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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↗

bioRxiv2016

Recent advances in the study of fine-scale population structure in humans

Empowered by modern genotyping and large samples, population structure can be accurately described and quantified even when it only explains a fraction of a percent of total genetic variance. This is especially relevant and interesting for humans, where fine-scale population structure can both confound disease-mapping studies and reveal the history of migration and divergence that shaped our species diversity. Here we review notable recent advances in the detection, use, and understanding of population structure. Our work addresses multiple areas where substantial progress is being made: improved statistics and models for better capturing differentiation, admixture, and the spatial distribution of variation; computational speed-ups that allow methods to scale to modern data; and advances in haplotypic modeling that have wide ranging consequences for the analysis of population structure. We conclude by outlining four important open challenges: The limitations of discrete population models, uncertainty in individual origins, the incorporation of both fine-scale structure and ancient DNA in parametric models, and the development of efficient computational tools, particularly for haplotype-based methods.

Evolutionary Biology↗

bioRxiv2016

High throughput sequencing of multiple amplicons for barcoding and integrative taxonomy

Until now, the potential of NGS has been seldom realised for the construction of barcode reference libraries. Using a two-step PCR approach and MiSeq sequencing, we tested a cost-effective method and developed a custom workflow to simultaneously sequence multiple markers (COI, Cytb and EF, altogether 2kb) from hundreds of specimens. Interestingly, primers and PCR conditions used for Sanger sequencing did not require optimisation to construct MiSeq library. After completion of quality controls, 87% of the species and 76% of the specimens had valid sequences for the three markers. Nine specimens (3%) exhibited two divergent (up to 10%) sequence clusters. In 95% of the species, MiSeq and Sanger sequences obtained from the same samplings were similar. For the remaining 5%, species were paraphyletic or the sequences clustered into two divergent groups (>7%) on the final trees (Sanger + MiSeq). These problematic cases are difficult to explain but may represent coding NUMTS or heteroplasms. These results highlight the importance of performing quality control steps, working with expert taxonomists and using more than one marker for DNA-taxonomy or species diversity assessment. The power and simplicity of this method appears promising to build on existing experience, tools and resources while taking advantage of NGS.

Evolutionary Biology↗

bioRxiv2016

Fossils matter: improved estimates of divergence times in Pinus reveal older diversification

BackgroundThe taxonomy of the genus Pinus is widely accepted and a well-resolved phylogeny based on entire plastome sequences exists. However, there is a large discrepancy in estimated divergence times of major pine clades among existing studies mainly due to differences in fossil placement and dating methods used. We currently lack a dated molecular pine phylogeny that makes full usage of the rich fossil record in pines. This study is the first to estimate the divergence dates of pines based on a large number of fossils (21) evenly distributed across all major clades in combination with applying the most novel dating method.\n\nResultsWe present a range of molecular phylogenetic trees of Pinus generated within a Bayesian framework using both the novel fossilized birth-death and the traditional node dating method with different fossil sets. We find the origin of pines likely to be up to 30 Myr older (Early Cretaceous) than inferred in most previous studies (Late Cretaceous) and propose generally older divergence times for major clades within Pinus than previously thought. Our age estimates vary significantly between the different dating approaches but the results generally agree on older divergence times. We present a revised list of 21 fossils that are suitable to use in dating or comparative analyses of pines.\n\nConclusionsAn accurate timescale for the divergence times in pines is essential if we are to link diversification processes and functional adaptation of this genus to geological events or to changing climates. Next to older divergence times in Pinus, our results indicate that node age estimates in pines depend on dating approaches and fossil sets used due to different inherent characteristics of dating approaches. Our set of dated phylogenetic trees of pines presented herein provide the basis to account for uncertainties in age estimations when applying comparative phylogenetic methods, which will improve our understanding of the evolutionary and ecological history in pines.

Evolutionary Biology↗

bioRxiv2016

Range stability predicts lineage persistence in a morphologically cryptic ground squirrel species complex

The processes responsible for patterns of cytonuclear discordance remain unclear. Here, we employ an exon capture dataset, demographic methods, and species distribution modeling to elucidate the impact of historical demography on patterns of genealogical concordance and discordance in ground squirrel lineages from the Otospermophilus beecheyi species complex. Previous studies in O. beecheyi revealed three morphologically cryptic and highly divergent mitochondrial DNA (mtDNA) lineages (named the Northern, Central, and Southern lineages based on geography) with only the Northern lineage exhibiting concordant divergence in nuclear markers. We show that these mtDNA lineages likely formed in allopatry during the Pleistocene, but responded differentially to climatic changes that occurred since the last interglacial ([~]120,000 years ago). We find that the Northern lineage maintained a stable range throughout this period, correlating with genetic distinctiveness among all genetic markers and low migration rates between the other lineages. In contrast, our results support a scenario where the Southern lineage expanded from Baja California Sur during the Late Pleistocene and hybridized with the Central lineage, eventually driving the Central lineage to extinction. While high intraspecific gene flow among newly colonized populations eroded significant signals of Central ancestry from autosomal markers, male sex-biased dispersal in this system preserved signals of this past hybridization and introgression event in matrilineal-biased X-chromosome and mtDNA markers. Our results highlight the importance of range stability in maintaining the persistence of phylogeographic lineages, whereas unstable range dynamics can increase the tendency for lineages to interact and collapse upon secondary contact.

Evolutionary Biology↗

bioRxiv2016

Comparative genomics and metagenomics analyses of endangered Père David’s deer (Elaphurus davidianus) provide insights into population recovery

The milu (Pere Davids deer, Elaphurus davidianus) has become a classic example of how highly endangered animal species can be rescued. However, the mechanisms that underpinned this population recovery remain largely unknown. As part of this study, we sequenced and analyzed whole genomes from multiple captive individuals. Following this analysis, we observed that the milu experienced a prolonged population decline over the last 200,000 years, which led to an elongated history of inbreeding. This protracted inbreeding history facilitated the purging of deleterious recessive alleles, thereby ameliorating associated threats to population viability. Because of this phenomenon, milu are now believed to be less susceptible to future inbreeding depression occurrences. SNP distribution patterns confirmed inbreeding history and also indicated sign of increased and increasing diversity in the recovered milu population. A selective sweep analysis identified two outlier genes (CTSR2 and GSG1) that were related to male fertility. Furthermore, we observed strong signatures of selection pertaining to the host immune system, including six genes (SERPINE1, PDIA3, CD302, IGLL1, VPREB3, and CD53 antigen), which are likely to strengthen resistance to pathogens. We also identified several adaptive features including the over-representation of gene families encoding for olfactory receptor activity, a high selection pressure pertaining to DNA repair and host immunity, and tolerance to high-salt swamp diets. Moreover, glycan biosynthesis, lipid metabolism, and cofactor and vitamin metabolism were all significantly enriched in the gut microbiomes of milu. We speculate that these characteristics play an important role in milu energy metabolism, immunity, development, and health. In conclusion, our findings provide a unique insight into animal population recovery strategies.

Evolutionary Biology↗

bioRxiv2016

The impact of recent population history on the deleterious mutation load in humans and close evolutionary relatives

Over the past decade, there has been both great interest and confusion about whether recent demographic events--notably the Out-of-Africa-bottleneck and recent population growth--have led to differences in mutation load among human populations. The confusion can be traced to the use of different summary statistics to measure load, which lead to apparently conflicting results. We argue, however, that when statistics more directly related to load are used, the results of different studies and data sets consistently reveal little or no difference in the load of non-synonymous mutations among human populations. Theory helps to understand why no such differences are seen, as well as to predict in what settings they are to be expected. In particular, as predicted by modeling, there is evidence for changes in the load of recessive loss of function mutations in founder and inbred human populations. Also as predicted, eastern subspecies of gorilla, Neanderthals and Denisovans, who are thought to have undergone reductions in population sizes that exceed the human Out-of-Africa bottleneck in duration and severity, show evidence for increased load of non-synonymous mutations (relative to western subspecies of gorillas and modern humans, respectively). A coherent picture is thus starting to emerge about the effects of demographic history on the mutation load in populations of humans and close evolutionary relatives.

Evolutionary Biology↗

bioRxiv2016

Molecular adaptation in Rubisco: discriminating between convergent evolution and positive selection using mechanistic and classical codon models

Rubisco (Ribulose-1, 5-biphosphate carboxylase/oxygenase) is the most important enzyme on earth, catalyzing the first step of CO2 fixation in photosynthesis. Its molecular adaptation to C4 photosynthetic pathway has attracted a lot of attention. C4 plants, which comprise less than 5% of land plants, have evolved more efficient photosynthesis compared to C3 plants. Interestingly, a large number of independent transitions from C3 to C4 phenotype have occurred. Each time, the Rubisco enzyme has been subject to similar changes in selective pressure, thus providing an excellent model for convergent evolution at the molecular level. Molecular adaptation is often identified with positive selection and is typically characterized by an elevated ratio of non-synonymous over synonymous substitution rates (dN/dS). However, convergent adaptation is expected to leave a different molecular signature, taking the form of repeated transitions toward identical or similar amino acids.\n\nHere, we use a previously introduced codon-based differential selection model to detect and quantify consistent patterns of convergent adaptation in Rubisco in Amaranthaceae. We further contrast the results thus obtained with those obtained under classical codon models based on the estimation of dN/dS. We find that the two classes of models tend to select distinct, although overlapping, sets of positions. This discrepancy in the results illustrates the conceptual difference between these models, while emphasizing the need to better discriminate between qualitatively different selective regimes, by using a broader class of codon models than those currently considered in molecular evolutionary studies.

Evolutionary Biology↗