TY - JOUR
T1 - Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality
AU - Simola, Daniel F.
AU - Wissler, Lothar
AU - Donahue, Greg
AU - Waterhouse, Robert M.
AU - Helmkampf, Martin
AU - Roux, Julien
AU - Nygaard, Sanne
AU - Glastad, Karl M.
AU - Hagen, Darren E.
AU - Viljakainen, Lumi
AU - Reese, Justin T.
AU - Hunt, Brendan G.
AU - Graur, Dan
AU - Elhaik, Eran
AU - Kriventseva, Evgenia V.
AU - Wen, Jiayu
AU - Parker, Brian J.
AU - Cash, Elizabeth
AU - Privman, Eyal
AU - Childers, Christopher P.
AU - Munoz-Torres, Monica C.
AU - Boomsma, Jacobus J.
AU - Bornberg-Bauer, Erich
AU - Currie, Cameron R.
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
AU - Wurm, Yannick
AU - Zdobnov, Evgeny M.
AU - Berger, Shelley L.
AU - Gadau, Jürgen
PY - 2013/8
Y1 - 2013/8
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=84881151042&partnerID=8YFLogxK
U2 - 10.1101/gr.155408.113
DO - 10.1101/gr.155408.113
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C2 - 23636946
AN - SCOPUS:84881151042
SN - 1088-9051
VL - 23
SP - 1235
EP - 1247
JO - Genome Research
JF - Genome Research
IS - 8
ER -