BackgroundThe duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum.ResultsWe found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication.ConclusionsOur results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0399-x) contains supplementary material, which is available to authorized users.

Spiders are ecologically important predators with complex venom and extraordinarily tough silk that enables capture of large prey. Here we present the assembled genome of the social velvet spider and a draft assembly of the tarantula genome that represent two major taxonomic groups of spiders. The spider genomes are large with short exons and long introns, reminiscent of mammalian genomes. Phylogenetic analyses place spiders and ticks as sister groups supporting polyphyly of the Acari. Complex sets of venom and silk genes/proteins are identified. We find that venom genes evolved by sequential duplication, and that the toxic effect of venom is most likely activated by proteases present in the venom. The set of silk genes reveals a highly dynamic gene evolution, new types of silk genes and proteins, and a novel use of aciniform silk. These insights create new opportunities for pharmacological applications of venom and biomaterial applications of silk.

Flowering plants often prevent selfing through mechanisms of self-incompatibility (S.I.). The loss of S.I. has occurred many times independently, because it provides short-term advantages in situations where pollinators or mates are rare. The genus Capsella, which is closely related to Arabidopsis, contains a pair of closely related diploid species, the self-incompatible Capsella grandiflora and the self-compatible Capsella rubella. To elucidate the transition to selfing and its relationship to speciation of C. rubella, we have made use of comparative sequence information. Our analyses indicate that C. rubella separated from C. grandiflora recently (Ϸ30,000 -50,000 years ago) and that breakdown of S.I. occurred at approximately the same time. Contrasting the nucleotide diversity patterns of the 2 species, we found that C. rubella has only 1 or 2 alleles at most loci, suggesting that it originated through an extreme population bottleneck. Our data are consistent with diploid speciation by a single, selfing individual, most likely living in Greece. The new species subsequently colonized the Mediterranean by Northern and Southern routes, at a time that also saw the spread of agriculture. The presence of phenotypic diversity within modern C. rubella suggests that this species will be an interesting model to understand divergence and adaptation, starting from very limited standing genetic variation.

Recently diverged species typically have incomplete reproductive barriers, allowing introgression of genetic material from one species into the genomic background of the other. The role of natural selection in preventing or promoting introgression remains contentious. Because of genomic co-adaptation, some chromosomal fragments are expected to be selected against in the new background and resist introgression. In contrast, natural selection should favor introgression for alleles at genes evolving under multi-allelic balancing selection, such as the MHC in vertebrates, disease resistance, or self-incompatibility genes in plants. Here, we test the prediction that negative, frequency-dependent selection on alleles at the multi-allelic gene controlling pistil self-incompatibility specificity in two closely related species, Arabidopsis halleri and A. lyrata, caused introgression at this locus at a higher rate than the genomic background. Polymorphism at this gene is largely shared, and we have identified 18 pairs of S-alleles that are only slightly divergent between the two species. For these pairs of S-alleles, divergence at four-fold degenerate sites (K = 0.0193) is about four times lower than the genomic background (K = 0.0743). We demonstrate that this difference cannot be explained by differences in effective population size between the two types of loci. Rather, our data are most consistent with a five-fold increase of introgression rates for S-alleles as compared to the genomic background, making this study the first documented example of adaptive introgression facilitated by balancing selection. We suggest that this process plays an important role in the maintenance of high allelic diversity and divergence at the S-locus in flowering plant families. Because genes under balancing selection are expected to be among the last to stop introgressing, their comparison in closely related species provides a lower-bound estimate of the time since the species stopped forming fertile hybrids, thereby complementing the average portrait of divergence between species provided by genomic data.

A recent investigation found evidence that the transition of Arabidopsis thaliana from ancestral self-incompatibility (SI) to full self-compatibility occurred very recently and suggested that this occurred through a selective fixation of a nonfunctional allele (PsiSCR1) at the SCR gene, which determines pollen specificity in the incompatibility response. The main evidence is the lack of polymorphism at the SCR locus in A. thaliana. However, the nearby SRK gene, which determines stigma specificity in self-incompatible Brassicaceae species, has extremely high sequence diversity, with 3 very divergent SRK haplotypes, 2 of them present in multiple strains. Such high diversity is extremely unusual in this species, and it suggests the possibility that multiple, different SRK haplotypes may have been preserved from A. thaliana's self-incompatible ancestor. To study the evolution of S-haplotypes in the A. thaliana lineage, we searched the 2 most closely related Arabidopsis species Arabidopsis lyrata and Arabidopsis halleri, in which most populations have retained SI, and found SRK sequences corresponding to all 3 A. thaliana haplogroup sequences. Our molecular evolutionary analyses of these 3 S-haplotypes provide an independent estimate of the timing of the breakdown of SI and again exclude an ancient transition to selfing in A. thaliana. Comparing sequences of each of the 3 haplogroups between species, we find that 2 of the 3 SRK sequences (haplogroups A and B) are similar throughout their length, suggesting that little or no recombination with other SRK alleles has occurred since these species diverged. The diversity difference between the SCR and SRK loci in A. thaliana, however, suggests crossing-over, either within SRK or between the SCR and SRK loci. If the loss of SI involved fixation of the PsiSCR1 sequence, the exchange must have occurred during its fixation. Divergence between the species is much lower at the S-locus, compared with reference loci, and we discuss two contributory possibilities. Introgression may have occurred between A. lyrata and A. halleri and between their ancestral lineage and A. thaliana, at least for some period after their split. In addition, the coalescence times of sequences of individual S-haplogroups are expected to be less than those of alleles at non-S-loci.