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 John Parker; Elizabeth Cash; Eyal Privman; Christopher P Childers; Monica C Muñoz-Torres; Jacobus Jan 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

doi:10.1101/gr.155408.113

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 John Parker, Elizabeth Cash, Eyal Privman, Christopher P ChildersMonica C Muñoz-Torres, Jacobus Jan 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

156 Citationer (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 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.

Originalsprog	Engelsk
Tidsskrift	Genome Research
Vol/bind	23
Udgave nummer	8
Sider (fra-til)	1235-1247
Antal sider	13
ISSN	1088-9051
DOI	https://doi.org/10.1101/gr.155408.113
Status	Udgivet - aug. 2013

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10.1101/gr.155408.113

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Simola, D. F., Wissler, L., Donahue, G., Waterhouse, R. M., Helmkampf, M., Roux, J., Nygaard, S., Glastad, K. M., Hagen, D. E., Viljakainen, L., Reese, J. T., Hunt, B. G., Graur, D., Elhaik, E., Kriventseva, E. V., Wen, J., Parker, B. J., Cash, E., Privman, E., ... Gadau, J. (2013). Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Research, 23(8), 1235-1247. https://doi.org/10.1101/gr.155408.113

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, Muñoz-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, bind 23, nr. 8, s. 1235-1247. https://doi.org/10.1101/gr.155408.113

@article{b2fbf0a8edc24eeaadae5c8337f3508c,

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.",

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

year = "2013",

month = aug,

doi = "10.1101/gr.155408.113",

language = "English",

volume = "23",

pages = "1235--1247",

journal = "Genome Research",

issn = "1088-9051",

publisher = "Cold Spring Harbor Laboratory Press",

number = "8",

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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 John

AU - Cash, Elizabeth

AU - Privman, Eyal

AU - Childers, Christopher P

AU - Muñoz-Torres, Monica C

AU - Boomsma, Jacobus Jan

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 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.

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 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.

U2 - 10.1101/gr.155408.113

DO - 10.1101/gr.155408.113

M3 - Journal article

C2 - 23636946

SN - 1088-9051

VL - 23

SP - 1235

EP - 1247

JO - Genome Research

JF - Genome Research

IS - 8

ER -

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

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