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The royal food of termites shows king and queen specificity

Tasaki, Eisuke Mitaka, Yuki Takahashi, Yutaka Waliullah, A S M Tamannaa, Zinat Sakamoto, Takumi Islam, Ariful Kamiya, Masaki Sato, Tomohito Aramaki, Shuhei Kikushima, Kenji Horikawa, Makoto Nakamura, Katsumasa Kahyo, Tomoaki Takata, Mamoru Setou, Mitsutoshi Matsuura, Kenji 京都大学 DOI:10.1093/pnasnexus/pgad222

2023.07

概要

Society in eusocial insects is based on the reproductive division of labor, with a small number of reproductive individuals supported by a large number of non-reproductive individuals. Because inclusive fitness of all colony members depends on the survival and fertility of reproductive members, sterile members provide royals with special treatment. Here we show that termite kings and queens each receive special food of a different composition from workers. Sequential analysis of feeding processes demonstrated that workers exhibit discriminative trophallaxis, indicating their decision-making capacity in allocating food to the kings and queens. LC-MS/MS analyses of the stomodeal food and midgut contents revealed king- and queen-specific compounds including diacylglycerols and short-chain peptides. DESI-MSI analyses of ¹³C-labelled termites identified phosphatidylinositol and acetyl-L-carnitine in the royal food. Comparison of the digestive tract structure showed remarkable differences in the volume ratio of the midgut-to-hindgut among castes, indicating that digestive division of labor underlies reproductive division of labor. Our demonstration of king- and queen-specific food in termites provides insight into the nutritional system that underpins the extraordinary reproduction and longevity of royals in eusocial insects.

参考文献

Acknowledgments

The authors thank T. Ishibashi, M. Takahashi, and T. Inagaki, and

N. Idogawa, members of the laboratory of insect ecology, Kyoto

University, for their help during sample collection and filming

behavior. The authors thank M.T. Kamiyama for helpful com­

ments on the manuscript. They acknowledge the support provided

by the Foundation for Promotion of Material Science and

Technology of Japan (MST) in micro-CT measurement. They thank

F. Eto of the Department of Cellular and Molecular Anatomy,

Hamamatsu University School of Medicine, and E. Hiyama and

T. Harada of the Natural Science Center for Basic Research and

Development (N-BARD), Hiroshima University, for their technical

support in sample preparation and measurement of MS. The au­

thors also thank Y. Tokunaga and T. Kitamoto of the Advanced

Research Facilities and Services (ARFS), Hamamatsu University

School of Medicine, for their technical support in TEM and

LC-MS/MS measurements.

Supplementary material

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Supplementary material is available at PNAS Nexus online.

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Funding

This work was supported by the Japan Society for the Promotion of

Science (JSPS) KAKENHI Grant Numbers JP22K14830 (E.T.) and

JP18H05268 (K.M.).

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Author contributions

E.T., M.T., M.S., and K.M. designed the research; E.T., Y.M., Y.T.,

A.S.M.W., Z.T., T.S., A.I., M.K., T.S., S.A., K.K., M.H., K.N., T.K.,

15

Wilson EO. 1971. The insect societies. Cambridge, MA, USA:

Harvard University Press.

Hölldobler B, Wilson EO. 2009. The superorganism: the beauty, ele­

gance, and strangeness of insect societies. New York, NY, USA: WW

Norton & Company.

Fischman BJ, Woodard SH, Robinson GE. 2011. Molecular evolu­

tionary analyses of insect societies. Proc Natl Acad Sci U S A.

108(Suppl 2):10847–10854.

Keller L, Genoud M. 1997. Extraordinary lifespans in ants: a test

of evolutionary theories of ageing. Nature. 389:958–960.

Keller L. 1998. Queen lifespan and colony characteristics in ants

and termites. Insectes Soc. 45:235–246.

Rau V, Flatt T, Korb J. 2023. The remoulding of dietary effects on

the fecundity/longevity trade-off in a social insect. BMC Genomics.

24:244.

Melampy RM, Jones DB. 1939. Chemical composition and vitamin

content of royal jelly. Proc Soc Exp Biol Med. 41:382–388.

Pratt Jr JJ, House HL. 1949. A qualitative analysis of the amino

acids in royal jelly. Science. 110:9–10.

Barker SA, Foster AB, Lamb DC, Hodgson N. 1959. Identification

of 10-hydroxy-delta 2-decenoic acid in royal jelly. Nature. 183:

996–997.

Lercker G, Capella P, Conte LS, Ruini F, Giordani G. 1981.

Components of royal jelly: I. Identification of the organic acids.

Lipids. 16:912–919.

Schmitzová J, et al. 1998. A family of major royal jelly proteins of

the honeybee Apis mellifera L. Cell Mol Life Sci. 54:1020–1030.

Scarselli R, et al. 2005. Towards royal jelly proteome. Proteomics. 5:

769–776.

LeBoeuf AC, et al. 2019. Oral transfer of chemical cues, growth

proteins and hormones in social insects. Elife. 8:e51082.

Meurville M-P, LeBoeuf AC. 2021. Trophallaxis: the functions and

evolution of social fluid exchange in ant colonies (Hymenoptera:

Formicidae). Myrmecol News. 31:1–30.

Snir O, et al. 2022. The pupal moulting fluid has evolved social

functions in ants. Nature. 612:488–494.

Downloaded from https://academic.oup.com/pnasnexus/article/2/7/pgad222/7218884 by Kyoto University user on 14 July 2023

forceps. The trimmed digestive tracts were transferred with a

small amount of PBS into a Fuchs-Rosenthal chamber with a

depth of 0.2 mm (Erma), and still images were taken under a

microscope. If the digestive tract was damaged, measurement

was stopped and redone with a new sample. The crop, midgut,

pylorus (a small region at the junction of the midgut, hindgut,

and Malpighian tubules), hindgut, and rectum were distinguished,

and the areas of the midgut and hindgut were measured using the

image-analysis software ImageJ (v2.0.0-rc-69/1.53j). The volume

of each tissue was obtained by multiplying by the depth. These

measurements were repeated for 10 colonies (colonies K–T; Data

set S2 and Table S2). We performed micro-computed tomography

(micro-CT) analysis of the morphology of the digestive tracts of

the various castes (see Supplementary Methods).

12 |

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39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

54

55

56

57

58

59

very-long-chain fatty acids in mammalian testes and spermato­

zoa. J Biol Chem. 267:1746–1751.

Cross NL. 2000. Sphingomyelin modulates capacitation of hu­

man sperm in vitro. Biol Reprod. 63:1129–1134.

Schmelz EM, et al. 1996. Sphingomyelin consumption suppresses

aberrant colonic crypt foci and increases the proportion of aden­

omas versus adenocarcinomas in CF1 mice treated with 1, 2-di­

methylhydrazine: implications for dietary sphingolipids and

colon carcinogenesis. Cancer Res. 56:4936–4941.

Vesper H, et al. 1999. Sphingolipids in food and the emerging im­

portance of sphingolipids to nutrition. J Nutr. 129:1239–1250.

Jiang C, et al. 2022. Dietary sphingomyelin metabolism and roles

in gut health and cognitive development. Adv Nutr. 13:474–491.

Inagaki T, Matsuura K. 2016. Colony-dependent sex differences

in protozoan communities of the lower termite Reticulitermes

speratus (Isoptera: Rhinotermitidae). Ecol Res. 31:749–755.

Hakala SM, et al. 2023. Socially transferred materials: why and

how to study them. Trends Ecol Evol. 38:446–458.

Negroni M, LeBoeuf A. 2023. Metabolic division of labor in social

insects. EcoEvoRxiv X26C7X. https://doi.org/10.32942/X26C7X,

preprint: not peer reviewed.

Ramanathan ANKG, Nair AJ, Sugunan VS. 2018. A review on royal

jelly proteins and peptides. J Funct Foods. 44:255–264.

Matsuura K, Nishida T. 2001. Comparison of colony foundation

success between sexual pairs and female asexual units in the

termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul

Ecol. 43:119–124.

Mitaka Y, Akino T, Matsuura K. 2023. Development of a standard

medium for culturing the termite Reticulitermes speratus. Insectes

Soc. 70:265–274.

Okuda S, et al. 2017. jPOSTrepo: an international standard data

repository for proteomes. Nucleic Acids Res. 45:D1107–D1111.

Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new gen­

eration of protein database search programs. Nucleic Acids Res. 25:

3389–3402.

Schäffer AA, et al. 2001. Improving the accuracy of PSI-BLAST

protein database searches with composition-based statistics

and other refinements. Nucleic Acids Res. 29:2994–3005.

Grabherr MG, et al. 2011. Full-length transcriptome assembly

from RNA-Seq data without a reference genome. Nat Biotechnol.

29:644–652.

Haas BJ, et al. 2013. De novo transcript sequence reconstruction

from RNA-seq using the Trinity platform for reference gener­

ation and analysis. Nat Protoc. 8:1494–1512.

Wilkins MR, et al. 1997. Detailed peptide characterization using

PEPTIDEMASS–a world-wide-web-accessible tool. Electrophoresis.

18:403–408.

Gasteiger E, et al. 2005. Protein identification and analysis tools

on the ExPASy server. In: Walker JM, editor. The proteomics proto­

cols handbook. Totowa, NJ, USA: Humana Press Inc. p. 571–607.

Sun C, Wang F, Zhang Y, Yu J, Wang X. 2020. Mass spectrometry

imaging-based metabolomics to visualize the spatially resolved

reprogramming of carnitine metabolism in breast cancer.

Theranostics. 10:7070–7082.

van der Hooft JJJ, Ridder L, Barrett MP, Burgess KEV. 2015.

Enhanced acylcarnitine annotation in high-resolution mass

spectrometry data: fragmentation analysis for the classification

and annotation of acylcarnitines. Front Bioeng Biotechnol. 3:26.

Weesner FM. 1969. External anatomy. Biol Termites. 1:19–47.

Zimet M, Stuart AM. 1982. Sexual dimorphism in the immature

stages of the termite, Reticulitermes flavipes (Isoptera:

Rhinotermitidae). Sociobiology. 7:1–7.

Downloaded from https://academic.oup.com/pnasnexus/article/2/7/pgad222/7218884 by Kyoto University user on 14 July 2023

16 Beetsma J. 1979. The process of queen-worker differentiation in

the honeybee. Bee World. 60:24–39.

17 Kamakura M. 2011. Royalactin induces queen differentiation in

honeybees. Nature. 473:478–483.

18 Ratcliffe NA, Mello CB, Garcia ES, Butt TM, Azambuja P. 2011.

Insect natural products and processes: new treatments for hu­

man disease. Insect Biochem Mol Biol. 41:747–769.

19 Lo N, et al. 2000. Evidence from multiple gene sequences indi­

cates that termites evolved from wood-feeding cockroaches.

Curr Biol. 10:801–804.

20 Bignell DE, Eggleton P. 2000. Termites in ecosystems. In: Abe T,

Bignell DE, Higashi M, editors. Termites: evolution, sociality, symbi­

oses, ecology. Dordrecht, Netherlands: Springer Netherlands. p.

363–387.

21 Korb J. 2007. Termites. Curr Biol. 17:R995–R999.

22 Du H, Chouvenc T, Su N-Y. 2017. Development of age polyethism

with colony maturity in Coptotermes formosanus (Isoptera:

Rhinotermitidae). Environ Entomol. 46:311–318.

23 Cunnigham JT. 1894. The logic of Weismannism. Nature. 50:

523–524.

24 Matsuura K, et al. 2009. Queen succession through asexual repro­

duction in termites. Science. 323:1687.

25 Yashiro T, Matsuura K. 2014. Termite queens close the sperm

gates of eggs to switch from sexual to asexual reproduction.

Proc Natl Acad Sci U S A. 111:17212–17217.

26 Suárez ME, Thorne BL. 2000. Rate, amount, and distribution pat­

tern of alimentary fluid transfer via trophallaxis in three species

of termites (Isoptera: Rhinotermitidae, Termopsidae). Ann

Entomol Soc Am. 93:145–155.

27 Tokuda G, et al. 2014. Metabolomic profiling of 13C-labelled cel­

lulose digestion in a lower termite: insights into gut symbiont

function. Proc Biol Sci. 281:20140990.

28 Hagen TM, et al. 1998. Acetyl-L-carnitine fed to old rats partially

restores mitochondrial function and ambulatory activity. Proc

Natl Acad Sci U S A. 95:9562–9566.

29 Palermo V, Falcone C, Calvani M, Mazzoni C. 2010.

Acetyl-L-carnitine protects yeast cells from apoptosis and aging

and inhibits mitochondrial fission. Aging Cell. 9:570–579.

30 Brune A. 2014. Symbiotic digestion of lignocellulose in termite

guts. Nat Rev Microbiol. 12:168–180.

31 Roskens VA, Carpenter JM, Pickett KM, Ballif BA. 2010.

Preservation of field samples for enzymatic and proteomic char­

acterization: analysis of proteins from the trophallactic fluid of

hornets and yellowjackets. J Proteome Res. 9:5484–5491.

32 Matsuura K. 2017. Evolution of the asexual queen succession sys­

tem and its underlying mechanisms in termites. J Exp Biol. 220:

63–72.

33 Postlethwait JH, Giorgi F. 1985. Vitellogenesis in insects. Dev Biol.

1:85–126.

34 Beenakkers AM, Van der Horst DJ, Van Marrewijk WJ. 1985. Insect

lipids and lipoproteins, and their role in physiological processes.

Prog Lipid Res. 24:19–67.

35 Turunen S, Crailsheim K. 1996. Lipid and sugar absorption. In:

Lehane MJ, Billingsley PF, editors. Biology of the insect midgut.

Dordrecht, Netherlands: Springer Netherlands. p. 293–320.

36 Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA. 2001.

Fat metabolism in insects. Annu Rev Nutr. 21:23–46.

37 Séité S, et al. 2022. Lifespan prolonging mechanisms and insulin

upregulation without fat accumulation in long-lived reproduc­

tives of a higher termite. Commun Biol. 5:44.

38 Robinson BS, Johnson DW, Poulos A. 1992. Novel molecular spe­

cies of sphingomyelin containing 2-hydroxylated polyenoic

...

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