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The pigment transporter Redboy confers programmed body colour transition in orchid mantises

Nature Ecology & Evolution volume 9, pages 1120–1137 (2025)Cite this article

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Abstract

Programmed phenotypic transition is prevalent throughout the tree of life, yet the concrete mechanisms that underpin this phenomenon are poorly understood. The orchid mantis (Hymenopus coronatus, Mantodea) is a model study system for programmed body colour transitions that displays a prominent black-red body colour in first-instar nymphs, then switches to a flowery white body colour in later-instar nymphs. Here we reveal that this body colour transition is achieved by the simultaneous excretion of decarboxylated-xanthommatin (red pigment) and the accumulation of uric acid (white pigment) in the epidermis during the first moult. This change in pigmentation is associated with a novel subtype of ABCG pigment transporter that we call ‘Redboy’ in Polyneoptera, which is upregulated by insect steroid hormone (ecdysone) during the first moult of orchid mantises. RNAi assay and pigment analyses show that Redboy functions together with the co-transporter White, exporting red pigments from and concurrently importing white pigments into the epidermal cells. Spectral reflectance analyses and predation experiments reveal that Redboy-conferred programmed body colour transition enhances predator avoidance during the first instar, and both prey attraction and predator avoidance in later instars. Our findings clarify how gene family evolution and hormone regulation coordinate programmed phenotypic transition and promote ecological adaptation in orchid mantises.

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Fig. 1: Programmed body colour transition in orchid mantis nymphs.
Fig. 2: Identification and tracking of pigments involved in programmed body colour transition.
Fig. 3: Gene family expansion and positive selection generate a novel subtype of ABCG pigment transporter, Redboy, in Polyneoptera.
Fig. 4: Ecdysone-induced Redboy confers body coloration and programmed body colour transition.
Fig. 5: Redboy-conferred programmed body colour transition enhances mimicry-camouflage shift.
Fig. 6: Genetics and evolution of Redboy in programmed body colour transition and its ecological significance.

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Data availability

Sanger sequencing verified mRNA sequences have been submitted to GenBank database (OR571863–OR571871). Genomic, transcriptomic and Hi-C sequencing data used in our study are submitted to the National Genomics Data Center (https://www.cncb.ac.cn/) with project number PRJCA019827. The genome assembly data are available from the Genome Warehouse with accession number GWHDUCZ00000000. The raw data of PacBio (CRX794670), Illumina (CRX794672), Hi-C (CRX794671) and RNA-seq (CRX794645–CRX794669) are available in the Genome Sequence Archive. Source data are provided with this paper.

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Acknowledgements

We greatly appreciate K. Kjer for polishing and improving this manuscript. We thank S. Z. Zhang from Northwest A & F University for his help in pigments analysis. This work was supported by the National Natural Science Foundation of China (grant number 32220103003, 31930014 to S.L., 32325009, 32170420 to W.Z., 32200384 to X.-J.P. and 32170425 to Y.-X.L), the Laboratory of Lingnan Modern Agriculture Project (grant number NT2021003 to S.L. and X.-X.C.), the Department of Science and Technology in Guangdong Province (grant number 2019B090905003 to S.L.), the Shenzhen Science and Technology Program (grant number KQTD20180411143628272 to S.L.), the China Postdoctoral Science Foundation (grant number 2022M710053 to X.-J.P.), the Guangdong Basic and Applied Basic Research Foundation (grant number 2025A1515012479 to X.-J.P.), and by grants from Benyuan Charity Young Investigator Exploration Fellowship in Life Science, The Feng Foundation of Biomedical Research, the Peking-Tsinghua Center for Life Sciences and the State Key Laboratory of Gene Function and Modulation to W.Z.

Author information

Author notes

  1. These authors contributed equally: Xiao-Jin Pei, Dong Zhao.

Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Guangzhou Key Laboratory of Insect Development Regulation and Application Research, Institute of Insect Science and Technology, School of Life Sciences, South China Normal University, Guangzhou, China

    Xiao-Jin Pei, Jie Luo, Pei-Yao Jia, Yuan Luo, Dong-Wei Yuan, Wen-Xin Hou, Dan-Yan Huang, Yun-Xia Luan & Sheng Li

  2. Guangmeiyuan R&D Center, Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou, China

    Xiao-Jin Pei, Dong-Wei Yuan, Yun-Xia Luan & Sheng Li

  3. Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China

    Xiao-Jin Pei, Xue-Xin Chen & Sheng Li

  4. State Key Laboratory of Gene Function and Modulation Research, School of Life Sciences, Peking University, Beijing, China

    Dong Zhao, Jia-Xin Ni, Hui-Ze Gao & Wei Zhang

  5. Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China

    Dong Zhao, Jia-Xin Ni, Hui-Ze Gao & Wei Zhang

  6. State Key Laboratory of Crop Stress Biology for Arid Areas and Key Laboratory of Integrated Pest Management on Crops in Northwestern Loess Plateau, Ministry of Agriculture and Rural Affairs, Northwest A&F University, Yangling, People’s Republic of China

    Zhan-Feng Zhang

  7. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Yunnan, China

    Zhanqi Chen

  8. Ministry of Agriculture and Rural Affairs Key Lab of Molecular Biology of Crop Pathogens and Insect Pests, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of insect Sciences, Zhejiang University, Hangzhou, China

    Xue-Xin Chen

  9. Institute of Ecology, Peking University, Beijing, China

    Wei Zhang

  10. Institute for Tibetan Plateau Research, Peking University, Beijing, China

    Wei Zhang

  11. Medog Biodiversity Observation and Research Station of Xizang Autonomous Region, Nyingchi, China

    Wei Zhang

Authors
  1. Xiao-Jin Pei
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  2. Dong Zhao
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Contributions

S.L., X.-J.P., W.Z. and X.-X.C. conceptualized the study. S.L., W.Z., X.-X.C. X.-J.P. and Y.-X.L. acquired the funding. X.-J.P., D.Z., J.L., P.-Y.J., Y.L., W.-X.H., Z.-F.Z., D.-Y.H., J.-X.N., H.-Z.G., Z.C. and Y.-X.L. carried out the investigation and curated the data. X.-J.P., D.Z. and J.L. visualized the data. X.-J.P. and D.Z. wrote the original paper. All authors reviewed and edited the paper. S.L., W.Z. and X.-X.C. supervised the study.

Corresponding authors

Correspondence to Xue-Xin Chen, Wei Zhang or Sheng Li.

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Nature Ecology & Evolution thanks Ryo Futahashi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Identification of melanin and ommochrome in first-instar nymphs.

a, Exuviae generated during the first moult. AC: abdominal cuticle, TC: thoracic cuticle. b,c,d,e,f, Relative expression of melanin synthesis genes (TH: tyrosine hydroxylase, DDC: dopa decarboxylase, ebony: N-β-alanyldopamine synthase, Tan: N-β-alanyldopamine hydrolase, and aaNAT: arylalkylamine-N-acetyltransferase) in various body parts in late embryos. Different letters indicate statistically significant differences between groups (Welch’s ANOVA, Games–Howell multiple comparisons test, P < 0.05, n = 4 biological replicates). g, Kr-h1 is highly expressed around hatching. n = 3 or 4 biological replicates. h,i, Phenotypic effects of DDC- and aaNAT-RNAi in fourth-instar nymphs. DDC knock-down lightens color of tibial end in higher-instar nymphs, while aaNAT inhibition darkens color of several cuticle parts. j,j’,j”, Relative expression of ommochrome synthesis genes including Ver, KFase, and KMO expression in different regions at ED35, Welch’s ANOVA, Games–Howell multiple comparisons test, different letters indicate significant differences between groups, P < 0.05, n = 4 biological replicates. k,k’,k”, Tertiary mass spectrometry of the red pigment (DX). k, Primary mass spectrometry identifies a high-abundance molecule with a molecular ion of m/z = 380, identified as molecular ion of DX, k’, Secondary mass spectrometry detects two ion fragments with m/z of 363 and 307, k”, further fracture analysis of ions with m/z of 363 generates two fragments with m/z of 345 and 317. The break of ion fragments is shown by dotted lines, removed groups is represented by red fonts. Data in b–g and j–j” are mean ± s.e.m. Individuals are represented by dots in b–f and j–j”. All statistical tests are two-tailed. Source data are provided in Source Data Extended Data Fig. 1.

Source data.

Extended Data Fig. 2 Genome analyses and gene family studies in the orchid mantis.

a, Chromosomes of Hymenopus coronatus in the testis cell from sixth-instar nymphs. Twenty-one chromosomes (2n = 42) present at spermatogonial metaphase. b, Genome-wide contact matrix from Hi-C data between all chromosomes. c, Venn plot of gene functional annotation in five databases of the orchid mantis. d, Genomic landscapes of H. coronatus. Denotation of each track listed on the left bottom of the circos plot. e, Genome size analyses of various insects from different orders. Each dot represents one species. f, Phylogeny and subfamily identification of ABC transporters from H. coronatus, D. melanogaster, and B. mori. g, Phylogenetic tree using representative ABCGpt sequences. Divergence times of each subtype and proteins calculated and shown as thick orange lines. h, Chromosomal localization of ABCG transporter genes in the orchid mantis. i, Detailed gene structure of White, Scarlet, Brown, and Redboy in the orchid mantis showing exon arrangement. j, Volcano plot represents the Log2 fold change (N2D0/N1D3) for each gene expression and the corresponding Log10 (p-value). Up-regulated ABCG pigment transporter genes labeled with red dots and black font, P values were calculated from 3 biological replicates using two-tailed Student t-test. Source data are provided in Source Data Extended Data Fig. 2.

Source data.

Extended Data Fig. 3 Screen of ABCG genes involved in body color transition in the orchid mantis.

a,b, Relative expression level of ABCG transporter genes in the integument (a) or Malpighian tubules of N2D0 mantises (b). Data are shown as mean ± s.e.m. Different letters indicate statistically significant differences between groups using Welch ANOVA (Games–Howell multiple comparisons test, P < 0.05, n = 4 biological replicates), all statistical tests are two-tailed. c, Influence of repressing highly expressed ABCG genes (ABCGpt gene are not included) on body color of the orchid mantis. d,e Relative expression of ecdysone synthesis (d) and response (e) genes. Data are shown as mean ± s.e.m, three biological replicates. Source data are provided in Source Data Extended Data Fig. 3.

Source data.

Extended Data Fig. 4 Functional studies of different ABCGpt genes in programmed body colour transition.

a, Effect of repression different ABCG pigment transporter (ABCGpt) genes on the fading of red pigments during the first moult. b, Relative expression of different ABCGpt genes in the abdominal cuticle (AC), fat body (FB), head, Malpighian tubule (MT), gut, leg, and thorax of N2D0 mantises. Data are shown as mean ± SEM, different letters indicate statistically significant differences between groups using Welch’s ANOVA (Games–Howell multiple comparisons test, P < 0.05, n = 4 biological replicates, individuals are represented by dots), all statistical tests are two-tailed. c, Fluorescence in situ hybridization of Redboy in the integument of early fourth-instar nymphs. The four diagrams in the upper left corner represent DAPI (blue), FITC (green), bright field and superposition diagram respectively. The four diagrams showcases in the lower left corner correspond to enlarged pictures. The green fluorescence signal in the dsMuslta sample disappeared in the right Redboy-RNAi samples, suggesting that the green signal represents Redboy mRNA. Notably, the signal in the epidermis is a non-specific signal of chitin in the cuticle. d, DX injected into the haemolymph is normally excreted into the MT after the knock-down of Brown. e, Inhibition of Brown or White causes the yellow pigment in the MT to disappear. f, Influence of inhibition different ABCGpt genes using the second RNAi targets on the body color of fourth-instar nymphs. Source data are provided in Source Data Extended Data Fig. 4.

Source data.

Extended Data Fig. 5 Supplementary results regarding the spectral reflectance and color contrast.

a, Color contrast (just noticeable difference, JND) between forth-instar orchid mantises and various flowers as perceived by the butterfly Pieris rapae, or the bird Cyanistes caeruleus and Pavo cristatus. The gray box plot represents the contrast between the WT orchid mantis (n = 10) and the flowers (J. sambac: n = 10, C. sinensis: n = 5, G. jasminoides: n = 10), while the purple box plot represents the contrast between the Redboy-RNAi orchid mantis (n = 9) and flowers. Color contrast values ≤ 3 indicate low discriminability of the colours for a given visual system (dashed line = 3). solid box plot: achromatic contrast, hollow box plot: chromatic contrast, and also for subsequent representation. b, Examination of color contrast between second-instar WT (black box plot, n = 10) or Redboy-RNAi (red box plot, n = 10) orchid mantises and various flowers from perspectives of the butterfly P. rapae and bird C. caeruleus. These data were also illustrated by spectral reflectance (mean ± S.E.). c, Color contrast between the flower model (n = 10) and real flowers from the perspective of the butterfly P. rapae or the peacock P. cristatus. Box plots depict the median, upper and lower quartiles, and maxima and minima; dots indicate outliers. *P < 0.05; **P < 0.01; ***P < 0.001, each test have been repeated for more than 3 times. Source data are provided in Source Data Extended Data Fig. 5. We chose one of Kruskal‒Wallis test, One-way ANOVA and Welch’s ANOVA according to the data normality and variance heterogeneity in statistics, and the results are provided in Supplementary Table 3.

Source data.

Extended Data Fig. 6 Initial choice behavior and position effects in Fig. 5d-f experiments.

a, The untrained spider P. labiata (n = 25) showed no initial orient preference between blackened/unblackened mantises, while trained spiders (n = 23) preferred blackened mantises. The relative positions of the praying mantis had no effect on the results. a’, The attention duration is not affected by the positions of the mantis. b, The first approach of untrained (n = 30) or black flower model trained Pieris rapae (n = 18) showed no preference between Redboy-RNAi and wild-type (WT) orchid mantises, while white flower model trained butterflies exhibit significant preference to WT orchid mantises (n = 16). This preference was irrelevant with the positions of the mantis. b’ The total number of approaches of trained or untrained butterflies show no relevant with the positions of the mantis. c, The number of chicks trying the flower model gradually decreased with the training, suggesting the effectiveness of the training. c’, Untrained chicks (n = 8) showed no initial attack preference, while white/black-flower-trained chicks (each n = 12) preferred Redboy-RNAi orchid mantises. This preference was irrelevant with the positions of the orchid mantis. c”, The total number of attacks of trained or untrained butterflies show no relevant with the positions of the orchid mantis. Box plots depict the median, upper and lower quartiles, and maximum and minimum values, with outliers represented by dots. *P < 0.05; **P < 0.01; ***P < 0.001. Source data are provided in Source Data Extended Data Fig. 5. a’, LMM statistical results are provided in Supplementary Table 4. b’ and c”, LMM statistical results are provided in Supplementary Table 5. a, b, and c’, GLMM statistical results are provided in Supplementary Table 6. c, Kruskal‒Wallis test or One-way ANOVA statistical results are provided in Supplementary Table 7.

Extended Data Fig. 7 Field observations of first- or fifth-instar orchid mantises.

a, The first-instar orchid mantis exhibits body colours reminiscent of various local bugs. b, The fifth-instar orchid mantis resembles local white flower blossoms. c, Mantises in the same habitat typically display a cryptic green or gray body color.

Supplementary information

Supplementary Information

Supplementary Tables 1–8.

Reporting Summary

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Supplementary Video 1

The first-instar orchid mantis hides behind leaves and jumps to escape from the predator (an ant).

Supplementary Video 2

The body colour of higher-instar orchid mantis nymphs can confuse bees.

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Pei, XJ., Zhao, D., Luo, J. et al. The pigment transporter Redboy confers programmed body colour transition in orchid mantises. Nat Ecol Evol 9, 1120–1137 (2025). https://doi.org/10.1038/s41559-025-02737-0

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