Biology subjects

Villesen, P.

Publications and source records attributed to Villesen, P..

3 recordsLinked to original sources

bioRxiv2025

Convergent Evolution of Sociality Causes Reduction of Mutation Rates in Spiders

Germline mutation rates influence the pace of molecular evolution, yet the roles of selection and life history in shaping their evolution remain to be determined. Comparative systems with replicated evolutionary transitions provide a unique opportunity to determine how changes in life history influence germline mutation rates. In the spider genus Stegodyphus, permanent sociality evolved independently three times within the past million years and is associated with obligate inbreeding, female-biased sex ratios, reduced fecundity, and sharply reduced effective population sizes. We sequenced 202 parent-offspring trios from 34 full-sibling families across three social and four closely related subsocial species and analysed quality-filtered trios in a phylogenetic comparative framework. Each independent transition to sociality was associated with an approximately 2-fold reduction in the de novo mutation rate in the germline. Phylogenetic analyses of synonymous branch lengths suggest that the mutation rates declined in parallel with the transitions to sociality. These rapid reductions in mutation rates in social lineages with small effective population sizes run counter to the drift-barrier hypothesis, which predicts that reduced selection efficacy would lead to higher mutation rates. We find no evidence that reduced mutation rates in the social species was favoured by selection for improving DNA repair efficiency, since there is no upregulation of DNA repair pathway genes in the ovaries of the social species. On the contrary, the mutation rate is reduced across mutational classes and in somatic tissue in social species compared with their subsocial counterparts. These patterns suggest that the reduction in mutation rate in social spiders is a consequence of convergent life history changes, including reduced body size and production of fewer, larger eggs. Our results highlight that the evolution of sociality, which entails major life history changes, can rapidly reshape fundamental evolutionary parameters, such as the germline mutation rate.

evolutionary biology↗

bioRxiv2024

Sociality in spiders is an evolutionary dead-end

In cooperatively breeding social animals, a few individuals account for all reproduction. In some taxa, sociality is accompanied by a transition from outcrossing to inbreeding, in concert, these traits act to reduce effective population size, potentially rendering transitions to sociality evolutionarily dead-ends. We addressed this hypothesis in a comparative genomic study in spiders, where sociality has evolved independently at least 23 times, but social species are recent and evolutionarily short-lived. We present genomic evidence for the evolutionary dead-end hypothesis in three independent transitions to sociality in the spider genus Stegodyphus. We sequenced, assembled and annotated high-quality, chromosome-level reference genomes from three pairs of closely related social and subsocial Stegodyphus species. Genome sizes range from 2.65 Gb to 3.32 Gb with high synteny, and we identify 10,065 single-copy orthologous genes. We timed the divergence between the social and subsocial species pairs to be from 1.3 to 1.8 million years. Social evolution in spiders involves a shift from outcrossing to inbreeding and from equal to female-biased sex ratio, causing severe reductions in effective population size and decreased efficacy of selection. Based on analyses of purifying selection, we determined whether transitions to sociality co-occurred with divergence. We show that transitions to sociality only had full effect on purifying selection at 119 kya (95CI: 71 kya -169 kya), 260 kya (95CI: 231 ky - 289 kya) and 279 kya (95CI: 230 kya - 332 kya) respectively, and follow remarkably similar convergent trajectories of progressive loss of diversity and shifts to an increasingly female-biased sex ratio. This almost deterministic genomic response to sociality may explain why social spider species do not persist. What causes species extinction is not clear, but could be either selfish meiotic drive that eliminates the production of males, or an inability to retain genome integrity in the face of extremely reduced efficacy of selection.

evolutionary biology↗

bioRxiv2020

From genotype to phenotype: maintenance of a chemical polymorphism in the context of high geneflow.

A major question in evolution is how to maintain many adaptive phenotypes within a species. In Mediterranean wild thyme, a staggering number of discrete chemical phenotypes (chemotypes) coexist in close geographic proximity. Plant chemotypes are defined by the dominant monoterpene produced in their essential oil. We study the genetics of six distinct chemotypes nested within two well established ecotypes. Ecotypes, and chemotypes within ecotypes, are spatially segregated, and their distribution tracks local differences in the abiotic environment. The ecotypes have undergone a rapid shift in distribution associated with current climate change. Here, combining genomic, phenotypic, and environmental data, we show how the genetics of ecotype determination can allow for such rapid evolutionary response despite high gene flow among ecotypes. Variation in three terpene-synthase loci explains almost all variation in ecotype identity, with one single locus accounting for as much as 78% of it. Phenotypic selection on ecotypes combined with low segregating genotypic redundancy and tight genetic determination leaves a clear footprint at the genomic level: alleles associated with ecotype identity track environmental variation despite extensive gene flow. Different chemotypes, nested within each ecotype, also track environmental variation. However, in contrast to ecotypes, chemotype identity is determined by more loci and show a wider range of genotypic redundancy, which dilutes the impact of phenotypic selection on alleles associated with different chemotypes. Identifying the genetics behind this polymorphism in thyme is a crucial step towards understanding the maintenance of this widespread chemical polymorphism found in many aromatic Lamiaceae.

evolutionary biology↗