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

Daniel F. Simola, Lothar Wissler, Greg Donahue, Robert M. Waterhouse, Martin Helmkampf, Julien Roux, Sanne Nygaard, Karl M. Glastad, Darren E. Hagen, Lumi Viljakainen, Justin T. Reese, Brendan G. Hunt, Dan Graur, Eran Elhaik, Evgenia V. Kriventseva, Jiayu Wen, Brian J. Parker, Elizabeth Cash, Eyal Privman, Christopher P. ChildersMonica C. Munoz-Torres, Jacobus J. Boomsma, Erich Bornberg-Bauer, Cameron R. Currie, Christine G. Elsik, Garret Suen, Michael A D Goodisman, Laurent Keller, Jürgen Liebig, Alan Rawls, Danny Reinberg, Chris D. Smith, Chris R. Smith, Neil Tsutsui, Yannick Wurm, Evgeny M. Zdobnov, Shelley L. Berger, Jürgen Gadau

Research output: Contribution to journalArticle

138 Citations (Scopus)

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; 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 lineagespecific 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.

Original languageEnglish (US)
Pages (from-to)1235-1247
Number of pages13
JournalGenome Research
Volume23
Issue number8
DOIs
StatePublished - Aug 2013

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Insect Genome
Ants
Genes
Genome
Drosophila
Insects
Odorant Receptors
Synteny
Untranslated RNA

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

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.; Viljakainen, Lumi; Reese, Justin T.; Hunt, Brendan G.; Graur, Dan; Elhaik, Eran; Kriventseva, Evgenia V.; Wen, Jiayu; Parker, Brian J.; Cash, Elizabeth; Privman, Eyal; Childers, Christopher P.; Munoz-Torres, Monica C.; Boomsma, Jacobus J.; Bornberg-Bauer, Erich; Currie, Cameron R.; Elsik, Christine G.; Suen, Garret; Goodisman, Michael A D; Keller, Laurent; Liebig, Jürgen; Rawls, Alan; Reinberg, Danny; Smith, Chris D.; Smith, Chris R.; Tsutsui, Neil; Wurm, Yannick; Zdobnov, Evgeny M.; Berger, Shelley L.; Gadau, Jürgen.

In: Genome Research, Vol. 23, No. 8, 08.2013, p. 1235-1247.

Research output: Contribution to journalArticle

Simola, DF, Wissler, L, Donahue, G, Waterhouse, RM, Helmkampf, M, Roux, J, Nygaard, S, Glastad, KM, Hagen, DE, Viljakainen, L, Reese, JT, Hunt, BG, Graur, D, Elhaik, E, Kriventseva, EV, Wen, J, Parker, BJ, Cash, E, Privman, E, Childers, CP, Munoz-Torres, MC, Boomsma, JJ, Bornberg-Bauer, E, Currie, CR, Elsik, CG, Suen, G, Goodisman, MAD, Keller, L, Liebig, J, Rawls, A, Reinberg, D, Smith, CD, Smith, CR, Tsutsui, N, Wurm, Y, Zdobnov, EM, Berger, SL & Gadau, J 2013, 'Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality', Genome Research, vol. 23, no. 8, pp. 1235-1247. https://doi.org/10.1101/gr.155408.113
Simola, Daniel F. ; Wissler, Lothar ; Donahue, Greg ; Waterhouse, Robert M. ; Helmkampf, Martin ; Roux, Julien ; Nygaard, Sanne ; Glastad, Karl M. ; Hagen, Darren E. ; Viljakainen, Lumi ; Reese, Justin T. ; Hunt, Brendan G. ; Graur, Dan ; Elhaik, Eran ; Kriventseva, Evgenia V. ; Wen, Jiayu ; Parker, Brian J. ; Cash, Elizabeth ; Privman, Eyal ; Childers, Christopher P. ; Munoz-Torres, Monica C. ; Boomsma, Jacobus J. ; Bornberg-Bauer, Erich ; Currie, Cameron R. ; Elsik, Christine G. ; Suen, Garret ; Goodisman, Michael A D ; Keller, Laurent ; Liebig, Jürgen ; Rawls, Alan ; Reinberg, Danny ; Smith, Chris D. ; Smith, Chris R. ; Tsutsui, Neil ; Wurm, Yannick ; Zdobnov, Evgeny M. ; Berger, Shelley L. ; Gadau, Jürgen. / Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. In: Genome Research. 2013 ; Vol. 23, No. 8. pp. 1235-1247.
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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; 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 lineagespecific 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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AU - Helmkampf, Martin

AU - Roux, Julien

AU - Nygaard, Sanne

AU - Glastad, Karl M.

AU - Hagen, Darren E.

AU - Viljakainen, Lumi

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AU - Childers, Christopher P.

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AU - Elsik, Christine G.

AU - Suen, Garret

AU - Goodisman, Michael A D

AU - Keller, Laurent

AU - Liebig, Jürgen

AU - Rawls, Alan

AU - Reinberg, Danny

AU - Smith, Chris D.

AU - Smith, Chris R.

AU - Tsutsui, Neil

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