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

TY - JOUR

T1 - Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

AU - Settepani, V.

AU - Schou, M. F.

AU - Greve, M.

AU - Grinsted, L.

AU - Bechsgaard, J.

AU - Bilde, T.

PY - 2017/8

Y1 - 2017/8

N2 - 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.

AB - 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.

KW - demographic modelling

KW - evolutionary dead end

KW - genetic diversity

KW - inbreeding

KW - RAD sequencing

KW - Stegodyphus

KW - LIFE-HISTORY TRAITS

KW - GENETIC DIVERSITY

KW - INBREEDING DEPRESSION

KW - SELF-FERTILIZATION

KW - DEAD-END

KW - METAPOPULATION STRUCTURE

KW - INTRASPECIFIC VARIATION

KW - DELETERIOUS MUTATIONS

KW - MOLECULAR EVOLUTION

KW - BREEDING SYSTEMS

U2 - 10.1111/mec.14196

DO - 10.1111/mec.14196

M3 - Journal article

C2 - 28570031

SN - 0962-1083

VL - 26

SP - 4197

EP - 4210

JO - Molecular Ecology

JF - Molecular Ecology

IS - 16

ER -