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

Settepani, V.; Schou, M.F. LU ; Greve, M.; Grinsted, L.; Bechsgaard, J. and Bilde, T. (2017) In Molecular Ecology 26(16). p.4197-4210
Abstract
textcopyright 2017 John Wiley Sons Ltd.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... (More)
textcopyright 2017 John Wiley Sons Ltd.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. (Less)
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author
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Demographic modelling, evolutionary dead end, genetic diversity, inbreeding, RAD sequencing, Stegodyphus
in
Molecular Ecology
volume
26
issue
16
pages
14 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:85021338126
ISSN
0962-1083
DOI
10.1111/mec.14196
language
Unknown
LU publication?
no
id
d46c3c60-f65e-44cb-a60b-c6830175d144
date added to LUP
2017-12-18 09:47:57
date last changed
2018-01-07 12:29:09
@article{d46c3c60-f65e-44cb-a60b-c6830175d144,
  abstract     = {textcopyright 2017 John Wiley  Sons Ltd.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.},
  author       = {Settepani, V. and Schou, M.F. and Greve, M. and Grinsted, L. and Bechsgaard, J. and Bilde, T.},
  issn         = {0962-1083},
  keyword      = {Demographic modelling,evolutionary dead end,genetic diversity,inbreeding,RAD sequencing,Stegodyphus },
  language     = {und},
  number       = {16},
  pages        = {4197--4210},
  publisher    = {Wiley-Blackwell},
  series       = {Molecular Ecology},
  title        = {Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels},
  url          = {http://dx.doi.org/10.1111/mec.14196},
  volume       = {26},
  year         = {2017},
}