First-generation linkage map for the common frog Rana temporaria reveals sex-linkage group

The common frog (Rana temporaria) has become a model species in the fields of ecology and evolutionary biology. However, lack of genomic resources has been limiting utility of this species for detailed evolutionary genetic studies. Using a set of 107 informative microsatellite markers genotyped in a large full-sib family (800 F1 offspring), we created the first linkage map for this species. This partial map-distributed over 15 linkage groups-has a total length of 1698.8 cM. In line with the fact that males are the heterogametic sex in this species and a reduction of recombination is expected, we observed a lower recombination rate in the males (map length: 1371.5 cM) as compared with females (2089.8 cM). Furthermore, three loci previously documented to be sex-linked (that is, carrying male-specific alleles) in adults from the wild mapped to the same linkage group. The linkage map described in this study is one of the densest ones available for amphibians. The discovery of a sex linkage group in Rana temporaria, as well as other regions with strongly reduced male recombination rates, should help to uncover the genetic underpinnings of the sex-determination system in this species. As the number of linkage groups found (n=15) is quite close to the actual number of chromosomes (n=13), the map should provide a useful resource for further evolutionary, ecological and conservation genetic work in this and other closely related species.     

Coestimation of recombination,substitution and molecular adaptation rates by approximate Bayesian computation

The estimation of parameters in molecular evolution may be biased when some processes are not considered. For example, the estimation of selection at the molecular level using codon-substitution models can have an upward bias when recombination is ignored. Here we address the joint estimation of recombination, molecular adaptation and substitution rates from coding sequences using approximate Bayesian computation (ABC). We describe the implementation of a regression-based strategy for choosing subsets of summary statistics for coding data, and show that this approach can accurately infer recombination allowing for intracodon recombination breakpoints, molecular adaptation and codon substitution rates. We demonstrate that our ABC approach can outperform other analytical methods under a variety of evolutionary scenarios. We also show that although the choice of the codon-substitution model is important, our inferences are robust to a moderate degree of model misspecification. In addition, we demonstrate that our approach can accurately choose the evolutionary model that best fits the data, providing an alternative for when the use of full-likelihood methods is impracticable. Finally, we applied our ABC method to co-estimate recombination, substitution and molecular adaptation rates from 24 published human immunodeficiency virus 1 coding data sets.     

AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana

The initiation of meiotic recombination by the formation of DNA double-strand breaks (DSBs) catalysed by the Spo11 protein is strongly evolutionary conserved. In Saccharomyces cerevisiae, Spo11 requires nine other proteins for meiotic DSB formation, but, unlike Spo11, few of these proteins seem to be conserved across kingdoms. In order to investigate this recombination step in higher eukaryotes, we have isolated a new gene, AtPRD1, whose mutation affects meiosis in Arabidopsis thaliana. In Atprd1 mutants, meiotic recombination rates fall dramatically, early recombination markers (e.g., DMC1 foci) are absent, but meiosis progresses until achiasmatic univalents are formed. Besides, Atprd1 mutants suppress DSB repair defects of a large range of meiotic mutants, showing that AtPRD1 is involved in meiotic recombination and is required for meiotic DSB formation. Furthermore, we showed that AtPRD1 and AtSPO11-1 interact in a yeast two-hybrid assay, suggesting that AtPRD1 could be a partner of AtSPO11-1. Moreover, our study reveals similarity between AtPRD1 and the mammalian protein Mei1, suggesting that AtPRD1 could be a Mei1 functional homologue.     

Low Selection Pressure Aids the Evolution of Cooperative Ribozyme Mutations in Cells

Understanding the evolution of functional RNA molecules is important for our molecular understanding of biology. Here we tested experimentally how two evolutionary parameters, selection pressure and recombination, influenced the evolution of an evolving RNA population. This was done using four parallel evolution experiments that employed low or gradually increasing selection pressure, and recombination events either at the end or dispersed throughout the evolution. As model system, a trans-splicing group I intron ribozyme was evolved in Escherichia coli cells over 12 rounds of selection and amplification, including mutagenesis and recombination. The low selection pressure resulted in higher efficiency of the evolved ribozyme populations, whereas differences in recombination did not have a strong effect. Five mutations were responsible for the highest efficiency. The first mutation swept quickly through all four evolving populations, whereas the remaining four mutations accumulated later and more efficiently under low selection pressure. To determine why low selection pressure aided this evolution, all evolutionary intermediates between the wild type and the 5-mutation variant were constructed, and their activities at three different selection pressures were determined. The resulting fitness profiles showed a high cooperativity among the four late mutations, which can explain why high selection pressure led to inefficient evolution. These results show experimentally how low selection pressure can benefit the evolution of cooperative mutations in functional RNAs.     

Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species

A central aim of evolutionary genomics is to identify the relative roles that various evolutionary forces have played in generating and shaping genetic variation within and among species. Here we use whole-genome resequencing data to characterize and compare genome-wide patterns of nucleotide polymorphism, site frequency spectrum, and population-scaled recombination rates in three species of Populus: Populus tremula, P. tremuloides, and P. trichocarpa. We find that P. tremuloides has the highest level of genome-wide variation, skewed allele frequencies, and population-scaled recombination rates, whereas P. trichocarpa harbors the lowest. Our findings highlight multiple lines of evidence suggesting that natural selection, due to both purifying and positive selection, has widely shaped patterns of nucleotide polymorphism at linked neutral sites in all three species. Differences in effective population sizes and rates of recombination largely explain the disparate magnitudes and signatures of linked selection that we observe among species. The present work provides the first phylogenetic comparative study on a genome-wide scale in forest trees. This information will also improve our ability to understand how various evolutionary forces have interacted to influence genome evolution among related species.     

Evolutionary genetics: the evils of abstinence from sex

The evolutionary significance of sexual reproduction and genetic recombination is a long-standing puzzle. Some recent experiments on Drosophila show that a lack of recombination can impede adaptive evolution.     

Recombination Detection Under Evolutionary Scenarios Relevant to Functional Divergence

Recombination can negatively impact methods designed to detect divergent gene function that rely on explicit knowledge of a gene tree. However, we know little about how recombination detection methods perform under evolutionary scenarios encountered in studies of functional molecular divergence. We use simulation to evaluate false positive rates for six recombination detection methods (GENECONV, MaxChi, Chimera, RDP, GARD-SBP, GARD-MBP) under evolutionary scenarios that might increase false positives. Broadly, these scenarios address: (i) asymmetric tree topology and sequence divergence, (ii) non-stationary codon bias and selection pressure, and (iii) positive selection. We also evaluate power to detect recombination under truly recombinant history. As with previous studies, we find that power increases with sequence divergence. However, we also find that accuracy to correctly infer the number of breakpoints is extremely low. When recombination is absent, increased sequence divergence leads to increased false positives. Furthermore, one method (GARD-SBP) is sensitive to tree shape, with higher false positive rates under an asymmetric tree topology. Somewhat surprisingly, all methods are robust to the simulated heterogeneity in codon bias, shifts in selection pressure and presence of positive selection. Based on these findings, we recommend that studies of functional divergence in systems where recombination is plausible can, and should, include a pre-test for recombination. Application of all methods to the core genome of Prochlorococcus reveals a substantial lack of concordance among results. Based on analysis of both real and simulated datasets we present some guidelines for the investigation of recombination in genes that may have experienced functional divergence.     

BRC-1 acts in the inter-sister pathway of meiotic double-strand break repair

The breast and ovarian cancer susceptibility protein BRCA1 is evolutionarily conserved and functions in DNA double-strand break (DSB) repair through homologous recombination, but its role in meiosis is poorly understood. By using genetic analysis, we investigated the role of the Caenorhabditis elegans BRCA1 orthologue (brc-1) during meiotic prophase. The null mutant in the brc-1 gene is viable, fertile and shows the wild-type complement of six bivalents in most diakinetic nuclei, which is indicative of successful crossover recombination. However, brc-1 mutants show an abnormal increase in apoptosis and RAD-51 foci at pachytene that are abolished by loss of spo-11 function, suggesting a defect in meiosis rather than during premeiotic DNA replication. In genetic backgrounds in which chiasma formation is abrogated, such as him-14/MSH4 and syp-2, loss of brc-1 leads to chromosome fragmentation suggesting that brc-1 is dispensable for crossing over but essential for DSB repair through inter-sister recombination.     

Ongoing Recombination in SARS-CoV-2 Revealed through Genealogical Reconstruction

The evolutionary process of genetic recombination has the potential to rapidly change the properties of a viral pathogen, and its presence is a crucial factor to consider in the development of treatments and vaccines. It can also significantly affect the results of phylogenetic analyses and the inference of evolutionary rates. The detection of recombination from samples of sequencing data is a very challenging problem and is further complicated for SARS-CoV-2 by its relatively slow accumulation of genetic diversity. The extent to which recombination is ongoing for SARS-CoV-2 is not yet resolved. To address this, we use a parsimony-based method to reconstruct possible genealogical histories for samples of SARS-CoV-2 sequences, which enables us to pinpoint specific recombination events that could have generated the data. We propose a statistical framework for disentangling the effects of recurrent mutation from recombination in the history of a sample, and hence provide a way of estimating the probability that ongoing recombination is present. We apply this to samples of sequencing data collected in England and South Africa and find evidence of ongoing recombination.     

The molecular population genetics of HIV-1 group O

HIV-1 group O originated through cross-species transmission of SIV from chimpanzees to humans and has established a relatively low prevalence in Central Africa. Here, we infer the population genetics and epidemic history of HIV-1 group O from viral gene sequence data and evaluate the effect of variable evolutionary rates and recombination on our estimates. First, model selection tools were used to specify suitable evolutionary and coalescent models for HIV group O. Second, divergence times and population genetic parameters were estimated in a Bayesian framework using Markov chain Monte Carlo sampling, under both strict and relaxed molecular clock methods. Our results date the origin of the group O radiation to around 1920 (1890-1940), a time frame similar to that estimated for HIV-1 group M. However, group O infections, which remain almost wholly restricted to Cameroon, show a slower rate of exponential growth during the twentieth century, explaining their lower current prevalence. To explore the effect of recombination, the Bayesian framework is extended to incorporate multiple unlinked loci. Although recombination can bias estimates of the time to the most recent common ancestor, this effect does not appear to be important for HIV-1 group O. In addition, we show that evolutionary rate estimates for different HIV genes accurately reflect differential selective constraints along the HIV genome.     

Evolution of the genomic rate of recombination in mammals

Rates of recombination vary considerably between species. Despite the significance of this observation for evolutionary biology and genetics, the evolutionary mechanisms that contribute to these interspecific differences are unclear. On fine physical scales, recombination rates appear to evolve rapidly between closely related species, but the mode and tempo of recombination rate evolution on the broader scale is poorly understood. Here, we use phylogenetic comparative methods to begin to characterize the evolutionary processes underlying average genomic recombination rates in mammals. We document a strong phylogenetic effect in recombination rates, indicating that more closely related species tend to have more similar average rates of recombination. We demonstrate that this phylogenetic signal is not an artifact of errors in recombination rate estimation and show that it is robust to uncertainty in the mammalian phylogeny. Neutral evolutionary models present good fits to the data and we find no evidence for heterogeneity in the rate of evolution in recombination across the mammalian tree. These results suggest that observed interspecific variation in average genomic rates of recombination is largely attributable to the steady accumulation of neutral mutations over evolutionary time. Although single recombination hotspots may live and die on short evolutionary time scales, the strong phylogenetic signal in genomic recombination rates indicates that the pace of evolution on this scale may be considerably slower.     

Gillespie eco‐evolutionary models (GEMs) reveal the role of heritable trait variation in eco‐evolutionary dynamics

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco‐evolutionary models usually fail to track how variation changes through time. Moreover, eco‐evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco‐evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco‐evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm – an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig–MacArthur consumer–resource model. We show not only how heritable trait variation fuels trait evolution and influences eco‐evolutionary dynamics, but also how the erosion of variation through time may hinder eco‐evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco‐evolutionary and evolutionary modeling by removing long‐standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco‐evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.     

Loss/retention and evolution of NBS-encoding genes upon whole genome triplication of Brassica rapa

A genome triplication took place in the ancestor of Brassiceae species after the split of the Arabidopsis lineage. The postfragmentation and shuffling of the genome turned the ancestral hexaploid back to diploids and caused the radiation of Brassiceae species. The course of speciation was accompanied by the loss of duplicate genes and also influenced the evolution of retained genes. Of all the genes, those encoding NBS domains are typical R genes that confer resistance to invading pathogens. In this study, using the genome of Arabidopsis thaliana as a reference, we examined the loss/retention of orthologous NBS-encoding loci in the tripled Brassica rapa genome and discovered differential loss/retention frequencies. Further analysis indicated that loci of different retention ratios showed different evolutionary patterns. The loci of classesII and III (maintaining two and three syntenic loci, respectively, multi-loci) show sharper expansions by tandem duplications, have faster evolutionary rates and have more potential to be associated with novel gene functions. On the other hand, the loci that are retained at the minimal rate (keeping only one locus, class I, single locus) showed opposite patterns. Phylogenetic analysis indicated that recombination and translocation events were common among multi-loci in B. rapa, and differential evolutionary patterns between multi- and single-loci are likely the consequence of recombination. Investigations towards other gene families demonstrated different evolutionary characteristics between different gene families. The evolution of genes is more likely determined by the property of each gene family, and the whole genome triplication provided only a specific condition.     

Why mice have lost genes for COL21A1, STK17A, GPR145 and AHRI: evidence for gene deletion at evolutionary breakpoints in the rodent lineage

The mouse genome has undergone extensive chromosome rearrangement relative to the human genome since these species last shared a common ancestor. One possible consequence of these rearrangements is the deletion of genes that are located within evolutionary breakpoint regions. In this article, we present evidence of four human genes (COL21A1, STK17A, GPR145 and ARHI) that are located in regions corresponding to evolutionary breakpoints in rodents and lack mouse and rat orthologues. We propose that "evolutionary breakpoint-associated gene deletion" is an unexpected consequence of evolutionary chromosome rearrangement, and we describe a novel mechanism through which genes can be lost during evolution.     

Molecular characterization of Indian Sugarcane streak mosaic virus isolates reveals recombination and negative selection in the P1 gene

Sugarcane streak mosaic virus (SCSMV), a member of the genus Poacevirus is an important viral pathogen affecting sugarcane production in India. The P1 gene of ten Indian isolates was sequenced and compared with previously reported SCSMV isolates. Comparative sequence analysis revealed a high level of diversity in the P1 gene (83–98% nucleotide sequence identity; 87–100% amino acid sequence identity), and the Indian SCSMV isolates were found to be the most variable (up to 9% diversity at the amino acid level). Phylogenetic tree analysis showed clustering of 17 SCSMV isolates into two groups: group I included isolates from India (except SCSMV-TPT) and Pakistan, and group II consisted of isolates from Japan, Indonesia, Thailand and SCSMV-TPT. The results obtained from phylogenetic study were further supported by the different in silico analysis viz. SNPs (single nucleotide polymorphism), INDELs (insertion and deletion) and evolutionary distance analysis. A significant proportion of recombination sites were observed at the N terminal region of P1 gene. Analysis of selection pressure indicated that the P1 gene of the Indian SCSMV isolates is under strong negative or purifying selection. It is likely that recombination identified in Indian SCSMV isolates, along with strong purifying selection, enhances the speed of elimination of deleterious mutations in the P1 gene. The evolutionary processes (recombination and selection pressure) together contributed to the observed genetic diversity and population structure of Indian SCSMV isolates.     

Multidimensional Epistasis and the Transitory Advantage of Sex

Identifying and quantifying the benefits of sex and recombination is a long-standing problem in evolutionary theory. In particular, contradictory claims have been made about the existence of a benefit of recombination on high dimensional fitness landscapes in the presence of sign epistasis. Here we present a comparative numerical study of sexual and asexual evolutionary dynamics of haploids on tunably rugged model landscapes under strong selection, paying special attention to the temporal development of the evolutionary advantage of recombination and the link between population diversity and the rate of adaptation. We show that the adaptive advantage of recombination on static rugged landscapes is strictly transitory. At early times, an advantage of recombination arises through the possibility to combine individually occurring beneficial mutations, but this effect is reversed at longer times by the much more efficient trapping of recombining populations at local fitness peaks. These findings are explained by means of well-established results for a setup with only two loci. In accordance with the Red Queen hypothesis the transitory advantage can be prolonged indefinitely in fluctuating environments, and it is maximal when the environment fluctuates on the same time scale on which trapping at local optima typically occurs.     

Macrogeographical variation in the song of a widely distributed African warbler

The songs of oscine passerine birds vary on many spatial scales, reflecting the actions of diverse evolutionary pressures. Here we examine the songs of Cisticola erythrops, which effectively signal species identity across a geographical area spanning 6500 km in sub-Saharan Africa. Selection for species identification should promote stability in song traits, while sexual selection and geographical segregation should promote diversity. Cisticola erythrops share syllable types across the entire range of species and structure songs similarly, but individuals sing highly variable songs through improvisational recombination of syllables. Patterns of syllable use change gradually across the range of the species and do not show distinct breaks at subspecies boundaries. The acoustic properties of the most common syllable type also change gradually with distance. The results illustrate how songs can be simultaneously species-specific and highly variable at an individual level. At a larger level, patterns of variation indicate that cultural drift has generated song diversity through an isolation by distance mechanism.     

Bacterial recombination promotes the evolution of multi-drug-resistance in functionally diverse populations

Bacterial recombination is believed to be a major factor explaining the prevalence of multi-drug-resistance (MDR) among pathogenic bacteria. Despite extensive evidence for exchange of resistance genes from retrospective sequence analyses, experimental evidence for the evolutionary benefits of bacterial recombination is scarce. We compared the evolution of MDR between populations of Acinetobacter baylyi in which we manipulated both the recombination rate and the initial diversity of strains with resistance to single drugs. In populations lacking recombination, the initial presence of multiple strains resistant to different antibiotics inhibits the evolution of MDR. However, in populations with recombination, the inhibitory effect of standing diversity is alleviated and MDR evolves rapidly. Moreover, only the presence of DNA harbouring resistance genes promotes the evolution of resistance, ruling out other proposed benefits for recombination. Together, these results provide direct evidence for the fitness benefits of bacterial recombination and show that this occurs by mitigation of functional interference between genotypes resistant to single antibiotics. Although analogous to previously described mechanisms of clonal interference among alternative beneficial mutations, our results actually highlight a different mechanism by which interactions among co-occurring strains determine the benefits of recombination for bacterial evolution.     

Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex

Sex chromosomes often carry large nonrecombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8-Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudohomothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of ten P. anserina strains and six closely related pseudohomothallic Podospora species. Importantly, the size of the nonrecombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The nonrecombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, transspecific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but nonnull outcrossing rates in nature in these pseudohomothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.