リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Discovery of an underground chamber to protect kings and queens during winter in temperate termites」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Discovery of an underground chamber to protect kings and queens during winter in temperate termites

Takata, Mamoru Konishi, Takao Nagai, Shuya Wu, Yao Nozaki, Tomonari Tasaki, Eisuke Matsuura, Kenji 京都大学 DOI:10.1038/s41598-023-36035-1

2023.05.31

概要

Overwintering is a critical part of the annual cycle for species that live in temperate, polar, and alpine regions. Consequently, low-temperature biology is a key determinant of temperate species distribution. Termites are distributed predominantly in tropical regions, and a limited number of species are found in the temperate zone. Here, in the termite Reticulitermes speratus, we report the discovery of an underground chamber that protects kings and queens to survive the winter, which is separate from the one they used during the warmer breeding season. In the spring, the royals inhabited decayed logs on the ground, then moved to their underground chamber located in the roots of stumps in the fall. The winter minimum temperature measured in the royal chamber was higher than that in the logs on the ground. In overwintering termites, the kings and queens had higher cold tolerance than workers and soldiers. Air temperatures dropped below the critical temperature multiple times, as evidenced from the past 140 years of weather records in Kyoto. These results demonstrated the survival strategies of reproductives to overcome the environment at the latitudinal limits. This study helps further the understanding of the termite’s seasonal phenology, long-term survivorship, and life cycle.

この論文で使われている画像

参考文献

1. Doucet, D., Walker, V. K. & Qin, W. The bugs that came in from the cold: Molecular adaptations to low temperatures in insects.

Cell. Mol. Life Sci. 66, 1404–1418 (2009).

2. Kokou, F. et al. Host genetic selection for cold tolerance shapes microbiome composition and modulates its response to temperature.

Elife 7, 1–21 (2018).

3. Kingsolver, J. G. & Huey, R. B. Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. Am. Zool. 38, 323–336 (1998).

4. Huey, R. B., Hertz, P. E. & Sinervo, B. Behavioral drive versus behavioral inertia in evolution: A null model approach. Am. Nat.

161, 357–366 (2003).

5. Huey, R. B. Evolutionary physiology of insect thermal adaptation to cold environments. In Low Temperature Biology of Insects (eds

Denlinger, D. L. & Lee, R. E. J.) 223–241 (Cambridge University Press, 2010). https://​doi.​org/​10.​1017/​CBO97​80511​675997.​010.

6. Danks, H. V. Insect adaptations to cold and changing environments. Can. Entomol. 138, 1–23 (2006).

7. Clark, M. S. & Worland, M. R. How insects survive the cold: Molecular mechanisms—A review. J. Comp. Physiol. B 178, 917–933

(2008).

8. Lee, R. E. J. Insect cold-hardiness: To freeze or not to freeze. Bioscience 39, 308–313 (1989).

9. Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects (Princeton University Press, 1978).

Scientific Reports |

Vol:.(1234567890)

(2023) 13:8809 |

https://doi.org/10.1038/s41598-023-36035-1

www.nature.com/scientificreports/

10. Robinson, G. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665 (1992).

11. Wilson, E. O. The Insect Societies (Belknap Press, 1971).

12. Crespi, B. J. & Yanega, D. The definition of eusociality. Behav. Ecol. 6, 109–115 (1995).

13. Bourke, A. F. G. Kin selection and the evolutionary theory of aging. Annu. Rev. Ecol. Evol. Syst. 38, 103–128 (2007).

14. Tasaki, E., Takata, M. & Matsuura, K. Why and how do termite kings and queens live so long?. Philos. Trans. R. Soc. B Biol. Sci.

376, 20190740 (2021).

15. Hansell, M. H. Animal Architecture (Oxford University Press, 2005).

16. Hughes, D. P., Pierce, N. E. & Boomsma, J. J. Social insect symbionts: Evolution in homeostatic fortresses. Trends Ecol. Evol. 23,

672–677 (2008).

17. Evans, T. A., Forschler, B. T. & Grace, J. K. Biology of invasive termites: A worldwide review. Annu. Rev. Entomol. 58, 455–474

(2013).

18. Eggleton, P. Global patterns of termite diversity. In Termites, Evolution, Sociality, Symbioses, Ecology (eds Abe, T. et al.) 25–51

(Springer, 2000).

19. Emerson, A. E. Geographic origins and dispersion of termite genera. Fieldiana Zool. 37, 465–521 (1955).

20. Eggleton, P., Williams, P. H. & Gaston, K. J. Explaining global termite diversity: Productivity or history?. Biodivers. Conserv. 3,

318–330 (1994).

21. Kofoid, C. A. Climate factors affecting the local occurrence of termite and their geographical distribution. In Termites and Termite

Control (ed. Kofoid, C. A.) 13–21 (University of California Press, 1934).

22. Matsuura, K. et al. Queen succession through asexual reproduction in termites. Science 323, 1687–1687 (2009).

23. Park, Y. C., Kitade, O., Schwarz, M., Kim, J. P. & Kim, W. Intraspecific molecular phylogeny, genetic variation and phylogeography

of Reticulitermes speratus (Isoptera: Rhinotermitidae). Mol. Cells 21, 89–103 (2006).

24. Takematsu, Y. The genus Reticulitermes (Isoptera: Rhinotermitidae) in Japan, with description of a new species. Entomol. Sci. 2,

231–243 (1999).

25. Abe, T. Evolution of life types in termites. In Evolution and Coadaptation in Biotic Communities (eds Kawano, S. et al.) 125–148

(University of Tokyo Press, 1987).

26. Shellman-Reeve, J. S. The spectrum of eusociality in termites. In Evolution of Social Behavior in Insects and Arachnids (eds Choe,

J. C. & Crespi, B. J.) 52–93 (Cambridge University Press, 1997).

27. Tsunoda, K., Matsuoka, H., Yoshimura, T. & Tokoro, M. Foraging populations and territories of Reticulitermes speratus (Isoptera:

Rhinotermitidae). J. Econ. Entomol. 92, 604–609 (1999).

28. Matsuura, K. et al. A genomic imprinting model of termite caste determination: Not genetic but epigenetic inheritance influences

offspring caste fate. Am. Nat. 191, 677–690 (2018).

29. Takata, M. et al. Heritable effects on caste determination and colony-level sex allocation in termites under field conditions. iScience

26, 106207 (2023).

30. Tasaki, E., Komagata, Y., Inagaki, T. & Matsuura, K. Reproduction deep inside wood: A low O

­ 2 and high C

­ O2 environment promotes

egg production by termite queens. Biol. Lett. 16, 20200049 (2020).

31. Yanagihara, S., Suehiro, W., Mitaka, Y. & Matsuura, K. Age-based soldier polyethism: Old termite soldiers take more risks than

young soldiers. Biol. Lett. 14, 20180025 (2018).

32. The Japan Meteorological Agency (2023). Available at: http://​www.​jma.​go.​jp/​jma/​indexe.​html.

33. Matsuura, K., Kobayashi, N. & Yashiro, T. Seasonal patterns of egg production in field colonies of the termite Reticulitermes speratus

(Isoptera: Rhinotermitidae). Popul. Ecol. 49, 179–183 (2007).

34. Nozaki, T. & Matsuura, K. Oocyte resorption in termite queens: Seasonal dynamics and controlling factors. J. Insect Physiol. 131,

104242 (2021).

35. Denlinger, D. L. & Lee, R. E. Physiology of cold sensitivity. In Temperature Sensitivity in Insects and Application in Integrated Pest

Management (eds Hallman, G. J. & Denlinger, D. L.) 55–96 (CRC Press, 1998).

36. Esenther, G. R. Termites in Wisconsin. Ann. Entomol. Soc. Am. 62, 1274–1284 (1969).

37. Hu, X. P. & Song, D. Behavioral responses of two subterranean termite species (Isoptera: Rhinotermitidae) to instant freezing or

chilling temperatures. Environ. Entomol. 36, 1450–1456 (2007).

38. Noirot, C. & Darlington, J. P. E. C. Termite nests: Architecture, regulation and defence. In Termites: Evolution, Sociality, Symbioses,

Ecology (eds Abe, T. et al.) 121–139 (Springer, 2000).

39. Miller, L. R. Nests and queen migration in Schedorhinotermes actuosus (Hill), Schedorhinotermes breinli (Hill) and Coptotermes

acinaciformis (Froggatt) (Isoptera: Rhinotermitidae). Aust. J. Entomol. 33, 317–318 (1994).

40. Camazine, S. et al. Self-Organization in Biological Systems (Princeton University Press, 2001).

41. Perna, A. & Theraulaz, G. When social behaviour is moulded in clay: On growth and form of social insect nests. J. Exp. Biol. 220,

83–91 (2017).

42. Theraulaz, G. & Bonabeau, E. Coordination in distributed building. Science 269, 686–688 (1995).

43. Konishi, T. & Matsuura, K. Royal presence promotes worker and soldier aggression against non-nestmates in termites. Insectes

Soc. 68, 15–21 (2021).

44. Crowe, J. H., Crowe, L. M. & Chapman, D. Preservation of membranes in anhydrobiotic organisms: The role of trehalose. Science

223, 701–703 (1984).

45. Storey, K. B. & Storey, J. M. Biochemistry of cryoprotectants. In Insects at low temperature (eds Lee, R. E. & Dennlinger, D. L.)

64–93 (Springer, 1991). https://​doi.​org/​10.​1007/​978-1-​4757-​0190-6_4.

46. Overgaard, J. et al. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J. Insect Physiol. 53,

1218–1232 (2007).

47. Lacey, M. J., Lenz, M. & Evans, T. A. Cryoprotection in dampwood termites (Termopsidae, Isoptera). J. Insect Physiol. 56, 1–7

(2010).

48. Husseneder, C. Symbiosis in subterranean termites: A review of insights from molecular studies. Environ. Entomol. 39, 378–388

(2010).

49. Brune, A. & Dietrich, C. The gut microbiota of termites: Digesting the diversity in the light of ecology and evolution. Annu. Rev.

Microbiol. 69, 145–166 (2015).

50. Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168–180 (2014).

51. Cabrera, B. J. & Kamble, S. T. Supercooling differences in the eastern subterranean termite (Isoptera: Rhinotermitidae). J. Entomol.

Sci. 39, 525–536 (2004).

52. Inagaki, T. & Matsuura, K. Colony-dependent sex differences in protozoan communities of the lower termite Reticulitermes speratus

(Isoptera: Rhinotermitidae). Ecol. Res. 31, 749–755 (2016).

53. Lewis, J. L. & Forschler, B. T. Protist communities from four castes and three species of Reticulitermes (Isoptera: Rhinotermitidae).

Ann. Entomol. Soc. Am. 97, 1242–1251 (2004).

54. Cook, T. C. & Gold, R. E. Organization of the symbiotic flagellate community in three castes of the eastern subterranean termite,

Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 31, 25–39 (1998).

55. Benjamino, J. & Graf, J. Characterization of the core and caste-specific microbiota in the termite, Reticulitermes flavipes. Front.

Microbiol. 7, 1–14 (2016).

Scientific Reports |

(2023) 13:8809 |

https://doi.org/10.1038/s41598-023-36035-1

Vol.:(0123456789)

www.nature.com/scientificreports/

56. Yashiro, T. & Matsuura, K. Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction. Proc. Natl.

Acad. Sci. 111, 17212–17217 (2014).

57. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).

Acknowledgements

We thank Kiyotaka Yabe, Ryoga Otake, and Matthew Tatsuo Kamiyama for the fruitful discussion, and Michihiko Takahashi, Yuto Morita, and Tomohiro Nakazono for assistance in collecting termites. This work was supported by JSPS KAKENHI grant numbers JP18H05268, JP20K20380, JP20J15697, JP20J20278, JP21K14863,

and JP23H00332.

Author contributions

M.T. and K.M. designed experiments. All authors contributed to collecting termites. M.T., T.K., and E.T. performed experiments. M.T. and K.M. wrote the manuscript, and all authors are accountable for the content and

approved the final version of the manuscript.

Competing interests The authors declare no competing interests.

Additional information

Supplementary Information The online version contains supplementary material available at https://​doi.​org/​

10.​1038/​s41598-​023-​36035-1.

Correspondence and requests for materials should be addressed to M.T.

Reprints and permissions information is available at www.nature.com/reprints.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and

institutional affiliations.

Open Access This article is licensed under a Creative Commons Attribution 4.0 International

License, which permits use, sharing, adaptation, distribution and reproduction in any medium or

format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the

Creative Commons licence, and indicate if changes were made. The images or other third party material in this

article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the

material. If material is not included in the article’s Creative Commons licence and your intended use is not

permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from

the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.

© The Author(s) 2023

Scientific Reports |

Vol:.(1234567890)

(2023) 13:8809 |

https://doi.org/10.1038/s41598-023-36035-1

10

...

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る