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Social dominance modifies behavioral rhythm in a queenless ant

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Abstract

Social insects provide an intriguing model system in chronobiology. Typically, an egg-laying queen exhibits arrhythmicity in activity while foraging worker has clear rhythmicity. In the queenless ant, Diacamma sp., from Japan, colony members lack morphological caste, and reproductive differentiation occurs as a consequence of dominance hierarchy formation. Their specialized dominance interaction “gemmae mutilation”, provide us a fascinating model system to investigate the effect of social dominance on rhythmic ontogeny. Measurement of individual rhythms revealed that they have clear circadian rhythm at eclosion but it is diminished by social mutilation of gemmae. Moreover, unlike highly eusocial species, mated egg-layer (i.e., gamergate) possessed a circadian rhythm even after mating in Diacamma. Measurement of colony-level rhythms revealed that gemmae mutilations are performed in the limited time of the day, but foraging occurs around-the-clock. The above finding is a novel form of temporal organization in social insects, providing a new insight in morphologically casteless species. We discuss the causes and consequences of rhythmic variability in social organization.

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References

  • Allard D, Ito F, Gobin B, Tsuji K, Billen J (2005) Differentiation of the reproductive tract between dominant and subordinate workers in the Japanese queenless ant Diacamma sp. Acta Zool 86:159–166

    Article  Google Scholar 

  • Baratte S, Cobb M, Peeters C (2006a) Reproductive conflicts and mutilation in queenless Diacamma ants. Anim Behav 72:305–311

    Article  Google Scholar 

  • Baratte S, Peeters C, Deutsch JS (2006b) Testing homology with morphology, development and gene expression: sex-specific thoracic appendages of the ant Diacamma. Evol Dev 8:433–445

    Article  PubMed  CAS  Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic, London

    Google Scholar 

  • Bloch G (2009) Plasticity in the circadian clock and the temporal organization of insect societies. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, pp 402–432

    Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton

    Google Scholar 

  • Eban-Rothschild A, Bloch G (2012) Circadian rhythms and sleep in honey bees. In Honeybee neurobiology and behavior. Springer, Netherlands, p 31–45

  • Eban-Rothschild A, Belluci S, Bloch G (2011) Maternity-related plasticity in circadian rhythms of bumble-bee queens. Proc R Soc B 278:3510–3516

    Article  PubMed  PubMed Central  Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Ann Rev Entomol 30:319–343

    Article  Google Scholar 

  • Fukumoto Y, Abe T, Taki A (1989) A novel form of colony organization in the "queenless" ant Diacamma rugosum. Physiol Ecol Jpn 26:55–61

    Google Scholar 

  • Gotoh A, Sameshima S, Tsuji K, Matsumoto T, Miura T (2005) Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae). Dev Genes Evol 215:69–77

    Article  PubMed  CAS  Google Scholar 

  • Gronenberg W, Peeters C (1993) Central projections of the sensory hairs on the gemma of the ant Diacamma: substrate for behavioural modulation? Cell Tissue Res 273:401–415

    Article  Google Scholar 

  • Harano K, Sasaki M, Sasaki K (2007) Effects of reproductive state on rhythmicity, locomotor activity and body weight in the European honeybee, Apis mellifera queens (Hymenoptera, Apini). Sociobiology 50:189–200

    Google Scholar 

  • Ingram KK, Krummey S, LeRoux M (2009) Expression patterns of a circadian clock gene are associated with age-related polyethism in harvester ants, Pogonomyrmex occidentalis. BMC Ecol 9:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Ito F, Higashi S (1991) Linear dominance hierarchy regulating reproduction and polyethism of the queenless ant Pachycondyla sublaevis. Naturwissenschaften 78:80–82

    Article  Google Scholar 

  • Johnson JN, Hardgrave E, Gill C, Moore D (2010) Absence of consistent diel rhythmicity in mated honey bee queen behavior. J Insect Physiol 56:761–773

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi T, Nakagawa T, Tsuji K (2008) Changes in relative importance of multiple social regulatory forces with colony size in the ant Diacamma sp from Japan. Anim Behav 76:2069–2077

    Article  Google Scholar 

  • Loros JJ, Hastings JW, Schibler U (2004) Adapting to life on a rotating world at the gene expression level. In: Dunlap JC, Loros JJ, DeCoursey PJ (eds) Chronobiology: biological timekeeping. Sinauer, Sunderland, pp 255–289

    Google Scholar 

  • McCluskey ES (1967) Circadian rhythms in female ants and loss after mating flight. Comp Biochem Physiol 23:665–677

    Article  PubMed  CAS  Google Scholar 

  • McCluskey ES (1973) Generic diversity in phase rhythm in Formicine ants. Psyche 80:295–304

    Article  Google Scholar 

  • McCluskey ES, Brown WL (1972) Rhythms and other biology of the giant tropical ant Paraponera. Psyche 79:335–347

    Article  Google Scholar 

  • McCluskey ES, Carter CE (1969) Loss of rhythmic activity in female ants caused by mating. Comp Biochem Physiol 31:217–226

    Article  PubMed  CAS  Google Scholar 

  • Monnin T, Ratnieks FLW (2001) Policing in queenless ants. Behav Ecol Sociobiol 50:97–108

    Article  Google Scholar 

  • Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160

    Article  Google Scholar 

  • Nakata K (1995) Age polyethism, idiosyncrasy and behavioral flexibility in the queenless ponerine ant, Diacamma sp. J Ethol 13:113–123

    Article  Google Scholar 

  • Nakata K, Tsuji K, Holldobler B, Taki A (1998) Sexual calling by workers using the metatibial glands in the ant, Diacamma sp., from Japan (Hymenoptera : Formicidae). J Insect Behav 11:869–877

  • Narendra A, Reid SF, Hemmi JM (2010) The twilight zone: ambient light levels trigger activity in primitive ants. Proc R Soc B 277:1531–1538

    Article  PubMed  PubMed Central  Google Scholar 

  • Okada Y, Miyazaki S, Miyakawa H, Ishikawa A, Tsuji K, Miura T (2010) Ovarian development and insulin-signaling pathways during reproductive differentiation in the queenless ponerine ant Diacamma sp. J Insect Physiol 56:288–295

    Article  PubMed  CAS  Google Scholar 

  • Peeters C (1991) The occurrence of sexual reproduction among ant workers. Biol J Linn Soc 44:141–152

    Article  Google Scholar 

  • Peeters C, Higashi S (1989) Reproductive dominance controlled by mutilation in the queenless ant Diacamma-Australe. Naturwissenschaften 76:177–180

    Article  Google Scholar 

  • Saunders DS (2002) Insect clocks, 3rd edn. Elsevier, Amsterdam

    Google Scholar 

  • Sharma VK, Lone SR, Goel A (2004a) Clocks for sex: loss of circadian rhythms in ants after mating? Naturwissenschaften 91:334–337

    PubMed  CAS  Google Scholar 

  • Sharma VK, Lone SR, Mathew D, Goel A, Chandrashekaran MK (2004b) Possible evidence for shift work schedules in the media workers of the ant species Camponotus compressus. Chronobiol Int 21:386–390

    Article  Google Scholar 

  • Sharma VK, Lone SR, Mathew D, Goel A, Chandrashekaran MK (2004c) Circadian consequences of social organization in the ant species Camponotus compressus. Naturwissenschaften 91:334–337

    PubMed  CAS  Google Scholar 

  • Shemesh Y, Eban-Rothschild A, Cohen M, Bloch G (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J Neurosci 30:12517–12525

    Article  PubMed  CAS  Google Scholar 

  • Sokolove PG, Bushell WN (1978) Chi square periodogram—its utility for analysis of circadian-rhythms. J Theor Biol 72:131–160

    Article  PubMed  CAS  Google Scholar 

  • Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and division of labor in honey bee colonies. PNAS 97:6914–6919

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wilson EO (1971) The insect societies. Cambridge, Mass., Belknap.

  • Yerushalmi S, Green RM (2009) Evidence for the adaptive significance of circadian rhythms. Ecol Lett 12:970–981

    Article  PubMed  Google Scholar 

  • Yerushalmi S, Bodenhaimer S, Bloch G (2006) Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees. J Exp Biol 209:1044–1051

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank for T. Shimoji, T. Kikuchi, M. Hojo, S. Dobata, K. Okada, M. Abe for supporting technical procedure and ant collection. This work was supported by Japan Society for the Promotion of Science to T.F., Y.O. (KAKENHI 24870006, 26870121), and T. M. (KAKENHI 23570027).

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Authors and Affiliations

  1. Laboratory of Evolutionary Ecology, Graduate School of Environmental and Life Science, Okayama University, Okayama, 700-8530, Japan

    Taro Fuchikawa & Takahisa Miyatake

  2. Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1, Komaba, Tokyo, Japan

    Yasukazu Okada

  3. Department of Subtropical Agro-Environmental Sciences, Faculty of Agriculture, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan

    Kazuki Tsuji

Authors
  1. Taro Fuchikawa
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  2. Yasukazu Okada
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  3. Takahisa Miyatake
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  4. Kazuki Tsuji
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Corresponding author

Correspondence to Yasukazu Okada.

Additional information

Communicated by J. Heinze

T. Fuchikawa and Y. Okada contributed equally to this work.

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Figure S1

Temporal dynamics of forager numbers. Each column is number of foragers (workers outside of the nest) in every 30-minutes. Open and closed arrowheads indicate light-on and light-off respectively in the environmental chamber before measurement. Measurements were under constant dark condition. Colony names are above the histograms. (DOC 92 kb)

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Fuchikawa, T., Okada, Y., Miyatake, T. et al. Social dominance modifies behavioral rhythm in a queenless ant. Behav Ecol Sociobiol 68, 1843–1850 (2014). https://doi.org/10.1007/s00265-014-1793-9

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  • DOI: https://doi.org/10.1007/s00265-014-1793-9

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