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bioRxiv2016

Metazoan ribotoxin genes acquired by Horizontal Gene Transfer

Ribosome inactivating proteins (RIPs) are RNA N-glycosidases that depurinate a specific adenine residue in the conserved sarcin/ricin loop of 28S rRNA. These enzymes are widely distributed among plants and their presence has also been confirmed in several bacterial species. Recently, we reported for the first time in silico evidence of RIP encoding genes in metazoans, in two closely related species of insects: Aedes aegypti and Culex quinquefasciatus. Here, we have experimentally confirmed the presence of these genes in mosquitoes and attempted to unveil their evolutionary history. A detailed study was conducted, including evaluation of taxonomic distribution, phylogenetic inferences and microsynteny analyses, indicating that the culicine RIP genes derived from a single Horizontal Gene Transfer (HGT) event, probably from a Cyanobacterial donor species. Moreover, evolutionary analyses show that, after transference, these genes evolved under purifying selection, strongly suggesting that they play functional roles in these organisms. In this work we confirm the presence of RIP genes in Culicinae species, and show solid evidence supporting the hypothesis that these genes are derived from a single prokaryotic transferred gene through HGT. In addition, clear evidence of purifying selection pressure has been recorded, supporting the hypothesis that these genes are functional within this subfamily.

Evolutionary Biology↗

bioRxiv2016

Inference of the distribution of selection coefficients for new nonsynonymous mutations using large samples

The distribution of fitness effects (DFE) has considerable importance in population genetics. To date, estimates of the DFE come from studies using a small number of individuals. Thus, estimates of the proportion of moderately to strongly deleterious new mutations may be unreliable because such variants are unlikely to be segregating in the data. Additionally, the true functional form of the DFE is unknown, and estimates of the DFE differ significantly between studies. Here we present a flexible and computationally tractable method, called Fit{partial}a{partial}i, to estimate the DFE using the site frequency spectrum from a large number of individuals. We apply our approach to the frequency spectrum of 1300 Europeans from the Exome Sequencing Project ESP6400 dataset, 1298 Danes from the LuCamp dataset, and 432 Europeans from the 1000 Genomes Project to estimate the DFE of deleterious nonsynonymous mutations. We infer significantly fewer (0.38-0.84x) strongly deleterious mutations with selection coefficient |s| > 0.01 and more (1.24-1.43x) weakly deleterious mutations with selection coefficient |s| < 0.001 compared to previous estimates. Furthermore, a DFE that is a mixture distribution of a point mass at neutrality plus a gamma distribution fits best to two of the three datasets. Our results suggest that nearly neutral forces play a larger role in human evolution than previously thought.

Evolutionary Biology↗

bioRxiv2016

Reinforcement of conspecific sperm precedence weakens sexual selection in sympatric populations of Drosophila

Sexual selection is well recognized as a driver of reproductive isolation between lineages. However, selection for increased reproductive isolation could reciprocally change the outcomes of sexual selection, when these processes share a genetic basis. Direct selection for reproductive isolation occurs in the context of reinforcement, where selection acts to increase prezygotic barriers to reduce the cost of heterospecific matings. Many studies of reinforcement focus on premating reproductive barriers, however postmating traits-such as conspecific sperm precedence (CSP)-can also respond to reinforcing selection. We tested whether i) CSP responded to reinforcing selection, and ii) this response in sympatric populations altered intraspecific sperm competition (ISC) and the strength of sexual selection, with the sister species Drosophila pseudoobscura and D. persimilis. We used sperm competition experiments to evaluate differences in CSP and ISC between two sympatric and two allopatric populations of D. pseudoobscura. Using multiple genotypes for each population allowed us to estimate not only patterns of phenotype divergence, but also the opportunity for sexual selection within each population. Consistent with a pattern of reinforcement, the sympatric populations had higher mean CSP. Moreover, ISC was altered in sympatric populations, where we observed decreased average offensive sperm competitive ability against conspecific males, allowing less opportunity for sexual selection to operate within these populations. These data demonstrate that strong reinforcing selection for reproductive isolation can have consequences for sexual selection and sexual interactions within species, in these important postmating sperm competition traits.

Evolutionary Biology↗

bioRxiv2016

Evolution of Drift Robustness in Small Populations of Digital Organisms

Most mutations are deleterious and cause a reduction in population fitness known as the mutational load. In small populations, weakened selection against slightly-deleterious mutations results in an additional fitness reduction. Many studies have established that populations can evolve a reduced mutational load by evolving mutational robustness, but it is uncertain whether small populations can evolve a reduced susceptibility to drift-related fitness declines. Here, using mathematical modeling and digital experimental evolution, we show that small populations do evolve a reduced vulnerability to drift, or \"drift robustness\". We find that, compared to genotypes from large populations, genotypes from small populations have a decreased likelihood of small-effect deleterious mutations, thus causing small-population genotypes to be drift-robust. We further show that drift robustness is not adaptive, but instead arises because small populations preferentially adapt to drift-robust fitness peaks. These results have implications for genome evolution in organisms with small population sizes.

Evolutionary Biology↗

bioRxiv2016

Remating responses are shaped by male post-copulatory manipulation but not reinforcement in D. pseudoobscura

Reinforcement occurs when hybridization between closely related lineages produces low fitness offspring, prompting selection for elevated reproductive isolation specifically in areas of sympatry. Both pre-mating and post-mating prezygotic behaviors have been shown to be the target of reinforcing selection, but it remains unclear whether remating behaviors experience reinforcement, although they can also influence offspring identity and limit formation of hybrids. Here we evaluated evidence for reinforcing selection on remating behaviors in D. pseudoobscura, by comparing remating traits in females from populations historically allopatric and sympatric with D. persimilis. We found that the propensity to remate was not higher in sympatric females, compared to allopatric females, regardless of whether the first mated male was heterospecific or conspecific. Moreover, remating behavior did not contribute to interspecific reproductive isolation among any population; that is, females showed no higher propensity to remate following a heterospecific first mating than they were following a conspecific first mating. Instead, we found that females are less likely to remate after initial matings with unfamiliar males, regardless of species identity. This is consistent with one scenario of postmating sexual conflict in which females are poorly defended against post-copulatory manipulation by males with whom they have not co-evolved. Our results are generally inconsistent with reinforcement on remating traits, and suggest that this behavior might be more strongly shaped by the consequences of local antagonistic male-female interactions than interactions with heterospecifics.

Evolutionary Biology↗

bioRxiv2016

panX: pan-genome analysis and exploration

Horizontal transfer, gene loss, and duplication result in dynamic bacterial genomes shaped by a complex mixture of different modes of evolution. Closely related strains can differ in the presence or absence of many genes, and the total number of distinct genes found in a set of related isolates - the pan-genome - is often many times larger than the genome of individual isolates. We have developed a pipeline that efficiently identifies orthologous gene clusters in the pan-genome. This pipeline is coupled to a powerful yet easy-to-use web-based visualization software for interactive exploration of the pan-genome. The visualization consists of connected components that allow rapid filtering and searching of genes and inspection of their evolutionary history. For each gene cluster, panX displays an alignment, a phylogenetic tree, maps mutations within that cluster to the branches of the tree and infers gain and loss of genes on the core-genome phylogeny. PanX is available at pangenome.de. Custom pan-genomes can be visualized either using a webserver or by serving panX locally as a browser-based application.

Evolutionary Biology↗

bioRxiv2016

Radiation and hybridization of the Little Devil poison frog (Oophaga sylvatica) in Ecuador

Geographic variation of color pattern in the South American poison frogs (Dendrobatidae) is an intriguing evolutionary phenomenon. These chemically defended anurans use bright aposematic colors to warn potential predators of their unpalatibility. However, aposematic signals are frequency-dependent and individuals deviating from a local model are at a higher risk of predation. The well-known examples of Batesian and Mullerian mimics, hymenopterans (wasps and bees) and Heliconius butterflies, both support the benefits of unique models with relatively high frequencies. However, extreme diversity in the aposematic signal has been documented in the poison frogs of the genus Dendrobates, especially in the Oophaga subgenus. Here we investigate the phylogenetic and genomic differentiations among populations of Oophaga sylvatica, which exhibit one of the highest phenotypic diversification among poison frogs. Using a combination of PCR amplicons (mitochondrial and nuclear markers) and genome wide markers from a double-digested RAD data set, we characterize 13 populations (12 monotypic and 1 polytypic) across the O. sylvatica distribution. These populations are mostly separated in two lineages distributed in the Northern and the Southern part of their range in Ecuador. We found relatively low genetic differentiation within each lineage, despite considerable phenotypic variation, and evidence suggesting ongoing gene flow and genetic admixture among some populations of the Northern lineage. Overall these data suggest that phenotypic diversification and novelty in aposematic coloration can arise in secondary contact zones even in systems where phenotypes are subject to strong stabilizing selection.

Evolutionary Biology↗

bioRxiv2016

Evolutionary dynamics of an epigenetic switch in a fluctuating environment

Adaptation and survival in fluctuating environments is an evolutionary challenge faced by organisms. Epigenetic switches (bistable, molecular systems built from self-reinforcing feedback loops) have been suggested as a mechanism of bet-hedging and adaptation to fluctuating environments. These epigenetic systems are capable of spontaneously switching between phenotypes in the absence of DNA mutation and these phenotypes are stably inherited through multiple cell generations. The extent to which epigenetic switches outcompete adaptation through genetic mutation in fluctuating environments remains unexplored. To better understand the conditions that select for epigenetic switching, we used computer simulation to evolve a mechanistic model of a self-activating genetic circuit, which can adapt genetically and exhibit epigenetic switching. We evolved this model in a fluctuating environment under different selection pressures, mutation step-sizes, population sizes, and fluctuation frequencies. There was a trade-off between minimizing the adaptation time after each environmental transition and increasing the robustness of the phenotype during the constant environment between transitions. We show that surviving lineages evolved bistable, epigenetic switching to adapt quickly in fast fluctuating environments, whereas genetic adaptation was favored in slowly fluctuating environments. For some evolutionary conditions, a strategy emerged where the population adapted genetically between two bistable genotypes.

Evolutionary Biology↗

bioRxiv2016

Factors contributing to the accumulation of reproductive isolation: a mixed model approach

The analysis of large data sets describing reproductive isolation between species that vary in their degrees of relatedness has been extremely influential in the study of speciation. However, several limitations make it difficult to test specific hypotheses about which factors predict the evolution of reproductive isolation. In particular, the statistical methods typically used are limited in their ability to test complex hypotheses involving multiple predictor variables or interactions between variables; at least one method, the Mantel Test, has also been found to be unreliable. In this paper, I describe a framework to determine which factors contribute to the evolution of reproductive isolation using phylogenetic linear mixed models. Phylogenetic linear mixed models do not suffer from the same statistical limitations as other methods and I demonstrate the flexibility of this framework to analyze data collected at different evolutionary scales, to test both categorical and continuous predictor variables, and to test the effect of multiple predictors simultaneously, all of which cannot be achieved using any other single statistical method. I do so by re-analyzing several classic data sets and explicitly testing hypotheses that had previously been untested directly, including differences in accumulation of reproductive isolation between sympatric and allopatric species pairs.

Evolutionary Biology↗

bioRxiv2016

Panpulmonate transcriptomes reveal candidate genes involved in the adaptation to freshwater and terrestrial habitats in gastropods

BackgroundThe conquest of the land from aquatic habitats is a fascinating evolutionary event that happened multiple times in different phyla. Mollusks are among the organisms that successfully invaded the non-marine realm, resulting in the radiation of terrestrial panpulmonate gastropods. We compared transcriptomes from panpulmonates to study the selective pressures that modeled the transitions from marine into freshwater and terrestrial realms in this molluscan lineage.\n\nResultsDe novo assembly of six panpulmonate transcriptomes resulted in 55,000 - 97,000 predicted open reading frames, of which 9 - 14% were functionally annotated. Adding published transcriptomes, we predicted 791 ortholog clusters shared among fifteen panpulmonate species, resulting in 702 amino acid and 736 codon-wise alignments. The branch-site test of positive selection applied to the codon-wise alignments showed twenty-eight genes under positive selection in the freshwater lineages and seven in the terrestrial lineages. Gene ontology categories of these candidate genes include actin assembly, transport of glucose, and the tyrosine metabolism in the terrestrial lineages; and, DNA repair, metabolism of xenobiotics, mitochondrial electron transport, and ribosome biogenesis in the freshwater lineages.\n\nConclusionsWe identified candidate genes representing processes that may have played a key role during the water-to-land transition in Panpulmonata. These genes were involved in energy metabolism and gas-exchange surface development in the terrestrial lineages and in the response to the abiotic stress factors (UV radiation, osmotic pressure, xenobiotics) in the freshwater lineages. Our study expands the knowledge of possible adaptive signatures in genes and metabolic pathways related to the invasion of non-marine habitats in invertebrates.

Evolutionary Biology↗

bioRxiv2016

Genomic signature of kin selection in an ant with obligately sterile workers

Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes showed relaxed adaptive evolution compared to genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically-restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also showed relaxed selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory.

Evolutionary Biology↗

bioRxiv2016

The impacts of drift and selection on genomic evolution in holometabolous insects

Genomes evolve through a medley of mutation, drift, and selection, all of which act heterogeneously across genes and lineages. The pacemaker models of genomic evolution describe the resulting patterns of evolutionary rate variation: genes that are governed by the same pacemaker exhibit the same pattern of rate heterogeneity across lineages. However, the relative importance of drift and selection in determining the structure of these pacemakers is unknown. Here, we propose a novel phylogenetic approach to explain the formation of pacemakers. We apply this method to a genomic dataset from holometabolous insects, an ancient and diverse group of organisms. We show that when drift is the dominant evolutionary process, each pacemaker tends to govern a large number of fast-evolving genes. In contrast, strong negative selection leads to many distinct pacemakers, each of which governs a few slow-evolving genes. Our results provide new insights into the interplay between drift and selection in driving genomic evolution.

Evolutionary Biology↗

bioRxiv2016

Evolutionary Genetics of Insecticide Resistance and the Effects of Chemical Rotation

Repeated use of the same class of pesticides to control a target pest is a form of artificial selection that leads to pesticide resistance. We studied insecticide resistance and cross-resistance to five commercial insecticides in each of six populations of the red flour beetle, Tribolium castaneum. We estimated the dosage response curves for lethality in each parent population for each insecticide and found an 800-fold difference among populations in resistance to insecticides. As expected, a naive laboratory population was among the most sensitive of populations to most insecticides. We then used inbred lines derived from five of these populations to estimate the heritability (h2) of resistance for each pesticide and the genetic correlation (rG) of resistance among pesticides in each population. These quantitative genetic parameters allow insight into the adaptive potential of populations to further evolve insecticide resistance. Lastly, we use our estimates of the genetic variance and covariance of resistance and stochastic simulations to evaluate the efficacy of \"windowing\" as an insecticide resistance management strategy, where the application of several insecticides is rotated on a periodic basis.

Evolutionary Biology↗

bioRxiv2016

Population-genomic inference of the strength and timing of selection against gene flow

The interplay of divergent selection and gene flow is key to understanding how populations adapt to local environments and how new species form. Here, we use DNA polymorphism data and genome-wide variation in recombination rate to jointly infer the strength and timing of selection, as well as the baseline level of gene flow under various demographic scenarios. We model how divergent selection leads to a genome-wide negative correlation between recombination rate and genetic differentiation among populations. Our theory shows that the selection density, i.e. the selection coefficient per base pair, is a key parameter underlying this relationship. We then develop a procedure for parameter estimation that accounts for the confounding effect of background selection. Applying this method to two datasets from Mimulus guttatus, we infer a strong signal of adaptive divergence in the face of gene flow between populations growing on and off phytotoxic serpentine soils. However, the genome-wide intensity of this selection is not exceptional compared to what M. guttatus populations may typically experience when adapting to local conditions. We also find that selection against genome-wide introgression from the selfing sister species M. nasutus has acted to maintain a barrier between these two species over at least the last 250 ky. Our study provides a theoretical framework for linking genome-wide patterns of divergence and recombination with the underlying evolutionary mechanisms that drive this differentiation.

Evolutionary Biology↗

bioRxiv2016

Genes mirror migrations and cultures in prehistoric Europe - a population genomic perspective

Genomic information from ancient human remains is beginning to show its full potential for learning about human prehistory. We review the last few years' dramatic finds about European prehistory based on genomic data from humans that lived many millennia ago and relate it to modern-day patterns of genomic variation. The early times, the Upper Palaeolithic, appears to contain several population turn-overs followed by more stable populations after the Last Glacial Maximum and during the Mesolithic. Some 11,000 years ago the migrations driving the Neolithic transition start from around Anatolia and reach the north and the west of Europe millennia later followed by major migrations during the Bronze age. These findings show that culture and lifestyle were major determinants of genomic differentiation and similarity in pre-historic Europe rather than geography as is the case today.

Evolutionary Biology↗

bioRxiv2016

Perpendicular axes of incipient speciation generated by mitochondrial introgression

Differential introgression of mitochondrial versus nuclear DNA generates discordant patterns of geographic variation and can promote speciation. We examined a potential case of mitochondrial introgression leading to two perpendicular axes of differentiation. The Eastern Yellow Robin, a widespread Australian bird, shows a deep mitochondrial split that is perpendicular to north-south nuclear DNA and plumage colour differentiation. We proposed a scenario to explain this pattern: (1) the two nuclear and mitochondrial genomes differentiated in concert during north-south population divergence; (2) later, their histories disconnected after two mitochondrial introgression events resulting in a deep mitochondrial split perpendicular to the nuclear DNA structure. We tested this scenario by coalescent modelling of ten mitochondrial genes and 400 nuclear DNA loci. Initial mitochondrial and nuclear genome divergences were estimated to have occurred in the early Pleistocene, consistent with the proposed scenario. Subsequent climatic transitions may have driven later mitochondrial introgression. We reject neutral introgression and consider evidence consistent with adaptive mitochondrial introgression and selection against incompatible mitochondrial-nuclear combinations. This likely generated an axis of incipient speciation associated with mitochondrial differentiation in the face of nuclear gene flow, perpendicular to the initial north-south axis of incipient speciation (reflected in nuclear differentiation and colour variation).

Evolutionary Biology↗

bioRxiv2016

Selective constraints on coding sequences of nervous system genes are a major determinant of duplicate gene retention in vertebrates

The evolutionary history of vertebrates is marked by three ancient whole-genome duplications: two successive rounds in the ancestor of vertebrates, and a third one specific to teleost fishes. Biased loss of most duplicates enriched the genome for specific genes, such as slow evolving genes, but this selective retention process is not well understood. To understand what drives the long-term preservation of duplicate genes, we characterized duplicated genes in terms of their expression patterns. We used a new method of expression enrichment analysis, TopAnat, applied to in situ hybridization data from thousands of genes from zebrafish and mouse. We showed that the presence of expression in the nervous system is a good predictor of a higher rate of retention of duplicate genes after whole-genome duplication. Further analyses suggest that purifying selection against the toxic effects of misfolded or misinteracting proteins, which is particularly strong in non-renewing neural tissues, likely constrains the evolution of coding sequences of nervous system genes, leading indirectly to the preservation of duplicate genes after whole-genome duplication. Whole-genome duplications thus greatly contributed to the expansion of the toolkit of genes available for the evolution of profound novelties of the nervous system at the base of the vertebrate radiation.

Evolutionary Biology↗

bioRxiv2016

Selection on heterozygosity drives adaptation in intra- and interspecific hybrids

Hybridization is often considered maladaptive, but sometimes hybrids can invade new ecological niches and adapt to novel or stressful environments better than their parents. However, the genomic changes that occur following hybridization and facilitate genome resolution and/or adaptation are not well understood. Here, we address these questions using experimental evolution of de novo interspecific hybrid yeast Saccharomyces cerevisiae x Saccharomyces uvarum and their parentals. We evolved these strains in nutrient limited conditions for hundreds of generations and sequenced the resulting cultures to identify genomic changes. Analysis of 16 hybrid clones and 16 parental clones identified numerous point mutations, copy number changes, and loss of heterozygosity events, including a number of nuclear-mitochondrial mutations and species biased amplification of nutrient transporters. We focused on a particularly interesting example, in which we saw repeated loss of heterozygosity at the high affinity phosphate transporter gene PHO84 in both intra- and interspecific hybrids. Using allele replacement methods, we tested the fitness of different alleles in hybrid and S. cerevisiae strain backgrounds and found that the loss of heterozygosity is indeed the result of selection on one allele over the other in both S. cerevisiae and the hybrids. This illuminates an example where hybrid genome resolution is driven by positive selection on existing heterozygosity, and generally demonstrates that outcrossing need not be frequent to have long lasting impacts on adaptation.

Evolutionary Biology↗