A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism
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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.
I: Nature Ecology & Evolution, Bind 6, Nr. 8, 2022, s. 1191-1204.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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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