bioRxiv Science⌕ Search

Biology subjects

Stephan, W.

Publications and source records attributed to Stephan, W..

6 recordsLinked to original sources

Large-scale analyses reveal the contribution of adaptive evolution in pathogenic and non-pathogenic fungal species

Genome studies of fungal pathogens have presented evidence for exceptionally high rates of evolution. It has been proposed that rapid adaptation is a hallmark of pathogen evolution that facilitates the invasion of new host niches and the overcoming of intervention strategies such as fungicide applications and drug treatments. To which extent high levels of genetic variation within and between species correlate with adaptive protein evolution in fungi more generally has so far not been explored. In this study, we addressed the contribution of adaptive evolution relative to genetic drift in 20 fungal species, hereby exploring genetic variation in 2,478 fungal genomes. We reannotated positions of protein-coding genes to obtain a high-quality dataset of 234,427 full-length core gene and 25,612 accessory gene alignments. We applied an extension of the McDonald-Kreitman test that models the distributions of fitness effects to infer the rate of adaptive ({omega}A) and non-adaptive ({omega}NA) non-synonymous substitutions in protein-coding genes. To explore the relevance of recombination on local adaptation rates, we inferred the population genomic recombination rate for all 20 species. Our analyses reveal extensive variation in rates of adaptation and show that high rates of adaptation are not a hallmark of a pathogenic lifestyle. Up to 83% of non-synonymous substitutions are adaptive in the species Parastagonospora nodorum. However, non-synonymous substitutions in other species, including the prominent rice-infecting pathogen Magnaporthe oryzae, are predominantly non-adaptive (neutral or slightly deleterious). Correlating adaptation measures with effective population size and recombination rate, we show that effective population size is a primary determinant of adaptive evolution in fungi. At the genome scale, recombination rate variation explains variation in both {omega}A and {omega}NA. Finally, we demonstrate the robustness of our estimates using simulations. We underline the value of population genetic principles in studies of fungal evolution, and we highlight the importance of demographic processes in adaptive evolution of pathogenic and non-pathogenic species.

evolutionary biology↗

Statistical inference in population genomics

The field of population genomics has grown rapidly in response to the recent advent of affordable, large-scale sequencing technologies. As opposed to the situation during the majority of the 20th century, in which the development of theoretical and statistical population-genetic insights out-paced the generation of data to which they could be applied, genomic data are now being produced at a far greater rate than they can be meaningfully analyzed and interpreted. With this wealth of data has come a tendency to focus on fitting specific (and often rather idiosyncratic) models to data, at the expense of a careful exploration of the range of possible underlying evolutionary processes. For example, the approach of directly investigating models of adaptive evolution in each newly sequenced population or species often neglects the fact that a thorough characterization of ubiquitous non-adaptive processes is a prerequisite for accurate inference. We here describe the perils of these tendencies, present our consensus views on current best practices in population genomic data analysis, and highlight areas of statistical inference and theory that are in need of further attention. Thereby, we argue for the importance of defining a biologically relevant baseline model tuned to the details of each new analysis, of skepticism and scrutiny in interpreting model-fitting results, and of carefully defining addressable hypotheses and underlying uncertainties.

evolutionary biology↗

The de novo reference genome and transcriptome assemblies of the wild tomato species Solanum chilense

BackgroundWild tomato species, like Solanum chilense, are important germplasm resources for enhanced biotic and abiotic stress resistance in tomato breeding. In addition, S. chilense serves as a model system to study adaptation of plants to drought and to investigate the evolution of seed banks. However to date, the absence of a well annotated reference genome in this compulsory outcrossing, very diverse species limits in-depth studies on the genes involved.\n\nFindingsWe generated [~]134 Gb of DNA and 157 Gb of RNA sequence data of S chilense, which yielded a draft genome with an estimated length of 914 Mb in total encoding 25,885 high-confidence (hc) predicted gene models, which show homology to known protein-coding genes of other tomato species. Approximately 71% (18,290) of the hc gene models are additionally supported by RNA-seq data derived from leaf tissue samples. A benchmarking with Universal Single-Copy Orthologs (BUSCO) analysis of predicted gene models retrieved 93.3% BUSCO genes, which is in the current range of high-quality genomes for non-inbred plants. To further verify the genome annotation completeness and accuracy, we manually inspected the NLR resistance gene family and assessed its assembly quality. We revealed the existence of unique gene families of NLRs to S. chilense. Comparative genomics analyses of S. chilense, cultivated tomato S. lycopersicum and its wild relative S. pennellii revealed similar levels of highly syntenic gene clusters between the three species.\n\nConclusionsWe generated the first genome and transcriptome sequence assembly for the wild tomato species Solanum chilense and demonstrated its value in comparative genomics analyses. We make these genomes available for the scientific community as an important resource for studies on adaptation to biotic and abiotic stress in Solanaceae, on evolution of self-incompatibility, and for tomato breeding.

plant biology↗

Neutral genomic signatures of host-parasite coevolution.

Coevolution is a selective process of reciprocal adaptation between antagonistic or mutualistic symbionts and their host. Classic population genetics theory predicts the signatures of selection at the interacting loci but not the neutral genome-wide polymorphism patterns. We here build a coevolutionary model with cyclic changes in the host and parasite population sizes. Using an analytical framework, we investigate if and when these population size changes can be observed in the neutral site frequency spectrum of the host and parasite full genome data. We show that polymorphism data sampled over time can capture the changes in the population size of the parasite but not of the host because genetic drift and mutations occur on different time scales in the coevolving species. This is due to the small parasite population size at the onset of the coevolutionary history subsequently undergoing a series of strong bottlenecks. We also show that tracking coevolutionary cycles is more likely for a small amount of parasite per host and for multiple parasite generations per host generation. Our results demonstrate that time sampling of host and parasite full genome data are crucial to infer the co-demographic history of interacting species.

evolutionary biology↗

Early split between African and European populations of Drosophila melanogaster

Natural populations of the fruit fly Drosophila melanogaster have been used extensively as a model system to investigate the effect of neutral and selective processes on genetic variation. The species expanded outside its Afrotropical ancestral range during the last glacial period and numerous studies have focused on identifying molecular adaptations associated with the colonization of northern habitats. The sequencing of many genomes from African and non-African natural populations has facilitated the analysis of the interplay between adaptive and demographic processes. However, most of the non-African sequenced material has been sampled from American and Australian populations that have been introduced within the last hundred years following recent human dispersal and are also affected by recent genetic admixture with African populations. Northern European populations, at the contrary, are expected to be older and less affected by complex admixture patterns and are therefore more appropriate to investigate neutral and adaptive processes. Here we present a new dataset consisting of 14 fully sequenced haploid genomes sampled from a natural population in Ume[a], Sweden. We co-analyzed this new data with an African population to compare the likelihood of several competing demographic scenarios for European and African populations. We show that allowing for gene flow between populations in neutral demographic models leads to a significantly better fit to the data and strongly affects estimates of the divergence time and of the size of the bottleneck in the European population. Our results indicate that the time of divergence between cosmopolitan and ancestral populations is 30,000 years older than reported by previous studies.

evolutionary biology↗

A small subset of NLR genes drives local adaptation to pathogens in wild tomato

O_LINucleotide binding site, Leucine-rich repeat Receptors (NLRs), are canonical resistance (R) genes in plants, fungi and animals, functioning as central (helper) and peripheral (sensor) genes in a signalling network. We investigate NLR evolution during the colonisation of novel habitats in a model tomato species, Solanum chilense.\nC_LIO_LIWe used R-gene enrichment sequencing (RENSeq) to obtain polymorphism data at NLRs of 140 plants sampled across 14 populations covering the whole species range. We inferred the past demographic history of habitat colonisation by resequencing whole genomes from three S. chilense plants from three key populations, and performing Approximate Bayesian Computation using data from the 14 populations.\nC_LIO_LIUsing these parameters we simulated the genetic differentiation statistics distribution expected under neutral NLR evolution, and identified small subsets of outlier NLRs exhibiting signatures of selection across populations.\nC_LIO_LINLRs under selection between habitats are more often helper genes, while those showing signatures of adaptation in single populations are more often sensor-NLRs. Thus, centrality in the NLR network does not constrain NLR evolvability, and new mutations in central genes in the network are key for R gene adaptation during colonisation of different habitats.\nC_LI

evolutionary biology↗