title: Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality.
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 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.
authors: Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
authors: Daniel F
authors: DF
authors: Simola
authors: Lothar
authors: L
authors: Wissler
authors: Greg
authors: G
authors: Donahue
authors: Robert M
authors: RM
authors: Waterhouse
authors: Martin
authors: M
authors: Helmkampf
authors: Julien
authors: J
authors: Roux
authors: Sanne
authors: S
authors: Nygaard
authors: Karl M
authors: KM
authors: Glastad
authors: Darren E
authors: DE
authors: Hagen
authors: Lumi
authors: L
authors: Viljakainen
authors: Justin T
authors: JT
authors: Reese
authors: Brendan G
authors: BG
authors: Hunt
authors: Dan
authors: D
authors: Graur
authors: Eran
authors: E
authors: Elhaik
authors: Evgenia V
authors: EV
authors: Kriventseva
authors: Jiayu
authors: J
authors: Wen
authors: Brian J
authors: BJ
authors: Parker
authors: Elizabeth
authors: E
authors: Cash
authors: Eyal
authors: E
authors: Privman
authors: Christopher P
authors: CP
authors: Childers
authors: Monica C
authors: MC
authors: Muñoz-Torres
authors: Jacobus J
authors: JJ
authors: Boomsma
authors: Erich
authors: E
authors: Bornberg-Bauer
authors: Cameron R
authors: CR
authors: Currie
authors: Christine G
authors: CG
authors: Elsik
authors: Garret
authors: G
authors: Suen
authors: Michael A D
authors: MA
authors: Goodisman
authors: Laurent
authors: L
authors: Keller
authors: Jürgen
authors: J
authors: Liebig
authors: Alan
authors: A
authors: Rawls
authors: Danny
authors: D
authors: Reinberg
authors: Chris D
authors: CD
authors: Smith
authors: Chris R
authors: CR
authors: Smith
authors: Neil
authors: N
authors: Tsutsui
authors: Yannick
authors: Y
authors: Wurm
authors: Evgeny M
authors: EM
authors: Zdobnov
authors: Shelley L
authors: SL
authors: Berger
authors: Jürgen
authors: J
authors: Gadau
mesh_terms: D000818:Animals; D001000:Ants / Q000235:genetics*; D001522:Behavior, Animal; D001665:Binding Sites; D017124:Conserved Sequence; D019175:DNA Methylation; D019143:Evolution, Molecular; D005786:Gene Expression Regulation; D049750:Genome, Insect; D006927:Hymenoptera / Q000235:genetics; D019476:Insect Proteins / Q000235:genetics; D035683:MicroRNAs / Q000235:genetics; D008957:Models, Genetic; D010802:Phylogeny; D012045:Regulatory Sequences, Nucleic Acid; D017422:Sequence Analysis, DNA; D012919:Social Behavior; D013045:Species Specificity; D026801:Synteny; D014157:Transcription Factors / Q000235:genetics
chemical_list: D019476:Insect Proteins; D035683:MicroRNAs; D014157:Transcription Factors
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