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Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

Simola, Daniel F ; Wissler, Lothar ; Donahue, Greg ; Waterhouse, Robert M ; Helmkampf, Martin ; Roux, Julien ; Nygaard, Sanne ; Glastad, Karl M ; Hagen, Darren E and Viljakainen, Lumi , et al. (2013) In Genome Research 23(8). p.47-1235
Abstract

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements;... (More)

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.

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publishing date
type
Contribution to journal
publication status
published
keywords
Animals, Ants/genetics, Behavior, Animal, Binding Sites, Conserved Sequence, DNA Methylation, Evolution, Molecular, Gene Expression Regulation, Genome, Insect, Hymenoptera/genetics, Insect Proteins/genetics, MicroRNAs/genetics, Models, Genetic, Phylogeny, Regulatory Sequences, Nucleic Acid, Sequence Analysis, DNA, Social Behavior, Species Specificity, Synteny, Transcription Factors/genetics
in
Genome Research
volume
23
issue
8
pages
47 - 1235
publisher
Cold Spring Harbor Laboratory Press (CSHL)
external identifiers
  • scopus:84881151042
  • pmid:23636946
ISSN
1549-5469
DOI
10.1101/gr.155408.113
language
English
LU publication?
no
id
3cfaeced-87cc-4324-aa4d-bc1a722e84f4
date added to LUP
2019-11-10 16:56:09
date last changed
2020-10-18 04:40:57
@article{3cfaeced-87cc-4324-aa4d-bc1a722e84f4,
  abstract     = {<p>Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations. </p>},
  author       = {Simola, Daniel F and Wissler, Lothar and Donahue, Greg and Waterhouse, Robert M and Helmkampf, Martin and Roux, Julien and Nygaard, Sanne and Glastad, Karl M and Hagen, Darren E and Viljakainen, Lumi and Reese, Justin T and Hunt, Brendan G and Graur, Dan and Elhaik, Eran and Kriventseva, Evgenia V and Wen, Jiayu and Parker, Brian J and Cash, Elizabeth and Privman, Eyal and Childers, Christopher P and Muñoz-Torres, Monica C and Boomsma, Jacobus J and Bornberg-Bauer, Erich and Currie, Cameron R and Elsik, Christine G and Suen, Garret and Goodisman, Michael A D and Keller, Laurent and Liebig, Jürgen and Rawls, Alan and Reinberg, Danny and Smith, Chris D and Smith, Chris R and Tsutsui, Neil and Wurm, Yannick and Zdobnov, Evgeny M and Berger, Shelley L and Gadau, Jürgen},
  issn         = {1549-5469},
  language     = {eng},
  number       = {8},
  pages        = {47--1235},
  publisher    = {Cold Spring Harbor Laboratory Press (CSHL)},
  series       = {Genome Research},
  title        = {Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality},
  url          = {http://dx.doi.org/10.1101/gr.155408.113},
  doi          = {10.1101/gr.155408.113},
  volume       = {23},
  year         = {2013},
}