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Search indexed bioRxiv preprints in genomics, neuroscience, cell biology and bioinformatics. Read source abstracts and check manuscript versions; preprints are not peer reviewed.

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bioRxiv2015

Successful asexual lineages of the Irish potato Famine pathogen are triploid

The oomycete Phytophthora infestans was the causal agent of the Irish Great Famine and is a recurring threat to global food security1. The pathogen can reproduce both sexually and asexually and has a potential to adapt both abiotic and biotic environment2. Although in many regions the A1 and A2 mating types coexist, the far majority of isolates belong to few clonal, asexual lineages3. As other oomycetes, P. infestans is thought to be diploid during the vegetative phase of its life cycle3, but it was observed that trisomy correlated with virulence and mating type locus4 and that polyploidy can occur in some isolates5,6. It remains unknown about the frequency of polyploidy occurrence in nature and the relationship between ploidy level and sexuality. Here we discovered that the sexuality of P. infestans isolates correlates with ploidy by comparison of microsatellite fingerprinting, genome-wide polymorphism, DNA quantity, and chromosome numbers. The sexual progeny of P. infestans in nature are diploid, whereas the asexual lineages are mostly triploids, including successful clonal lineages US-1 and 13_A2. This study reveals polyploidization as an extra evolutionary risk to this notorious plant destroyer.

Evolutionary Biology↗
bioRxiv2015

Sex-dependent dominance at a single locus maintains variation in age at maturity in Atlantic salmon

Males and females share many traits that have a common genetic basis, however selection on these traits often differs between the sexes leading to sexual conflict1,2. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict2-6. Yet, despite intense theoretical and empirical interest, the specific genetic loci behind sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution4,7,8 and the maintenance of genetic diversity8,9. Here, we identify a large effect locus controlling age at maturity in 57 salmon populations, an important fitness trait in which selection favours earlier maturation in males than females10, and show it is a clear example of sex dependent dominance reducing intralocus sexual conflict and maintaining adaptive variation in wild populations. Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39.4% of phenotypic variation, an unexpectedly high effect size for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection11-13. Our results provide the first empirical example of dominance reversal permitting greater optimisation of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We further anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.

Evolutionary Biology↗
bioRxiv2015

Genome divergence and gene flow between Drosophila simulans and D. mauritiana

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that, rather than contributing to interspecific divergence, a known drive element has recently migrated between species, caused a strong reduction in local divergence, and undermined the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

Evolutionary Biology↗
bioRxiv2015

A resurrection experiment finds evidence of both reduced genetic diversity and potential adaptive evolution in the agricultural weed Ipomoea purpurea

Despite the negative economic and ecological impact of weeds, relatively little is known about the evolutionary mechanisms that influence their persistence in agricultural fields. Here, we use a resurrection ecology approach and compare the genetic and phenotypic divergence of temporally sampled seed progenies of Ipomoeapurpurea, an agricultural weed that is resistant to glyphosate, the most widely used herbicide in current-day agriculture. We found striking reductions in allelic diversity between cohorts sampled nine years apart (2003 vs 2012), suggesting that populations of this species sampled from agricultural fields have experienced genetic bottleneck events that have led to lower neutral genetic diversity. Heterozygosity excess tests indicate that this bottleneck may have occurred prior to 2003. Further, a greenhouse assay of individuals sampled from the field as seed found that populations of this species, on average, exhibited modest increases in herbicide resistance over time. Our results show that populations of this noxious weed, capable of adapting to strong selection imparted by herbicide application, may lose genetic variation as a result of this or other environmental factors. We likely uncovered only modest increases in resistance between sampling cohorts due to a strong and previously identified fitness cost of resistance in this species, along with the potential that non-resistant migrants germinate from the seed bank.

Evolutionary Biology↗
bioRxiv2015

A simple approach for maximizing the overlap of phylogenetic and comparative data

O_LIBiologists are increasingly using curated, public data sets to conduct phylogenetic comparative analyses. Unfortunately, there is often a mismatch between species for which there is phylogenetic data and those for which other data is available. As a result, researchers are commonly forced to either drop species from analyses entirely or else impute the missing data.\nC_LIO_LIHere we outline a simple solution to increase the overlap while avoiding potential the biases introduced by imputing data. If some external topological or taxonomic information is available, this can be used to maximize the overlap between the data and the phylogeny. We develop an algorithm that replaces a species lacking data with a species that has data. This swap can be made because for those two species, all phylogenetic relationships are exactly equivalent.\nC_LIO_LIWe have implemented our method in a new R package phyndr, which will allow researchers to apply our algorithm to empirical data sets. It is relatively efficient such that taxon swaps can be quickly computed, even for large trees. To facilitate the use of taxonomic knowledge we created a separate data package taxonlookup; it contains a curated, versioned taxonomic lookup for land plants and is interoperable with phyndr.\nC_LIO_LIEmerging online databases and statistical advances are making it possible for researchers to investigate evolutionary questions at unprecedented scales. However, in this effort species mismatch among data sources will increasingly be a problem; evolutionary informatics tools, such as phyndr and taxonlookup, can help alleviate this issue.\nC_LI

Evolutionary Biology↗
bioRxiv2015

Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations

Urbanization results in pervasive habitat fragmentation and reduces standing genetic variation through bottlenecks and drift. Loss of genome-wide variation may ultimately reduce the evolutionary potential of animal populations experiencing rapidly changing conditions. In this study, we examined genome-wide variation among 23 white-footed mouse (Peromyscus leucopus) populations sampled along an urbanization gradient in the New York City metropolitan area. Genome-wide variation was estimated as a proxy for evolutionary potential using more than 10,000 SNP markers generated by ddRAD-Seq. We found that genome-wide variation is inversely related to urbanization as measured by percent impervious surface cover, and to a lesser extent, human population density. We also report that urbanization results in enhanced genome-wide differentiation between populations in cities. There was no pattern of isolation by distance among these populations, but an isolation by resistance model based on impervious surface significantly explained patterns of genetic differentiation. Isolation by environment modeling also indicated that urban populations deviate much more strongly from global allele frequencies than suburban or rural populations. This study is the first to examine loss of genome-wide SNP variation along an urban-to-rural gradient and quantify urbanization as a driver of population genomic patterns.

Evolutionary Biology↗
bioRxiv2015

The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals

The parthenogenetic all-female marbled crayfish is a novel research model and potent invader of freshwater ecosystems. It is a triploid descendant of the sexually reproducing slough crayfish, Procambarus fallax, but its taxonomic status has remained unsettled. By crossbreeding experiments and parentage analysis we show here that marbled crayfish and P. fallax are reproductively separated. Both crayfish copulate readily, suggesting that the reproductive barrier is set at the cytogenetic rather than the behavioural level. Analysis of complete mitochondrial genomes of marbled crayfish from laboratory lineages and wild populations demonstrates genetic identity and indicates a single origin. Flow cytometric comparison of DNA contents of haemocytes and analysis of nuclear microsatellite loci confirm triploidy and suggest autopolyploidization as its cause. Global DNA methylation is significantly reduced in marbled crayfish implying the involvement of molecular epigenetic mechanisms in its origination. Morphologically, both crayfish are very similar but growth and fecundity are considerably larger in marbled crayfish, making it a different animal with superior fitness. These data and the high probability of a divergent future evolution of the marbled crayfish and P. fallax clusters suggest that marbled crayfish should be considered as an independent asexual species. Our findings also establish the P. fallax-marbled crayfish pair as a novel paradigm for rare chromosomal speciation by autopolyploidy and parthenogenesis in animals and for saltational evolution in general.

Evolutionary Biology↗
bioRxiv2015

Phylogeographic Inference Using Approximate Likelihoods

The demographic history of most species is complex, with multiple evolutionary processes combining to shape the observed patterns of genetic diversity. To infer this history, the discipline of phylogeography has (to date) used models that simplify the historical demography of the focal organism, for example by assuming or ignoring ongoing gene flow between populations or by requiring a priori specification of divergence history. Since no single model incorporates every possible evolutionary process, researchers rely on intuition to choose the models that they use to analyze their data. Here, we develop an approach to circumvent this reliance on intuition. PHRAPL allows users to calculate the probability of a large number of demographic histories given their data, enabling them to identify the optimal model and produce accurate parameter estimates for a given system. Using PHRAPL, we reanalyze data from 19 recent phylogeographic investigations. Results indicate that the optimal models for most datasets parameterize both gene flow and population divergence, and suggest that species tree methods (which do not consider gene flow) are overly simplistic for most phylogeographic systems. These results highlight the importance of phylogeographic model selection, and reinforce the role of phylogeography as a bridge between population genetics and phylogenetics.

Evolutionary Biology↗
bioRxiv2015

Fitness-valley crossing with generalized parent-offspring transmission

Simple and ubiquitous gene interactions create rugged fitness landscapes composed of coadapted gene complexes separated by "valleys" of low fitness. Crossing such fitness valleys allows a population to escape suboptimal local fitness peaks to become better adapted. This is the premise of Sewall Wright's shifting balance process. Here we generalize the theory of fitness-valley crossing in the two-locus, biallelic case by allowing bias in parent-offspring transmission. This generalization extends the existing mathematical framework to genetic systems with segregation distortion and uniparental inheritance. Our results are also flexible enough to provide insight into shifts between alternate stable states in cultural systems with "transmission valleys". Using a semi-deterministic analysis and a stochastic diffusion approximation, we focus on the limiting step in valley crossing: the first appearance of the genotype on the new fitness peak whose lineage will eventually fix. We then apply our results to specific cases of segregation distortion, uniparental inheritance, and cultural transmission. Segregation distortion favouring mutant alleles facilitates crossing most when recombination and mutation are rare, i.e., scenarios where crossing is otherwise unlikely. Interactions with more mutable genes (e.g., uniparental inherited cytoplasmic elements) substantially reduce crossing times. Despite component traits being passed on poorly in the previous cultural background, small advantages in the transmission of a new combination of cultural traits can greatly facilitate a cultural transition. While peak shifts are unlikely under many of the common assumptions of population genetic theory, relaxing some of these assumptions can promote fitness-valley crossing.

Evolutionary Biology↗
bioRxiv2015

Low base-substitution mutation rate in the germline genome of ciliate Tetrahymena thermophila

Mutation is the ultimate source of all genetic variation and is, therefore, central to evolutionary change. Previous work on Paramecium tetraurelia found an unusually low germline base-substitution mutation rate in this ciliate. Here, we tested the generality of this result among ciliates using Tetrahymena thermophila. We sequenced the genomes of 10 lines of T. thermophila that had each undergone approximately 1,000 generations of mutation accumulation (MA). We applied an existing mutation-calling pipeline and developed a new probabilistic mutation detection approach that directly models the design of an MA experiment and accommodates the noise introduced by mismapped reads. Our probabilistic mutation-calling method provides a straightforward way of estimating the number of sites at which a mutation could have been called if one was present, providing the denominator for our mutation rate calculations. From these methods, we find that T. thermophila has a germline base-substitution mutation rate of 7.61 x 10-12 per site, per cell division, which is consistent with the low base-substitution mutation rate in P. tetraurelia. Over the course of the evolution experiment, genomic exclusion lines derived from the MA lines experienced a fitness decline that cannot be accounted for by germline base-substitution mutations alone, suggesting that other genetic or epigenetic factors must be involved. Because selection can only operate to reduce mutation rates based upon the \"visible\" mutational load, asexual reproduction with a transcriptionally silent germline may allow ciliates to evolve extremely low germline mutation rates.

Evolutionary Biology↗
bioRxiv2015

The site-frequency spectrum associated with Xi-coalescents

We give recursions for the expected site-frequency spectrum associated with so-called Xi-coalescents, that is exchangeable coalescents which admit simultaneous multiple mergers of ancestral lineages. Xi-coalescents arise, for example, in association with population models of skewed offspring distributions with diploidy, recurrent advantageous mutations, or strong bottlenecks. In contrast, the simpler Lambda-coalescents admit multiple mergers of lineages, but at most one such merger each time. Xi-coalescents, as well as Lambda-coalescents, can predict an excess of singletons, compared to the Kingman coalescent. We compare estimates of coalescent parameters when Xi-coalescents are applied to data generated by Lambda-coalescents, and vice versa. In general, Xi-coalescents predict fewer singletons than corresponding Lambda-coalescents, but a higher count of mutations of size larger than singletons. We fit examples of Xi-coalescents to unfolded site-frequency spectra obtained for autosomal loci of the diploid Atlantic cod, and obtain different coalescent parameter estimates than obtained with corresponding Lambda-coalescents. Our results provide new inference tools, and suggest that for autosomal population genetic data from diploid or polyploid highly fecund populations who may have skewed offspring distributions, one should not apply Lambda-coalescents, but Xi-coalescents.

Evolutionary Biology↗
bioRxiv2015

Incomplete domestication of South American grain amaranth (Amaranthus caudatus) from its wild relatives

The process of domestication leads to major morphological and genetic changes, which in combination are known as domestication syndrome that differentiates crops from their wild ancestors. We characterized the genomic and phenotypic diversity of the South American grain amaranth Amaranthus caudatus, which has been cultivated for thousands of years and is one of the three native grain amaranths of South and Central America. Previously, several models of domestication were proposed including a domestication from the close relatives and putative ancestors A. hybridus or A. quitensis. To investigate the evolutionary relationship of A. caudatus and its two close relatives, we genotyped 119 amaranth accessions of the three species from the Andean region using genotyping-by-sequencing (GBS) and compared phenotypic variation in two domestication-related traits, seed size and seed color. The analysis of 9,485 SNPs revealed a strong genetic differentiation of cultivated A. caudatus from the relatives A. hybridus and A. quitensis. The two relatives did not cluster according to the species assigment but formed mixed groups according to their geographic origin in Ecuador and Peru, respectively. A. caudatus had a higher genetic diversity than its close relatives and shared a high proportion of polymorphisms with their wild relatives consistent with the absence of a strong bottleneck or a high level of recent gene flow. Genome sizes and seed sizes were not significantly different between A. caudatus and its relatives, although a genetically distinct group of A. caudatus from Bolivia had significantly larger seeds. We conclude that despite a long history of human cultivation and selection for white grain color, A. caudatus shows a weak genomic and phenotypic domestication syndrome and is an incompletely domesticated species because of weak selection or high levels of gene flow from its sympatric close undomesticated relatives that counteracted the fixation of key domestication traits.

Evolutionary Biology↗
bioRxiv2015

Extreme Mitogenomic Variation Without Cryptic Speciation in Chaetognaths

The extent of within-species genetic variation across the diversity of animal life is a fundamental but largely unexplored problem in ecology and evolution. The neutral theory of molecular evolution predicts that genetic variation scales positively with population size. However, the genetic diversity of mitochondrial DNA, a prominent marker used in DNA barcoding studies, shows very little variation across animal species. Here, we report an unprecedented case of extreme mitochondrial variation within natural populations of two species of chaetognaths (arrow worms). We determined that this diversity is composed of deep intraspecific mitochondrial lineages within single populations that could be as divergent as human and newt. This mitochondrial diversity is the highest ever reported in animals without evidence of cryptic speciation or allopatric divergence as supported by nuclear evidence. We sequenced 54 complete mitogenomes revealing gene order rearrangements between these intraspecific lineages. Such structural differences have never previously been reported within single species. We confirm that this divergence was not driven by positive selection, and conversely show that these lineages evolved under purifying selection, consistently with neutral expectations. Our findings question the generally accepted narrow range of genetic variation in animal mitochondria and argue for a reappraisal of DNA barcoding techniques. Furthermore, extreme levels of mitogenomic variation in chaetognaths challenge classical views regarding mitochondrial evolution and cytonuclear co-evolution.

Evolutionary Biology↗
bioRxiv2015

Comparing RADseq and microsatellites to infer complex phylogeographic patterns, a real data informed perspective in the Crucian carp, Carassius carassius, L.

The conservation of threatened species must be underpinned by phylogeographic knowledge in order to be effective. This need is epitomised by the freshwater fish Carassius carassius, which has recently undergone drastic declines across much of its European range. Restriction Site Associated DNA sequencing (RADseq) is being increasingly used for such phylogeographic questions, however RADseq is expensive, and limitations on sample number must be weighed against the benefit of large numbers of markers. Such tradeoffs have predominantly been addressed using simulated data. Here we compare the results generated from microsatellites and RADseq to the phylogeography of C. carassius, to add real-data-informed perspectives to this important debate. These datasets, along with data from the mitochondrial cytochrome b gene, agree on broad phylogeographic patterns; showing the existence of two previously unidentified C. carassius lineages in Europe. These lineages have been isolated for approximately 2.2-2.3 M years, and should arguably be considered as separate conservation units. RADseq recovered finer population structure and stronger patterns of IBD than microsatellites, despite including only 17.6% of samples (38% of populations and 52% of samples per population). RADseq was also used along with Approximate Bayesian Computation to show that the postglacial colonisation routes of C. carassius differ from the general patterns of freshwater fish in Europe, likely as a result of their distinctive ecology.

Evolutionary Biology↗
bioRxiv2015

Evolutionary dynamics of roX lncRNA function and genomic occupancy

Many long noncoding RNAs (lncRNAs) can regulate chromatin states, but the evolutionary origin and dynamics driving lncRNA-genome interactions are unclear. We developed an integrative strategy that identifies lncRNA orthologs in different species despite limited sequence similarity that is applicable to fly and mammalian lncRNAs. Analysis of the roX lncRNAs, which are essential for dosage compensation of the single X-chromosome in Drosophila males, revealed 47 new roX orthologs in diverse Drosophilid species across ~40 million years of evolution. Genetic rescue by roX orthologs and engineered synthetic lncRNAs showed that evolutionary maintenance of focal structural repeats mediates roX function. Genomic occupancy maps of roX RNAs in four species revealed rapid turnover of individual binding sites but conservation within nearby chromosomal neighborhoods. Many new roX binding sites evolved from DNA encoding a pre-existing RNA splicing signal, effectively linking dosage compensation to transcribed genes. Thus, evolutionary analysis illuminates the principles for the birth and death of lncRNAs and their genomic targets.

Evolutionary Biology↗
bioRxiv2015

Evolutionary quantitative genomics of Populus trichocarpa

Forest trees generally show high levels of local adaptation and efforts focusing on understanding adaptation to climate will be crucial for species survival and management.\n\nMerging quantitative genetics and population genomics, we studied the molecular basis of climate adaptation in 433 Populus trichocarpa (black cottonwood) genotypes originating across western North America. Variation in 74 field-assessed traits (growth, ecophysiology, phenology, leaf stomata, wood, and disease resistance) was investigated for signatures of selection (comparing QST-FST) using clustering of individuals by climate of origin. 29,354 SNPs were investigated employing three different outlier detection methods.\n\nNarrow-sense QST for 53% of distinct field QST traits was significantly divergent from expectations of neutrality (indicating adaptive trait variation); 2,855 SNPs showed signals of diversifying selection and of these, 118 SNPs (within 81 genes) were associated with adaptive traits (based on significant QST). Many SNPs were putatively pleiotropic for functionally uncorrelated adaptive traits, such as autumn phenology, height, and disease resistance.\n\nEvolutionary quantitative genomics in P. trichocarpa provides an enhanced understanding regarding the molecular basis of climate-driven selection in forest trees. We highlight that important loci underlying adaptive trait variation also show relationship to climate of origin.\n\nAuthor summaryComparisons between population differentiation on the basis of quantitative traits and neutral genetic markers inform about the importance of natural selection, genetic drift and gene flow for local adaptation of populations. Here, we address fundamental questions regarding the molecular basis of adaptation in undomesticated forest tree populations to past climatic environments by employing an integrative quantitative genetics and landscape genomics approach. Marker-inferred relatedness was estimated to obtain the narrow-sense estimate of population differentiation in wild populations. We analyzed an unstructured population of common garden grown Populus trichocarpa individuals to uncover different extents of variation for a suite of field traits, wood quality and pathogen resistance with temperature and precipitation. We consider our approach the most comprehensive, as it uncovers the molecular mechanisms of adaptation using multiple methods and tests. We provide a detailed outline of the required analyses for studying adaptation to the environment in a population genomics context to better understand the species potential adaptive capacity to future climatic scenarios.

Evolutionary Biology↗
bioRxiv2015

Genetic evidence challenges the native status of a threatened freshwater fish (Carassius carassius) in England

A fundamental consideration for the conservation of a species is the extent of its native range, however defining a native range is often challenging as changing environments drive shifts in species distributions over time. The crucian carp, Carassius carassius (L.) is a threatened freshwater fish native to much of Europe, however the extent of this range is ambiguous. One particularly contentious region is England, in which C. carassius is currently considered native on the basis of anecdotal evidence. Here, we use 13 microsatellite loci, population structure analyses and approximate bayesian computation (ABC), to empirically test the native status of C. carassius in England. Contrary to the current consensus, ABC yields strong support for introduced origins of C. carassius in England, with posterior distribution estimates placing their introduction in the 15th century, well after the loss of the doggerland landbridge. This result brings to light an interesting and timely debate surrounding our motivations for the conservation of species. We discuss this topic, and make arguments for the continued conservation of C. carassius in England, despite its non-native origins.

Evolutionary Biology↗
bioRxiv2015

Limits to adaptation in partially selfing species

In outcrossing populations, \"Haldanes Sieve\" states that recessive beneficial alleles are less likely to fix than dominant ones, because they are less expose to selection when rare. In contrast, selfing organisms are not subject to Haldanes Sieve and are more likely to fix recessive types than outcrossers, as selfing rapidly creates homozygotes, increasing overall selection acting on mutations. However, longer homozygous tracts in selfers also reduces the ability of recombination to create new genotypes. It is unclear how these two effects influence overall adaptation rates in partially selfing organisms. Here, we calculate the fixation probability of beneficial alleles if there is an existing selective sweep in the population. We consider both the potential loss of the second beneficial mutation if it has a weaker advantage than the first, and the possible replacement of the initial allele if the second mutant is fitter. Overall, loss of weaker adaptive alleles during a first selective sweep has a larger impact on preventing fixation of both mutations in highly selfing organisms. Furthermore, the presence of linked mutations has two opposing effects on Haldanes Sieve. First, recessive mutants are disproportionally likely to be lost in outcrossers, so it is likelier that dominant mutations will fix. Second, with elevated rates of adaptive mutation, selective interference annuls the advantage in selfing organisms of not suffering from Haldanes Sieve; outcrossing organisms are more able to fix weak beneficial mutations of any dominance value. Overall, weakened recombination effects can greatly limit adaptation in selfing organisms.

Evolutionary Biology↗