Orthologous genes identified by transcriptome sequencing in the spider genus Stegodyphus.

BACKGROUND: The evolution of sociality in spiders involves a transition from an outcrossing to a highly inbreeding mating system, a shift to a female biased sex ratio, and an increase in the reproductive skew among individuals. Taken together, these features are expected to result in a strong reduction in the effective population size. Such a decline in effective population size is expected to affect population genetic and molecular evolutionary processes, resulting in reduced genetic diversity and relaxed selective constraint across the genome. In the genus Stegodyphus, permanent sociality and regular inbreeding has evolved independently three times from periodic-social (outcrossing) ancestors. This genus is therefore an ideal model for comparative studies of the molecular evolutionary and population genetic consequences of the transition to a regularly inbreeding mating system. However, no genetic resources are available for this genus. RESULTS: We present the analysis of high throughput transcriptome sequencing of three Stegodyphus species. Two of these are periodic-social (Stegodyphus lineatus and S.tentoriicola) and one is permanently social (S. mimosarum). From non-normalized cDNA libraries, we obtained on average 7,000 putative uni-genes for each species. Three-way orthology, as predicted from reciprocal BLAST, identified 1,792 genes that could be used for cross-species comparison. Open reading frames (ORFs) could be deduced from 1,345 of the three-way alignments. Preliminary molecular analyses suggest a five- to ten-fold reduction in heterozygosity in the social S. mimosarum compared with the periodic-social species. Furthermore, an increased ratio of non-synonymous to synonymous polymorphisms in the social species indicated relaxed efficiency of selection. However, there was no sign of relaxed selection on the phylogenetic branch leading to S. mimosarum. CONCLUSIONS: The 1,792 three-way ortholog genes identified in this study provide a unique resource for comparative studies of the eco-genomics, population genetics and molecular evolution of repeated evolution of inbreeding sociality within the Stegodyphus genus. Preliminary analyses support theoretical expectations of depleted heterozygosity and relaxed selection in the social inbreeding species. Relaxed selection could not be detected in the S. mimosarum lineage, suggesting that there has been a recent transition to sociality in this species.

The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species.

The fungus Mycosphaerella graminicola emerged as a new pathogen of cultivated wheat during its domestication ~11,000 yr ago. We assembled 12 high-quality full genome sequences to investigate the genetic footprints of selection in this wheat pathogen and closely related sister species that infect wild grasses. We demonstrate a strong effect of natural selection in shaping the pathogen genomes with only ~3% of nonsynonymous mutations being effectively neutral. Forty percent of all fixed nonsynonymous substitutions, on the other hand, are driven by positive selection. Adaptive evolution has affected M. graminicola to the highest extent, consistent with recent host specialization. Positive selection has prominently altered genes encoding secreted proteins and putative pathogen effectors supporting the premise that molecular host-pathogen interaction is a strong driver of pathogen evolution. Recent divergence between pathogen sister species is attested by the high degree of incomplete lineage sorting (ILS) in their genomes. We exploit ILS to generate a genetic map of the species without any crossing data, document recent times of species divergence relative to genome divergence, and show that gene-rich regions or regions with low recombination experience stronger effects of natural selection on neutral diversity. Emergence of a new agricultural host selected a highly specialized and fast-evolving pathogen with unique evolutionary patterns compared with its wild relatives. The strong impact of natural selection, we document, is at odds with the small effective population sizes estimated and suggest that population sizes were historically large but likely unstable.

Genomic determinants of protein evolution and polymorphism in Arabidopsis.

Recent results from Drosophila suggest that positive selection has a substantial impact on genomic patterns of polymorphism and divergence. However, species with smaller population sizes and/or stronger population structure may not be expected to exhibit Drosophila-like patterns of sequence variation. We test this prediction and identify determinants of levels of polymorphism and rates of protein evolution using genomic data from Arabidopsis thaliana and the recently sequenced Arabidopsis lyrata genome. We find that, in contrast to Drosophila, there is no negative relationship between nonsynonymous divergence and silent polymorphism at any spatial scale examined. Instead, synonymous divergence is a major predictor of silent polymorphism, which suggests variation in mutation rate as the main determinant of silent variation. Variation in rates of protein divergence is mainly correlated with gene expression level and breadth, consistent with results for a broad range of taxa, and map-based estimates of recombination rate are only weakly correlated with nonsynonymous divergence. Variation in mutation rates and the strength of purifying selection seem to be major drivers of patterns of polymorphism and divergence in Arabidopsis. Nevertheless, a model allowing for varying negative and positive selection by functional gene category explains the data better than a homogeneous model, implying the action of positive selection on a subset of genes. Genes involved in disease resistance and abiotic stress display high proportions of adaptive substitution. Our results are important for a general understanding of the determinants of rates of protein evolution and the impact of selection on patterns of polymorphism and divergence.

Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola.

The fungus Mycosphaerella graminicola has been a pathogen of wheat since host domestication 10,000-12,000 years ago in the Fertile Crescent. The wheat-infecting lineage emerged from closely related Mycosphaerella pathogens infecting wild grasses. We use a comparative genomics approach to assess how the process of host specialization affected the genome structure of M. graminicola since divergence from the closest known progenitor species named M. graminicola S1. The genome of S1 was obtained by Illumina sequencing resulting in a 35 Mb draft genome sequence of 32X. Assembled contigs were aligned to the previously sequenced M. graminicola genome. The alignment covered >90% of the non-repetitive portion of the M. graminicola genome with an average divergence of 7%. The sequenced M. graminicola strain is known to harbor thirteen essential chromosomes plus eight dispensable chromosomes. We found evidence that structural rearrangements significantly affected the dispensable chromosomes while the essential chromosomes were syntenic. At the nucleotide level, the essential and dispensable chromosomes have evolved differently. The average synonymous substitution rate in dispensable chromosomes is considerably lower than in essential chromosomes, whereas the average non-synonymous substitution rate is three times higher. Differences in molecular evolution can be related to different transmission and recombination patterns, as well as to differences in effective population sizes of essential and dispensable chromosomes. In order to identify genes potentially involved in host specialization or speciation, we calculated ratios of synonymous and non-synonymous substitution rates in the >9,500 aligned protein coding genes. The genes are generally under strong purifying selection. We identified 43 candidate genes showing evidence of positive selection, one encoding a potential pathogen effector protein. We conclude that divergence of these pathogens was accompanied by structural rearrangements in the small dispensable chromosomes, while footprints of positive selection were present in only a small number of protein coding genes.