A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism. / Li, Qiye; Wang, Mingyue; Zhang, Pei; Liu, Yang; Guo, Qunfei; Zhu, Yuanzhen; Wen, Tinggang; Dai, Xueqin; Zhang, Xiafang; Nagel, Manuel; Dethlefsen, Bjarke Hamberg; Xie, Nianxia; Zhao, Jie; Jiang, Wei; Han, Lei; Wu, Liang; Zhong, Wenjiang; Wang, Zhifeng; Wei, Xiaoyu; Dai, Wei; Liu, Longqi; Xu, Xun; Lu, Haorong; Yang, Huanming; Wang, Jian; Boomsma, Jacobus J.; Liu, Chuanyu; Zhang, Guojie; Liu, Weiwei.

In: Nature Ecology & Evolution, Vol. 6, No. 8, 2022, p. 1191-1204.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Li, Q, Wang, M, Zhang, P, Liu, Y, Guo, Q, Zhu, Y, Wen, T, Dai, X, Zhang, X, Nagel, M, Dethlefsen, BH, Xie, N, Zhao, J, Jiang, W, Han, L, Wu, L, Zhong, W, Wang, Z, Wei, X, Dai, W, Liu, L, Xu, X, Lu, H, Yang, H, Wang, J, Boomsma, JJ, Liu, C, Zhang, G & Liu, W 2022, 'A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism', Nature Ecology & Evolution, vol. 6, no. 8, pp. 1191-1204. https://doi.org/10.1038/s41559-022-01784-1

APA

Li, Q., Wang, M., Zhang, P., Liu, Y., Guo, Q., Zhu, Y., Wen, T., Dai, X., Zhang, X., Nagel, M., Dethlefsen, B. H., Xie, N., Zhao, J., Jiang, W., Han, L., Wu, L., Zhong, W., Wang, Z., Wei, X., ... Liu, W. (2022). A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism. Nature Ecology & Evolution, 6(8), 1191-1204. https://doi.org/10.1038/s41559-022-01784-1

Vancouver

Li Q, Wang M, Zhang P, Liu Y, Guo Q, Zhu Y et al. A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism. Nature Ecology & Evolution. 2022;6(8):1191-1204. https://doi.org/10.1038/s41559-022-01784-1

Author

Li, Qiye ; Wang, Mingyue ; Zhang, Pei ; Liu, Yang ; Guo, Qunfei ; Zhu, Yuanzhen ; Wen, Tinggang ; Dai, Xueqin ; Zhang, Xiafang ; Nagel, Manuel ; Dethlefsen, Bjarke Hamberg ; Xie, Nianxia ; Zhao, Jie ; Jiang, Wei ; Han, Lei ; Wu, Liang ; Zhong, Wenjiang ; Wang, Zhifeng ; Wei, Xiaoyu ; Dai, Wei ; Liu, Longqi ; Xu, Xun ; Lu, Haorong ; Yang, Huanming ; Wang, Jian ; Boomsma, Jacobus J. ; Liu, Chuanyu ; Zhang, Guojie ; Liu, Weiwei. / A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism. In: Nature Ecology & Evolution. 2022 ; Vol. 6, No. 8. pp. 1191-1204.

Bibtex

@article{5532a2056f7448f5ae916359b1ed6390,
title = "A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism",
abstract = "Using single-cell transcriptomics, the authors generate a brain cell atlas for the pharaoh ant including individuals of different sexes and castes and show changes in cell composition underlying division of labour and reproductive specialization.Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.",
keywords = "MUSHROOM BODIES, GENE-EXPRESSION, PHARAOHS ANT, BRAIN, INTERNEURONS, EVOLUTION, HONEYBEE, DIFFERENTIATION, REPRODUCTION, HIERARCHY",
author = "Qiye Li and Mingyue Wang and Pei Zhang and Yang Liu and Qunfei Guo and Yuanzhen Zhu and Tinggang Wen and Xueqin Dai and Xiafang Zhang and Manuel Nagel and Dethlefsen, {Bjarke Hamberg} and Nianxia Xie and Jie Zhao and Wei Jiang and Lei Han and Liang Wu and Wenjiang Zhong and Zhifeng Wang and Xiaoyu Wei and Wei Dai and Longqi Liu and Xun Xu and Haorong Lu and Huanming Yang and Jian Wang and Boomsma, {Jacobus J.} and Chuanyu Liu and Guojie Zhang and Weiwei Liu",
year = "2022",
doi = "10.1038/s41559-022-01784-1",
language = "English",
volume = "6",
pages = "1191--1204",
journal = "Nature Ecology & Evolution",
issn = "2397-334X",
publisher = "nature publishing group",
number = "8",

}

RIS

TY - JOUR

T1 - A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism

AU - Li, Qiye

AU - Wang, Mingyue

AU - Zhang, Pei

AU - Liu, Yang

AU - Guo, Qunfei

AU - Zhu, Yuanzhen

AU - Wen, Tinggang

AU - Dai, Xueqin

AU - Zhang, Xiafang

AU - Nagel, Manuel

AU - Dethlefsen, Bjarke Hamberg

AU - Xie, Nianxia

AU - Zhao, Jie

AU - Jiang, Wei

AU - Han, Lei

AU - Wu, Liang

AU - Zhong, Wenjiang

AU - Wang, Zhifeng

AU - Wei, Xiaoyu

AU - Dai, Wei

AU - Liu, Longqi

AU - Xu, Xun

AU - Lu, Haorong

AU - Yang, Huanming

AU - Wang, Jian

AU - Boomsma, Jacobus J.

AU - Liu, Chuanyu

AU - Zhang, Guojie

AU - Liu, Weiwei

PY - 2022

Y1 - 2022

N2 - Using single-cell transcriptomics, the authors generate a brain cell atlas for the pharaoh ant including individuals of different sexes and castes and show changes in cell composition underlying division of labour and reproductive specialization.Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.

AB - Using single-cell transcriptomics, the authors generate a brain cell atlas for the pharaoh ant including individuals of different sexes and castes and show changes in cell composition underlying division of labour and reproductive specialization.Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.

KW - MUSHROOM BODIES

KW - GENE-EXPRESSION

KW - PHARAOHS ANT

KW - BRAIN

KW - INTERNEURONS

KW - EVOLUTION

KW - HONEYBEE

KW - DIFFERENTIATION

KW - REPRODUCTION

KW - HIERARCHY

U2 - 10.1038/s41559-022-01784-1

DO - 10.1038/s41559-022-01784-1

M3 - Journal article

C2 - 35711063

VL - 6

SP - 1191

EP - 1204

JO - Nature Ecology & Evolution

JF - Nature Ecology & Evolution

SN - 2397-334X

IS - 8

ER -

ID: 312372505