Canalized gene expression during development mediates caste differentiation in ants

Research output: Contribution to journalJournal articlepeer-review

Standard

Canalized gene expression during development mediates caste differentiation in ants. / Qiu, Bitao; Dai, Xueqin; Li, Panyi; Larsen, Rasmus Stenbak; Li, Ruyan; Price, Alivia Lee; Ding, Guo; Texada, Michael James; Zhang, Xiafang; Zuo, Dashuang; Gao, Qionghua; Jiang, Wei; Wen, Tinggang; Pontieri, Luigi; Guo, Chunxue; Rewitz, Kim; Li, Qiye; Liu, Weiwei; Boomsma, Jacobus J.; Zhang, Guojie.

In: Nature Ecology and Evolution, Vol. 6, No. 11, 2022, p. 1753-1765.

Research output: Contribution to journalJournal articlepeer-review

Harvard

Qiu, B, Dai, X, Li, P, Larsen, RS, Li, R, Price, AL, Ding, G, Texada, MJ, Zhang, X, Zuo, D, Gao, Q, Jiang, W, Wen, T, Pontieri, L, Guo, C, Rewitz, K, Li, Q, Liu, W, Boomsma, JJ & Zhang, G 2022, 'Canalized gene expression during development mediates caste differentiation in ants', Nature Ecology and Evolution, vol. 6, no. 11, pp. 1753-1765. https://doi.org/10.1038/s41559-022-01884-y

APA

Qiu, B., Dai, X., Li, P., Larsen, R. S., Li, R., Price, A. L., Ding, G., Texada, M. J., Zhang, X., Zuo, D., Gao, Q., Jiang, W., Wen, T., Pontieri, L., Guo, C., Rewitz, K., Li, Q., Liu, W., Boomsma, J. J., & Zhang, G. (2022). Canalized gene expression during development mediates caste differentiation in ants. Nature Ecology and Evolution, 6(11), 1753-1765. https://doi.org/10.1038/s41559-022-01884-y

Vancouver

Qiu B, Dai X, Li P, Larsen RS, Li R, Price AL et al. Canalized gene expression during development mediates caste differentiation in ants. Nature Ecology and Evolution. 2022;6(11):1753-1765. https://doi.org/10.1038/s41559-022-01884-y

Author

Qiu, Bitao ; Dai, Xueqin ; Li, Panyi ; Larsen, Rasmus Stenbak ; Li, Ruyan ; Price, Alivia Lee ; Ding, Guo ; Texada, Michael James ; Zhang, Xiafang ; Zuo, Dashuang ; Gao, Qionghua ; Jiang, Wei ; Wen, Tinggang ; Pontieri, Luigi ; Guo, Chunxue ; Rewitz, Kim ; Li, Qiye ; Liu, Weiwei ; Boomsma, Jacobus J. ; Zhang, Guojie. / Canalized gene expression during development mediates caste differentiation in ants. In: Nature Ecology and Evolution. 2022 ; Vol. 6, No. 11. pp. 1753-1765.

Bibtex

@article{e6a4f71aaa30489d8e3098d860e02ded,
title = "Canalized gene expression during development mediates caste differentiation in ants",
abstract = "Ant colonies are higher-level organisms consisting of specialized reproductive and non-reproductive individuals that differentiate early in development, similar to germ–soma segregation in bilateral Metazoa. Analogous to diverging cell lines, developmental differentiation of individual ants has often been considered in epigenetic terms but the sets of genes that determine caste phenotypes throughout larval and pupal development remain unknown. Here, we reconstruct the individual developmental trajectories of two ant species, Monomorium pharaonis and Acromyrmex echinatior, after obtaining >1,400 whole-genome transcriptomes. Using a new backward prediction algorithm, we show that caste phenotypes can be accurately predicted by genome-wide transcriptome profiling. We find that caste differentiation is increasingly canalized from early development onwards, particularly in germline individuals (gynes/queens) and that the juvenile hormone signalling pathway plays a key role in this process by regulating body mass divergence between castes. We quantified gene-specific canalization levels and found that canalized genes with gyne/queen-biased expression were enriched for ovary and wing functions while canalized genes with worker-biased expression were enriched in brain and behavioural functions. Suppression in gyne larvae of Freja, a highly canalized gyne-biased ovary gene, disturbed pupal development by inducing non-adaptive intermediate phenotypes between gynes and workers. Our results are consistent with natural selection actively maintaining canalized caste phenotypes while securing robustness in the life cycle ontogeny of ant colonies.",
author = "Bitao Qiu and Xueqin Dai and Panyi Li and Larsen, {Rasmus Stenbak} and Ruyan Li and Price, {Alivia Lee} and Guo Ding and Texada, {Michael James} and Xiafang Zhang and Dashuang Zuo and Qionghua Gao and Wei Jiang and Tinggang Wen and Luigi Pontieri and Chunxue Guo and Kim Rewitz and Qiye Li and Weiwei Liu and Boomsma, {Jacobus J.} and Guojie Zhang",
note = "Publisher Copyright: {\textcopyright} 2022, The Author(s).",
year = "2022",
doi = "10.1038/s41559-022-01884-y",
language = "English",
volume = "6",
pages = "1753--1765",
journal = "Nature Ecology & Evolution",
issn = "2397-334X",
publisher = "nature publishing group",
number = "11",

}

RIS

TY - JOUR

T1 - Canalized gene expression during development mediates caste differentiation in ants

AU - Qiu, Bitao

AU - Dai, Xueqin

AU - Li, Panyi

AU - Larsen, Rasmus Stenbak

AU - Li, Ruyan

AU - Price, Alivia Lee

AU - Ding, Guo

AU - Texada, Michael James

AU - Zhang, Xiafang

AU - Zuo, Dashuang

AU - Gao, Qionghua

AU - Jiang, Wei

AU - Wen, Tinggang

AU - Pontieri, Luigi

AU - Guo, Chunxue

AU - Rewitz, Kim

AU - Li, Qiye

AU - Liu, Weiwei

AU - Boomsma, Jacobus J.

AU - Zhang, Guojie

N1 - Publisher Copyright: © 2022, The Author(s).

PY - 2022

Y1 - 2022

N2 - Ant colonies are higher-level organisms consisting of specialized reproductive and non-reproductive individuals that differentiate early in development, similar to germ–soma segregation in bilateral Metazoa. Analogous to diverging cell lines, developmental differentiation of individual ants has often been considered in epigenetic terms but the sets of genes that determine caste phenotypes throughout larval and pupal development remain unknown. Here, we reconstruct the individual developmental trajectories of two ant species, Monomorium pharaonis and Acromyrmex echinatior, after obtaining >1,400 whole-genome transcriptomes. Using a new backward prediction algorithm, we show that caste phenotypes can be accurately predicted by genome-wide transcriptome profiling. We find that caste differentiation is increasingly canalized from early development onwards, particularly in germline individuals (gynes/queens) and that the juvenile hormone signalling pathway plays a key role in this process by regulating body mass divergence between castes. We quantified gene-specific canalization levels and found that canalized genes with gyne/queen-biased expression were enriched for ovary and wing functions while canalized genes with worker-biased expression were enriched in brain and behavioural functions. Suppression in gyne larvae of Freja, a highly canalized gyne-biased ovary gene, disturbed pupal development by inducing non-adaptive intermediate phenotypes between gynes and workers. Our results are consistent with natural selection actively maintaining canalized caste phenotypes while securing robustness in the life cycle ontogeny of ant colonies.

AB - Ant colonies are higher-level organisms consisting of specialized reproductive and non-reproductive individuals that differentiate early in development, similar to germ–soma segregation in bilateral Metazoa. Analogous to diverging cell lines, developmental differentiation of individual ants has often been considered in epigenetic terms but the sets of genes that determine caste phenotypes throughout larval and pupal development remain unknown. Here, we reconstruct the individual developmental trajectories of two ant species, Monomorium pharaonis and Acromyrmex echinatior, after obtaining >1,400 whole-genome transcriptomes. Using a new backward prediction algorithm, we show that caste phenotypes can be accurately predicted by genome-wide transcriptome profiling. We find that caste differentiation is increasingly canalized from early development onwards, particularly in germline individuals (gynes/queens) and that the juvenile hormone signalling pathway plays a key role in this process by regulating body mass divergence between castes. We quantified gene-specific canalization levels and found that canalized genes with gyne/queen-biased expression were enriched for ovary and wing functions while canalized genes with worker-biased expression were enriched in brain and behavioural functions. Suppression in gyne larvae of Freja, a highly canalized gyne-biased ovary gene, disturbed pupal development by inducing non-adaptive intermediate phenotypes between gynes and workers. Our results are consistent with natural selection actively maintaining canalized caste phenotypes while securing robustness in the life cycle ontogeny of ant colonies.

U2 - 10.1038/s41559-022-01884-y

DO - 10.1038/s41559-022-01884-y

M3 - Journal article

C2 - 36192540

AN - SCOPUS:85139265641

VL - 6

SP - 1753

EP - 1765

JO - Nature Ecology & Evolution

JF - Nature Ecology & Evolution

SN - 2397-334X

IS - 11

ER -

ID: 322870716