Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels.

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a "social syndrome," that includes cooperative breeding, reproductive skew, primary female-biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short-term benefits but come with long-term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD-sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister-species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within-population diversity were sixfold to 10-fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species-wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species-wide genetic diversity of social species was 5-8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.

Comparative genomic study of arachnid immune systems indicates loss of beta-1,3-glucanase-related proteins and the immune deficiency pathway.

Analyses of arthropod genomes have shown that the genes in the different innate humoral immune responses are conserved. These genes encode proteins that are involved in immune signalling pathways that recognize pathogens and activate immune responses. These immune responses include phagocytosis, encapsulation of the pathogen and production of effector molecules for pathogen elimination. So far, most studies have focused on insects leaving other major arthropod groups largely unexplored. Here, we annotate the immune-related genes of six arachnid genomes and present evidence for a conserved pattern of some immune genes, but also evolutionary changes in the arachnid immune system. Specifically, our results suggest that the family of recognition molecules of beta-1,3-glucanase-related proteins (ßGRPs) and the genes from the immune deficiency (IMD) signalling pathway have been lost in a common ancestor of arachnids. These findings are consistent with previous work suggesting that the humoral immune effector proteins are constitutively produced in arachnids in contrast to insects, where these have to be induced. Further functional studies are needed to verify this. We further show that the full haemolymph clotting cascade found in the horseshoe crab is retrieved in most arachnid genomes. Tetranychus lacks at least one major component, although it is possible that this cascade could still function through recruitment of a different protein. The gel-forming protein in horseshoe crabs, coagulogen, was not recovered in any of the arachnid genomes; however, it is possible that the arachnid clot consists of a related protein, spätzle, that is present in all of the genomes.

Low genetic diversity and strong but shallow population differentiation suggests genetic homogenization by metapopulation dynamics in a social spider.

Mating systems and population dynamics influence genetic diversity and structure. Species that experience inbreeding and limited gene flow are expected to evolve isolated, divergent genetic lineages. Metapopulation dynamics with frequent extinctions and colonizations may, on the other hand, deplete and homogenize genetic variation, if extinction rate is sufficiently high compared to the effect of drift in local demes. We investigated these theoretical predictions empirically in social spiders that are highly inbred. Social spiders show intranest mating, female-biased sex ratio, and frequent extinction and colonization events, factors that deplete genetic diversity within nests and populations and limit gene flow. We characterized population genetic structure in Stegodyphus sarasinorum, a social spider distributed across the Indian subcontinent. Species-wide genetic diversity was estimated over approximately 2800 km from Sri Lanka to Himalayas, by sequencing 16 protein-coding nuclear loci. We found 13 SNPs in 6592 bp (π = 0.00045) indicating low species-wide nucleotide diversity. Three genetic lineages were strongly differentiated; however, only one fixed difference among them suggests recent divergence. This is consistent with a scenario of metapopulation dynamics that homogenizes genetic diversity across the species' range. Ultimately, low standing genetic variation may hamper a species' ability to track environmental change and render social inbreeding spiders 'evolutionary dead-ends'.

Molecular evolution within and between self-incompatibility specificities.

Genes under multiallelic balancing selection have sharply contrasted evolutionary dynamics across timescales, with much longer coalescence time among functionally distinct allelic lines but much shorter coalescence time among gene copies within allelic lines as compared with the genomic background. In this paper, we combine theoretical and empirical approaches to investigate patterns of molecular evolution within and between self-incompatibility (SI) specificities. We first use numerical simulations to investigate coalescence times within allelic lines in a subdivided population for a sporophytic SI system. We then report on a comprehensive analysis of nucleotide polymorphism among gene copies within five distinct allelic lines in the closely related Arabidopsis halleri and Arabidopsis lyrata. In line with our model predictions, we find that the observed level of polymorphism among gene copies was generally low but differed among allelic lines. The data provide compelling direct evidence for recombination and/or gene conversion not only within the two most recessive allelic lines but also between two closely related but distinct allelic lines, suggesting that recombination at the Arabidopsis SI locus is possible in the absence of large sequence divergence among haplotypes. We observed shared polymorphic sites between the two species in one allelic line and strikingly similar haplotypes in another allelic line. We discuss whether convergent evolution may have led to this pattern and suggest that these observations are consistent with ongoing or very recent introgression, as previously documented.

Transmission ratio distortion in Arabidopsis lyrata: effects of population divergence and the S-locus.

We investigated transmission ratio distortion within an Icelandic population of Arabidopsis lyrata using 16 molecular markers unlinked to the S-locus. Transmission ratio distortion was found more often than expected by chance at the gametic level, but not at the genotypic or zygotic level. The gametic effect may be due to meiotic drive or selection acting postmeiotically. At the gametic level, 10.9% of the tests were significant, which is substantially lower than earlier observed in an interpopulation cross (allowing for differences in power)-suggesting that the high level of transmission ratio distortion in the interpopulation cross is due to population divergence. It is also substantially lower than previously observed in intrapopulation crosses at the self-incompatibility locus, suggesting inherent fitness differences of the self-incompatibility alleles. We discuss the possible role of deleterious alleles accumulating at loci under balancing selection. Zygotic effects play a larger role in the interpopulation cross than in the intrapopulation crosses suggesting that Dobzhansky-Muller incompatibilities may be accumulating between the widely diverged populations.

Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata.

Self-incompatibility in Arabidopsis lyrata is sporophytically controlled by the multi-allelic S-locus. Self-incompatibility alleles (S-alleles) are under strong negative frequency dependent selection because pollen carrying common S-alleles have fewer mating opportunities. Population genetics theory predicts that deleterious alleles can accumulate if linked to the S-locus. This was tested by studying segregation of S-alleles in 11 large full sib families in A. lyrata. Significant segregation distortion leading to an up to fourfold difference in transmission rates was found in six families. Differences in transmission rates were not significantly different in reciprocal crosses and the distortions observed were compatible with selection acting at the gametic stage alone. The S-allele with the largest segregation advantage is also the most recessive, and is very common in natural populations concordant with its apparent segregation advantage. These results imply that frequencies of S-alleles in populations of A. lyrata cannot be predicted based on simple models of frequency-dependent selection alone.