Canalized gene expression during development mediates caste differentiation in ants

Bitao Qiu*, Xueqin Dai, Panyi Li, Rasmus Stenbak Larsen, Ruyan Li, Alivia Lee Price, Guo Ding, Michael James Texada, Xiafang Zhang, Dashuang Zuo, Qionghua Gao, Wei Jiang, Tinggang Wen, Luigi Pontieri, Chunxue Guo, Kim Rewitz, Qiye Li, Weiwei Liu, Jacobus J. Boomsma, Guojie Zhang

*Corresponding author for this work

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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.

Original languageEnglish
JournalNature Ecology and Evolution
Volume6
Issue number11
Pages (from-to)1753-1765
ISSN2397-334X
DOIs
Publication statusPublished - 2022

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