Tomato

BackgroundThe evolution of cis- and trans-regulatory components of transcription is central to how stress response and tolerance differ across species. However, it remains largely unknown how divergence in TF binding specificity and cis-regulatory sites contribute to the divergence of stress-responsive gene expression between wild and domesticated species.\n\nResultsUsing tomato as model, we analyzed the transcriptional profile of wound-responsive genes in wild Solanum pennellii and domesticated S. lycopersicum. We found that extensive expression divergence of wound-responsive genes is associated with speciation. To assess the degree of trans-regulatory divergence between these two species, 342 and 267 putative cis-regulatory elements (pCREs) in S. lycopersicum and S. pennellii, respectively, were identified that were predictive of wound-induced gene expression. We found that 35-66% of pCREs were conserved across species, suggesting that the remaining proportion (34-65%) of pCREs are species specific. This finding indicates a substantially higher degree of trans-regulatory divergence between these two plant species, which diverged [~]3-7 million years ago, compared to that observed in mouse and human, which diverged [~]100 million years ago. In addition, differences in pCRE sites were significantly associated with differences in wound-responsive gene expression between wild and domesticated tomato orthologs, suggesting the presence of substantial cis-regulatory divergence.\n\nConclusionsOur study provides new insights into the mechanistic basis of how the transcriptional response to wounding is regulated and, importantly, the contribution of cis- and trans-regulatory components to variation in wound-responsive gene expression during species domestication.

evolutionary biology↗

bioRxiv2017

Evolutionary compromises to environmental toxins: ammonia and urea tolerance in Drosophila suzukii and Drosophila melanogaster.

The invasive species Drosophila suzukii has evolved morphological and behavioral adaptations to lay eggs under the skin of fresh fruits. This results in severe damage of a wide range of small and stone fruits, thus making this species a serious agricultural and economical threat.\n\nDrosophila suzukii females typically lay few eggs per fruit, preferring not infested fruits. Hence larvae are exposed to a reduced amount of nitrogenous waste products. On the contrary, the innocuous Drosophila melanogaster lays eggs on fermented fruits already infested by conspecifics, with larvae developing in a crowded environment characterized by accumulation of nitrogenous waste such as ammonia and urea. Given these differences in oviposition and larval ecological niche, we expected different behavioral and physiological mechanisms in the two species to cope with nitrogenous waste. We investigated the impact of different concentrations of ammonia and urea on fecundity and larval development in both species. Females and larvae of D. suzukii showed a greater sensitivity to high concentration of both compounds, with a dramatic decrease in fecundity and egg viability.\n\nTo better understand the pathways underlying these differences, we evaluated the effect on ornithine aminotransferase and glutathione-S-transferase, two enzymes involved in nitrogen metabolism and stress response that are expressed during larval development. Under ammonia and urea exposure, the expression of these enzymes was significantly reduced in D. suzukii.\n\nThe fact that D. suzukiis shift from rotten to fresh fruit as oviposition and larval substrate resulted in less efficient detoxifying and excretory mechanisms represents a potential approach for its control. Fecundity and larval development are in fact dramatically impaired by nitrogen waste products. These findings can help in planning effective strategies of sustainable pest management that targets both females and larvae.

evolutionary biology↗

bioRxiv2017

Bayesian Inference Of Species Networks From Multilocus Sequence Data

Reticulate species evolution, such as hybridization or introgression, is relatively common in nature. In the presence of reticulation, species relationships can be captured by a rooted phylogenetic network, and orthologous gene evolution can be modeled as bifurcating gene trees embedded in the species network. We present a Bayesian approach to jointly infer species networks and gene trees from multilocus sequence data. A novel birth-hybridization process is used as the prior for the species network. We assume a multispecies network coalescent (MSNC) prior for the embedded gene trees. We verify the ability of our method to correctly sample from the posterior distribution, and thus to infer a species network, through simulations. We reanalyze a large dataset of genes from closely related spruces, and verify the previously suggested homoploid hybridization event in this clade. Our method is available within the BEAST 2 add-on SpeciesNetwork, and thus provides a general framework for Bayesian inference of reticulate evolution.

evolutionary biology↗

bioRxiv2017

Disentangling The Causes For Faster-X Evolution In Aphids

Faster evolution of X chromosomes has been documented in several species and results from the increased efficiency of selection on recessive alleles in hemizygous males and/or from increased drift due to the smaller effective population size of X chromosomes. Aphids are excellent models for evaluating the importance of selection in faster-X evolution, because their peculiar life-cycle and unusual inheritance of sex-chromosomes lead to equal effective population sizes for X and autosomes. Because we lack a high-density genetic map for the pea aphid whose complete genome has been sequenced, we assigned its entire genome to the X and autosomes based on ratios of sequencing depth in males and females. Unexpectedly, we found frequent scaffold misassembly, but we could unambiguously locate 13,726 genes on the X and 19,263 on autosomes. We found higher non-synonymous to synonymous substitutions ratios (dN/dS) for X-linked than for autosomal genes. Our analyses of substitution rates together with polymorphism and expression data showed that relaxed selection is likely to contribute predominantly to faster-X as a large fraction of X-linked genes are expressed at low rates and thus escape selection. Yet, a minor role for positive selection is also suggested by the difference between substitution rates for X and autosomes for male-biased genes (but not for asexual female-biased genes) and by lower Tajimas D for X-linked than for autosomal genes with highly male-biased expression patterns. This study highlights the relevance of organisms displaying alternative inheritance of chromosomes to the understanding of forces shaping genome evolution.

evolutionary biology↗

bioRxiv2017

Young Genes To The Front -- A Strategy For Future Resistance Against Powdery Mildew?

Nonhost resistance of a plant against a microbial pathogen can be the result of a long-lasting coevolutionary optimization of resource allocation in both host and pathogen. Although this has been suggested for years, coevolutionary aspects leading to nonhost resistance in plants are not fully understood yet. Instead, most studies focus on limited subsets of genes which are differentially expressed in infected plants to describe details of defense strategies and symptoms of diseases.\n\nHere, we exploit publicly available whole genome gene expression data and combine them with evolutionary characteristics of genes to uncover a mechanism of host-pathogen coevolution. Our results suggest that metabolic efficiency in gene regulation is a key aspect leading to nonhost resistance. In addition, we find that progressing host-pathogen coevolution is accompanied by subtle, but systematic overexpression of recently founded genes. In support of our plant-specific data, we observe similar effects in animal species.

evolutionary biology↗

bioRxiv2017

The Y-Chromosome Clarifies The Evolutionary History Of Sus scrofa By Large-Scale Deep Genome Sequencing

The genetics and evolution of sex chromosomes are largely distinct from autosomes and mitochondrial DNA (mtDNA). The Y chromosome offers unique genetic perspective on male-line inheritance. Here, we uncover novel evolutionary history of Sus scrofa based on 205 high-quality genomes from worldwide-distributed different wild boars and domestic pig breeds. We find that only two haplotypes exist in the distal and proximal blocks of at least 7.7 Mb on chromosome Y in pigs across European and Asian continents. And the times of most recent common ancestors (TMRCA) within both haplotypes, approximately 0.14 and 0.10 million years, are far smaller than their divergence time of around 1.07 million years. Whats more, the relationship between Sumatran and Eurasian continent Sus scrofa is much closer than that we knew before. And surprisingly, European pigs share the same haplotype with many Chinese pigs, which is not consistent with their deep splitting status on autosome and mtDNA. Further analyses show that the haplotype in Chinese pigs was likely introduced from European wild boars via ancient gene flow before pig domestication about 24k years ago. Low mutation rates and no recombination in the distal and proximal blocks on chromosome Y help us detect this male-driven ancient gene flow. Taken together, our results update the knowledge of pig demography and evolution, and might shed insight into the genetics and evolution studies on chromosome Y in other mammals.

evolutionary biology↗