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
10
Supplementary material is available at PNAS Nexus online.
11
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
...