A resurrection experiment finds evidence of both reduced genetic diversity and adaptive evolution in the agricultural weed Ipomoea purpurea
Adam Kuester, Shu-Mei Chang, Regina Baucom
doi: http://dx.doi.org/10.1101/024950

Despite the negative economic and ecological impact of weeds, relatively little is known about the evolutionary mechanisms that influence their ability to persist and thrive in agricultural fields. Here, we use a resurrection ecology approach and compare the neutral and adaptive genetic variation of temporally sampled seed progenies of Ipomoea purpurea, 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, suggesting that populations of this species sampled from agricultural fields experience genetic bottleneck and/or founder events through time. We further found that populations of this species exhibit modest increases in herbicide resistance over time and evidence that this increase was due to adaptation and not genetic drift. Our results show that even in light of reduced genetic variation, populations of this noxious weed are capable of adapting to strong selection imparted by herbicide application. 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.

Genome divergence and gene flow between Drosophila simulans and D. mauritiana
Sarah B. Kingan, Anthony J. Geneva, Jeffrey P. Vedanayagam, Daniel Garrigan
doi: http://dx.doi.org/10.1101/024711

The fruit fly Drosophila simulans and its sister species D. mauritiana are a model system for studying the genetic basis of reproductive isolation, primarily because interspecific crosses produce sterile hybrid males and their phylogenetic proximity to D. melanogaster. We present an analysis of whole-genome patterns of polymorphism and divergence that shows, on average, the genomes of the two species differ at slightly more than 1% of nucleotide positions and an estimated 40% of autosomal and 60% of X linked loci are reciprocally monophyletic. However, the analysis also identifies 21 major genomic regions, comprising ~1% of the genome, in which one species is segregating for haplotypes that are more similar to haplotypes from the other species than expected, given the levels of sequence divergence in that genomic region. This disjoint distribution of interspecific coalescence times is consistent with recent introgression between the cosmopolitan D. simulans and the island endemic D. mauritiana. We find that the putatively introgressed regions are more likely to have significantly higher rates of crossing-over and are enriched for genes with significantly slower rates of protein evolution. We also uncover instances in which genes experiencing lineage-specific positive selection closely interact with genes experiencing introgression. Finally, we find that a large introgressing region on the X chromosome has experienced a strong selective sweep in D. mauritiana and also has high levels of homozygosity in D. simulans. A detailed analysis reveals that the introgressing X chromosome haplotypes are closely associated with the presence of the MDox locus, which is the progenitor of the Winters sex-ratio meiotic drive genes. These results highlight how genetic systems that evolve rapidly in allopatry, including selfish meiotic drive elements, remain robust in natural hybrid genotypes and do not systematically promote reproductive isolation.

Life history effects on the molecular clock of autosomes and sex chromosomes
Guy Amster, Guy Sella
doi: http://dx.doi.org/10.1101/024281

One of the foundational results of molecular evolution is that the rate at which neutral substitutions accumulate on a lineage equals the rate at which mutations arise. Traits that affect rates of mutation therefore also affect the phylogenetic “molecular clock”. We consider the effects of sex-specific generation times and mutation rates in species with two sexes. In particular, we focus on the effects that the age of onset of male puberty and rates of spermatogenesis have likely had in extant hominines (i.e., human, chimpanzee and gorilla), considering a model that approximates features of the mutational process in most mammals and birds and some other vertebrates. As we show, this model helps explain and reconcile a number of seemingly puzzling observations. In hominines, it can explain the puzzlingly low X-to-autosome ratios of substitution rates and how the ratios and rates of autosomal substitutions differ among lineages. Importantly, it suggests how to translate pedigree-based estimates of human mutation rates into split times among apes, given sex-specific life histories. In so doing, it helps bridge the gap between estimates of split times of apes based on fossil and molecular evidence. Finally, considering these effects can help to reconcile recent evidence that changes in generation times should have small effects on mutation rates in humans with classic studies suggesting that they have had major effects on rates of evolution in the mammalian phylogeny.

Successful asexual lineages of the Irish potato Famine pathogen are triploidYing Li, Qian Zhou, Kun Qian, Theo van der Lee, Sanwen Huang
doi: http://dx.doi.org/10.1101/024596
The oomycete Phytophthora infestans was the causal agent of the Irish Great Famine and is a recurring threat to global food security. The pathogen can reproduce both sexually and asexually and has a potential to adapt both abiotic and biotic environment. Although in many regions the A1 and A2 mating types coexist, the far majority of isolates belong to few clonal, asexual lineages. As other oomycetes, P. infestans is thought to be diploid during the vegetative phase of its life cycle, but it was observed that trisomy correlated with virulence and mating type locus and that polyploidy can occur in some isolates. 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.

S/HIC: Robust identification of soft and hard sweeps using machine learningDaniel R Schrider, Andrew D Kern
doi: http://dx.doi.org/10.1101/024547
Detecting the targets of adaptive natural selection from whole genome sequencing data is a central problem for population genetics. However, to date most methods have shown sub-optimal performance under realistic demographic scenarios. Moreover, over the past decade there has been a renewed interest in determining the importance of selection from standing variation in adaptation of natural populations, yet very few methods for inferring this model of adaptation at the genome scale have been introduced. Here we introduce a new method, S/HIC, which uses supervised machine learning to precisely infer the location of both hard and soft selective sweeps. We show that S/HIC has unrivaled accuracy for detecting sweeps under demographic histories that are relevant to human populations, and distinguishing sweeps from linked as well as neutrally evolving regions. Moreover we show that S/HIC is uniquely robust among its competitors to model misspecification. Thus even if the true demographic model of a population differs catastrophically from that specified by the user, S/HIC still retains impressive discriminatory power. Finally we apply S/HIC to the case of resequencing data from human chromosome 18 in a European population sample and demonstrate that we can reliably recover selective sweeps that have been identified earlier using less specific and sensitive methods.

Genomic study of the Ket: a Paleo-Eskimo-related ethnic group with significant ancient North Eurasian ancestryPavel Flegontov, Piya Changmai, Anastassiya Zidkova, Maria D. Logacheva, Olga Flegontova, Mikhail S. Gelfand, Evgeny S. Gerasimov, Ekaterina V. Khrameeva, Olga P. Konovalova, Tatiana Neretina, Yuri V. Nikolsky, George Starostin, Vita V. Stepanova, Igor V. Travinsky, Martin Tříska, Petr Tříska, Tatiana V. Tatarinova
doi: http://dx.doi.org/10.1101/024554
The Kets, an ethnic group in the Yenisei River basin, Russia, are considered the last nomadic hunter-gatherers of Siberia, and Ket language has no transparent affiliation with any language family. We investigated connections between the Kets and Siberian and North American populations, with emphasis on the Mal’ta and Paleo-Eskimo ancient genomes, using original data from 46 unrelated samples of Kets and 42 samples of their neighboring ethnic groups (Uralic-speaking Nganasans, Enets, and Selkups). We genotyped over 130,000 autosomal SNPs, determined mitochondrial and Y-chromosomal haplogroups, and performed high-coverage genome sequencing of two Ket individuals. We established that the Kets belong to the cluster of Siberian populations related to Paleo-Eskimos. Unlike other members of this cluster (Nganasans, Ulchi, Yukaghirs, and Evens), Kets and closely related Selkups have a high degree of Mal’ta ancestry. Implications of these findings for the linguistic hypothesis uniting Ket and Na-Dene languages into a language macrofamily are discussed.

Genomic analysis of allele-specific expression in the mouse liverAshutosh K Pandey, Robert W Williams
doi: http://dx.doi.org/10.1101/024588

Genetic differences in gene expression contribute significantly to phenotypic diversity and differences in disease susceptibility. In fact, the great majority of causal variants highlighted by genome-wide association are in non-coding regions that modulate expression. In order to quantify the extent of allelic differences in expression, we analyzed liver transcriptomes of isogenic F1 hybrid mice. Allele-specific expression (ASE) effects are pervasive and are detected in over 50% of assayed genes. Genes with strong ASE do not differ from those with no ASE with respect to their length or promoter complexity. However, they have a higher density of sequence variants, higher functional redundancy, and lower evolutionary conservation compared to genes with no ASE. Fifty percent of genes with no ASE are categorized as house-keeping genes. In contrast, the high ASE set may be critical in phenotype canalization. There is significant overlap between genes that exhibit ASE and those that exhibit strong cis expression quantitative trait loci (cis eQTLs) identified using large genetic expression data sets. Eighty percent of genes with cis eQTLs also have strong ASE effects. Conversely, 40% of genes with ASE effects are associated with strong cis eQTLs. Cis-acting variation detected at the protein level is also detected at the transcript level, but the converse is not true. ASE is a highly sensitive and direct method to quantify cis-acting variation in gene expression and complements and extends classic cis eQTL analysis. ASE differences can be combined with coding variants to produce a key resource of functional variants for precision medicine and genome-to-phenome mapping.

The constant philopater hypothesis: a new life history invariant for dispersal evolution
António M. M. Rodrigues, Andy Gardner
doi: http://dx.doi.org/10.1101/023655
Life history invariants play a pivotal role in the study of social adaptation: they provide theoretical hypotheses that can be empirically tested, and benchmark frameworks against which new theoretical developments can be understood. Here we derive a novel invariant for dispersal evolution: the “constant philopater hypothesis” (CPH). Specifically, we find that, irrespective of variation in maternal fecundity, all mothers are favoured to produce exactly the same number of philopatric offspring, with high-fecundity mothers investing proportionally more, and low-fecundity mothers investing proportionally less, into dispersing offspring. This result holds for female and male dispersal, under haploid, diploid and haplodiploid modes of inheritance, irrespective of the sex ratio, local resource availability, and whether mother or offspring controls the latter’s dispersal propensity. We explore the implications of this result for evolutionary conflicts of interest – and the exchange and withholding of contextual information – both within and between families, and we show that the CPH is the fundamental invariant that underpins and explains a wider family of invariance relationships that emerge from the study of social evolution.

Multilocus sex determination revealed in two populations of gynodioecious wild strawberry, Fragaria vesca subsp. bracteata
Tia-Lynn Ashman, Jacob Tennessen, Rebecca Dalton, Rajanikanth Govindarajulu, Mathew Koski, Aaron Liston
doi: http://dx.doi.org/10.1101/023713

Gynodioecy, the coexistence of females and hermaphrodites, occurs in 20% of angiosperm families and often enables transitions between hermaphroditism and dioecy. Clarifying mechanisms of sex determination in gynodioecious species can thus illuminate sexual system evolution. Genetic determination of gynodioecy, however, can be complex and is not fully characterized in any wild species. We used targeted sequence capture to genetically map a novel nuclear contributor to male sterility in a self-pollinated hermaphrodite of Fragaria vesca subsp. bracteata from the southern portion of its range. To understand its interaction with another identified locus and possibly additional loci, we performed crosses within and between two populations separated by 2000 km, phenotyped the progeny and sequenced candidate markers at both sex-determining loci. The newly mapped locus contains a high density of pentatricopeptide repeat genes, a class commonly involved in restoration of fertility caused by cytoplasmic male sterility. Examination of all crosses revealed three unlinked epistatically interacting loci that determine sexual phenotype and vary in frequency between populations. Fragaria vesca subsp. bracteata represents the first wild gynodioecious species with genomic evidence of both cytoplasmic and nuclear genes in sex determination. We propose a model for the interactions between these loci and new hypotheses for the evolution of sex determining chromosomes in the subdioecious and dioecious Fragaria.

Comparing Variant Call Files for Performance Benchmarking of Next-Generation Sequencing Variant Calling Pipelines
John G. Cleary, Ross Braithwaite, Kurt Gaastra, Brian S Hilbush, Stuart Inglis, Sean A Irvine, Alan Jackson, Richard Littin, Mehul Rathod, David Ware, Justin M. Zook, Len Trigg, Francisco M. M. De La Vega
doi: http://dx.doi.org/10.1101/023754
To evaluate and compare the performance of variant calling methods and their confidence scores, comparisons between a test call set and a “gold standard” need to be carried out. Unfortunately, these comparisons are not straightforward with the current Variant Call Files (VCF), which are the standard output of most variant calling algorithms for high-throughput sequencing data. Comparisons of VCFs are often confounded by the different representations of indels, MNPs, and combinations thereof with SNVs in complex regions of the genome, resulting in misleading results. A variant caller is inherently a classification method designed to score putative variants with confidence scores that could permit controlling the rate of false positives (FP) or false negatives (FN) for a given application. Receiver operator curves (ROC) and the area under the ROC (AUC) are efficient metrics to evaluate a test call set versus a gold standard. However, in the case of VCF data this also requires a special accounting to deal with discrepant representations. We developed a novel algorithm for comparing variant call sets that deals with complex call representation discrepancies and through a dynamic programing method that minimizes false positives and negatives globally across the entire call sets for accurate performance evaluation of VCFs.