Alarm communication predates eusociality in termites

0
89
Alarm communication predates eusociality in termites

  • Stankowich, T., Haverkamp, P. J. & Caro, T. Ecological drivers of antipredator defenses in Carnivores. Evolution 68, 1415–1425 (2014).

    Google Scholar 

  • Sugiura, S. Predators as drivers of insect defenses. Entomol. Sci. 23, 316–337 (2020).

    Google Scholar 

  • Beauchamp, G. Animal Vigilance—Monitoring Predators And Competitors. p. 254 (Elsevier, 2015).

  • Hollén, L. I. & Radford, A. N. The development of alarm call behaviour in mammals and birds. Anim. Behav. 78, 791–800 (2009).

    Google Scholar 

  • Gill, S. & Bierema, A. M.-K. On the meaning of alarm calls: a review of functional reference in avian alarm calling. Ethology 119, 449–461 (2013).

    Google Scholar 

  • Blumstein, D. T. Rodent Societies: An Ecological & Evolutionary Perspective (eds. J. O. Wolff & P. W. Sherman) pp. 317–327. (University of Chicago Press, 2007).

  • Snowdon, C. T. Vervet monkey alarm calls: setting the historical context. Anim. Behav. Cogn. 7, 87–94 (2020).

    Google Scholar 

  • Hamilton, W. D. The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52 (1964).

    CAS 

    Google Scholar 

  • Smith, J. M. The evolution of alarm calls. Am. Nat. 99, 59–63 (1965).

    Google Scholar 

  • Taylor, R. J., Balph, D. F. & Balph, M. H. The evolution of alarm calling: a cost-benefit analysis. Anim. Behav. 39, 860–868 (1990).

    Google Scholar 

  • Hermann, H. R. Defensive Mechanisms in Social Insects. p. 259 (Praeger Publishers, 1984).

  • Stern, D. L. & Foster, W. A. The evolution of soldiers in aphids. Biol. Rev. 71, 27–79 (1996).

    CAS 

    Google Scholar 

  • Smith, R. J. F. Alarm signals in fishes. Rev. Fish. Biol. Fish. 2, 33–63 (1992).

    Google Scholar 

  • Klump, G. M. & Shalter, M. D. Acoustic behaviour of birds and mammals in the predator context; I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm signals. Z. Tierpsychol. 66, 189–226 (1984).

    Google Scholar 

  • Caro, T. Antipredator Defenses in Birds and Mammals. p. 592 (University of Chicago Press, 2005).

  • Seyfarth, R. M., Cheney, D. L. & Marler, P. Monkey responses to three different alarm calls: Classification and semantic communication. Science 210, 801–803 (1980).

    CAS 

    Google Scholar 

  • Wyatt, T. D. Pheromones and Animal Behaviour. p. 391 (Cambridge University Press, 2003).

  • Hill, P. S. M. Vibrational Communication in Animals. p. 272 (Harvard, Cambridge, 2008).

  • Hill, P. S. M. Biotremology: We fight for food. Curr. Biol. 29, R209–R212 (2019).

    CAS 

    Google Scholar 

  • Cocroft, R. B. & Rodríguez, R. L. The behavioral ecology of insect vibrational communication. BioScience 55, 323–334 (2005).

    Google Scholar 

  • Kettler, R. & Leuthold, R. H. Inter- and intraspecific alarm response in the termite Macrotermes subhyalinus (Rambur). Insectes Soc. 42, 145–156 (1995).

    Google Scholar 

  • Hölldobler, B., Braun, U., Gronenberg, W., Kirchner, W. H. & Peeters, C. Trail communication in the ant Megaponera foetens (Fabr.) (Formicidae, Ponerinae). J. Insect Physiol. 40, 585–593 (1994).

    Google Scholar 

  • Hunt, J. H. & Richard, F.-J. Intracolony vibroacoustic communication in social insects. Insectes Soc. 60, 403–417 (2013).

    Google Scholar 

  • Howse, P. E. The perception of vibration by the subgenual organ in Zootermopsis angusticollis Emerson and Periplaneta americana L. Experientia 18, 457–458 (1962).

    Google Scholar 

  • Golden, T. M. J. & Hill, P. S. M. The evolution of stridulatory communication in ants, revisited. Insectes Soc. 63, 309–319 (2016).

    Google Scholar 

  • Šobotník, J., Hanus, R. & Roisin, Y. Agonistic behavior of the termite Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J. Insect Behav. 21, 521–534 (2008).

    Google Scholar 

  • Delattre, O. et al. Complex alarm strategy in the most basal termite species. Behav. Ecol. Sociobiol. 69, 1945–1955 (2015).

    Google Scholar 

  • Krausa, K., Hager, F. A., Kiatoko, N. & Kirchner, W. H. Vibrational signals of African stingless bees. Insectes Soc. 64, 415–424 (2017).

    Google Scholar 

  • Rosengaus, R., Jordan, C., Lefebvre, M. & Traniello, J. F. A. Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86, 544–548 (1999).

    CAS 

    Google Scholar 

  • Evans, T. A. et al. Termites assess wood size by using vibration signals. Proc. Natl Acad. Sci. USA 102, 3732–3737 (2005).

    CAS 

    Google Scholar 

  • Evans, T. A. et al. Termites eavesdrop to avoid competitors. Proc. R. Soc. B 276, 4035–4041 (2009).

    Google Scholar 

  • Blum, M. S. Comprehensive Insect Physiology, Biochemistry and Pharmacology: Behavior, Vol. 9 (eds. G. A. Kerkut & L. I. Gilbert), pp. 193–224 (Pergamon Press, 1985).

  • Verheggen, F. J., Haubruge, E. & Mescher, M. C. Alarm pheromones—Chemical signaling in response to danger, Editor(s): Gerald Litwack. Vitam. Horm. 83, 215–239 (2010).

    CAS 

    Google Scholar 

  • Šobotník, J., Jirošová, A. & Hanus, R. Chemical warfare in termites. J. Insect Physiol. 56, 1012–1021 (2010).

    Google Scholar 

  • Eisner, T., Kriston, I. & Aneshansley, D. J. Defensive behavior of a termite (Nasutitermes exitiosus). Behav. Ecol. Sociobiol. 1, 83–125 (1976).

    Google Scholar 

  • Šobotník, J. et al. (E,E)-α-Farnesene, an alarm pheromone of the termite Prorhinotermes canalifrons. J. Chem. Ecol. 34, 478–486 (2008).

    Google Scholar 

  • Leonhardt, S. D., Menzel, F., Nehring, V. & Schmitt, T. Ecology and evolution of communication in social insects. Cell 164, 1277–1287 (2016).

    CAS 

    Google Scholar 

  • Wilson, E. O. & Regnier, F. E. Jr The evolution of the alarm-defense system in the formicine ants. Am. Nat. 105, 279–289 (1971).

    Google Scholar 

  • Bradshaw, J. W. S., Baker, R. & Howse, P. E. Multicomponent alarm pheromones of the weaver ant. Nature 258, 230–231 (1975).

    CAS 

    Google Scholar 

  • Norman, V. C., Butterfield, T., Drijfhout, F., Tasman, K. & Hughes, W. O. Alarm pheromone composition and behavioral activity in fungus-growing ants. J. Chem. Ecol. 43, 225–235 (2017).

    CAS 

    Google Scholar 

  • Prestwich, G. D. Defense Mechanisms of Termites. Annu. Rev. Entomol. 29, 201–232 (1984).

    CAS 

    Google Scholar 

  • Bell, W. J., Roth, L. M. & Nalepa, C. A. Cockroaches: Ecology, Behavior, and Natural History. p. 247 (The Johns Hopkins University Press, 2007).

  • Evans, D. A., Baker, R., Briner, P. H. & McDowell, P. G. Defensive secretions of some African termites. Proceedings of the International Congress of the International Union for the Study of Social Insects (1977).

  • Anderson, M. The evolution of eusociality. Annu. Rev. Ecol. Syst. 15, 165–189 (1984).

    Google Scholar 

  • Stern, D. L. A phylogenetic analysis of soldier evolution in the aphid family Hormaphididae. Proc. R. Soc. B 256, 203–209 (1994).

    CAS 

    Google Scholar 

  • Bourke, A. F. Behavioural Ecology: An Evolutionary Approach, 4th ed. (eds. J. R. Krebs & N. B. Davies) pp. 203–227. (Blackwell Publishing, 1997).

  • Deligne, J., Quennedey, A. & Blum, M. S. Social Insects (ed. H. R. Hermann) p. 1–76 (Academic Press, 1981).

  • Bignell, D. E. The Mechanistic Benefits of Microbial Symbionts, Advances in Environmental Microbiology (ed. C. J. Hurst), p. 121–172. (Springer, 2016).

  • Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).

    CAS 

    Google Scholar 

  • Tuma, J., Eggleton, P. & Fayle, T. M. Ant-termite interactions: an important but under-explored ecological linkage. Biol. Rev. 95, 555–572 (2020).

    Google Scholar 

  • Noirot, C. & Pasteels, J. M. Ontogenetic development and evolution of the worker caste in termites. Experientia 43, 851–860 (1987).

    Google Scholar 

  • Prestwich, G. D., Bierl, B. A., Devilbiss, E. D. & Chaudhury, M. F. B. Soldier frontal glands of the termite Macrotermes subhyalinus: Morphology, chemical composition, and use in defense. J. Chem. Ecol. 3, 579–590 (1977).

    CAS 

    Google Scholar 

  • Waller, D. A. & La Face, J. P. Unpalatability as a passive defense of Coptotermes formosanus Shiraki soldiers against ant predation. J. Appl. Entomol. 103, 148–153 (1987).

    Google Scholar 

  • Quennedey, A. Defensive Mechanisms in Social Insects (ed. H. R. Hermann) p. 151–200. (1984)

  • Kuan, K.-C., Chiu, C. I., Shih, M.-C., Chi, K.-J. & Li, H.-F. Termite’s twisted mandible presents fast, powerful, and precise strikes. Sci. Rep. 10, 9462 (2020).

    CAS 

    Google Scholar 

  • Šobotník, J. et al. Explosive backpacks in old termite workers. Science 337, 436 (2012).

    Google Scholar 

  • Bourguignon, T. et al. Molecular mechanism of the two-component suicidal weapon of Neocapritermes taracua old workers. Mol. Biol. Evol. 33, 809–819 (2016).

    CAS 

    Google Scholar 

  • Wilson, E. O. The Insect Societies (Harvard University Press, 1971).

  • Roisin, Y., Everaerts, C., Pasteels, J. M. & Bonnard, O. Caste-dependent reactions to soldier defensive secretion and chiral alarm/recruitment pheromone in Nasutitermes princeps. J. Chem. Ecol. 16, 2865–2875 (1990).

    CAS 

    Google Scholar 

  • Connétable, S., Robert, A., Bouffault, F. & Bordereau, C. Vibratory alarm signals in two sympatric higher termite species: Pseudacanthotermes spiniger and P. militaris (Termitidae, Macrotermitinae). J. Insect Behav. 12, 329–342 (1999).

    Google Scholar 

  • Lubin, Y. D. & Montgomery, G. G. Defenses of Nasutitermes termites (Isoptera, Termitidae) against Tamandua anteaters (Edentata, Myrmecophagidae). Biotropica 13, 66–76 (1981).

    Google Scholar 

  • Hölldobler, B. & Wilson, E. O. The Ants (Harvard University Press, 1990).

  • Moore, B. P. Studies on the chemical composition and function of the cephalic gland secretion in Australian termites. J. Insect Physiol. 14, 33–39 (1968).

    CAS 

    Google Scholar 

  • Maschwitz, U. & Mühlenberg, M. Chemische Gefahrenalarmierung bei einer Termite. Sci. Nat. 59, 516–516 (1972).

    Google Scholar 

  • Vrkoč, J., Křeček, J. & Hrdý, I. Monoterpenic alarm pheromones in two Nasutitermes species. Acta Entomol. Bohemoslov. 75, 1–8 (1978).

    Google Scholar 

  • Röhrig, A., Kirchner, W. H. & Leuthold, R. H. Vibrational alarm communication in the African fungus-growing termite genus Macrotermes (Isoptera, Termitidae). Insectes Soc. 46, 71–77 (1999).

    Google Scholar 

  • Reinhard, J. & Clément, J.-L. Alarm reaction of European Reticulitermes termites to soldier head capsule volatiles (Isoptera, Rhinotermitidae). J. Insect Behav. 15, 95–107 (2002).

    Google Scholar 

  • Cristaldo, P. F. et al. The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae): the integration of chemical and vibroacoustic signals. Biol. Open 4, 1649–1659 (2015).

    CAS 

    Google Scholar 

  • Delattre, O. et al. Chemical and vibratory signals used in alarm communication in the termite Reticulitermes flavipes (Rhinotermitidae). Insectes Soc. 66, 265–272 (2019).

    Google Scholar 

  • Krishna, K., Grimaldi, D. A., Krishna, V. & Engel, M. S. Treatise on the Isoptera of the world. Bull. Am. Mus. Nat. Hist. 377, 1–2407 (2013).

    Google Scholar 

  • Howse, P. E. On the significance of certain oscillatory movements of termites. Insectes Soc. 12, 335–345 (1965).

    Google Scholar 

  • Stuart, A. M. Studies on the communication of alarm in the termite Zootermopsis nevadensis (Hagen), Isoptera. Physiol. Zool. 36, 85–96 (1963).

    Google Scholar 

  • Šobotník, J., Bourguignon, T., Hanus, R., Weyda, F. & Roisin, Y. Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol. J. Linn. Soc. 99, 839–848 (2010).

    Google Scholar 

  • Farine, J.-P. et al. The defensive secretion of Eurycotis floridana (Dictyoptera, Blattidae, Polyzosteriinae): chemical identification and evidence of an alarm function. Insect Biochem. Mol. Biol. 27, 577–586 (1997).

    CAS 

    Google Scholar 

  • Farine, J.-P. et al. Defensive secretion of Therea petiveriana: Chemical identification and evidence of an alarm function. J. Chem. Ecol. 28, 1629–1640 (2002).

    CAS 

    Google Scholar 

  • Brossut, R. Allomonal secretions in cockroaches. J. Chem. Ecol. 9, 143–158 (1983).

    CAS 

    Google Scholar 

  • Noirot, C. Biology of Termites (eds. K. Krishna, F. M. Weesner), p. 89–123. (Academic Press, 1969).

  • Neoh, K.-B., Yeap, B.-K., Tsunoda, K., Yoshimura, T. & Lee, C.-Y. Do termites avoid carcasses? Behavioral responses depend on the nature of the carcasses. PLoS ONE 7, e36375 (2012).

    CAS 

    Google Scholar 

  • Sun, Q., Hampton, J. D., Merchant, A., Haynes, K. F. & Zhou, X. Cooperative policing behaviour regulates reproductive division of labour in a termite. Proc. R. Soc. B 287, 20200780 (2020).

    Google Scholar 

  • Lenz, M. Caste Differentiation in Social Insects (eds. J. A. L. Watson, B. M. Okot-Kotber, C. Noirot), p. 125–145. (Pergamon Press, 1985).

  • Stuart, A. M. The determination and regulation of the neotenic reproductive caste in the lower termites (Isoptera): with special reference to the genus Zootermopsis (Hagen). Sociobiology 4, 223–237 (1979).

    Google Scholar 

  • Bourguignon, T. et al. The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol. Biol. Evol. 32, 406–421 (2015).

    CAS 

    Google Scholar 

  • Buček, A. et al., Evolution of termite symbiosis informed by transcriptome-based phylogenies. Curr. Biol. 29 (2019).

  • Shellman-Reeve, J. S. The Evolution of Social Behaviour in Insects and Arachnids. (eds. B. J. Crespi, J. C. Choe), p. 52–93. (Cambridge University Press, 1997)

  • Seelinger, G. & Seelinger, U. On the social organisation, alarm and fighting in the primitive cockroach Cryptocercus punctulatus Scudder. Z. Tierpsychol. 61, 315–333 (1983).

    Google Scholar 

  • Maistrello, L. & Sbrenna, G. Behavioural differences between male and female replacement reproductives in Kalotermes flavicollis (Isoptera, Kalotermitidae). Insectes Soc. 46, 186–191 (1999).

    Google Scholar 

  • Maistrello, L. & Sbrenna, G. Frequency of some behavioural patterns in colonies of Kalotermes flavicollis (Isoptera Kalotermitidae): the importance of social interactions and vibratory movements as mechanisms for social integration. Ethol. Ecol. Evol. 8, 365–375 (1996).

    Google Scholar 

  • Whitman, J. G. & Forschler, B. T. Observational notes on short-lived and infrequent behaviors displayed by Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 100, 763–771 (2007).

    Google Scholar 

  • Ruhland, F., Moulin, M., Choppin, M., Meunier, J. & Lucas, C. Reproductives and eggs trigger worker vibration in a subterranean termite. Ecol. Evol. 10, 5892–5898 (2020).

    Google Scholar 

  • Stuart, A. M. Preliminary studies on the significance of head-banging movements in termites with special reference to Zootermopsis angusticollis (Hagen) (Isoptera: Hodotermitidae). Sociobiology 14, 49–60 (1988).

    Google Scholar 

  • Noirot, C. Biology of Termites (eds. K. Krishna, F. Weesner) Vol. 2, p. 73–125 (Academic Press, 1970).

  • Aguilera-Olivares, D., Palma-Onetto, V., Flores-Prado, L., Zapata, V. & Niemeyer, H. M. X-ray computed tomography reveals that intraspecific competition promotes soldier differentiation in a one-piece nesting termite. Entomol. Exp. Appl. 163, 26–34 (2017).

    Google Scholar 

  • King, E. G. & Spink, W. T. Foraging galleries of the Formosan subterranean termite, Coptotermes formosanus, in Louisiana. Ann. Entomol. Soc. Am. 62, 536–542 (1969).

    Google Scholar 

  • Valterová, I., Vrkoč, J., Lindström, M. & Norin, T. On the natural occurrence of (-)-3-carene, a component of termite defense secretions. Sci. Nat. 79, 416–417 (1992).

    Google Scholar 

  • Nutting, W. L. Colonizing flights and associated activities of termites. I. The desert damp-wood termite Paraneotermes simplicicornis (Kalotermitidae). Psyche 73, 131–149 (1966).

    Google Scholar 

  • Mizumoto, N. & Bourguignon, T. Modern termites inherited the potential of collective construction from their common ancestor. Ecol. Evol. 10, 6775–6784 (2020).

    Google Scholar 

  • Sands, W. A. The soldierless termites of Africa. Bull. Br. Mus. Nat. Hist. (Suppl.) 18, 1–244 (1972).

    Google Scholar 

  • Ahmad, M. The soldierless termite genera of the Oriental region, with a note on their phylogeny (Isoptera: Termitidae). Pak. J. Zool. 8, 105–123 (1976).

    Google Scholar 

  • Miller, L. R. Invasitermes, a new genus of soldierless termites from northern Australia (Isoptera: Termitidae). J. Aust. Entomol. Soc. 23, 33–37 (1984).

    Google Scholar 

  • Šobotník, J. et al. The frontal gland in workers of Neotropical soldierless termites. Naturwissenschaften 97, 495–503 (2010).

    Google Scholar 

  • Chouvenc, T., Šobotník, J., Engel, M. S. & Bourguignon, T. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cell. Mol. Life Sci. 78, 2749–2769 (2021).

    CAS 

    Google Scholar 

  • Hermann, H. R. & Blum, M. S. Social Insects (ed. H. R. Hermann) Vol. 2, pp 77–197 (Academic Press, 1981).

  • Buschinger, A., Maschwitz, U. Defensive Mechanisms In Social Insects (ed. H. R. Hermann), p. 95–150 (Praeger, 1984).

  • Schönrogge, K., Barbero, F., Casacci, L. P., Settele, J. & Thomas, J. A. Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles. Anim. Behav. 134, 249–256 (2017).

    Google Scholar 

  • Lo, N. et al. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol. 10, 801–804 (2000).

    CAS 

    Google Scholar 

  • Inward, D., Beccaloni, G. & Eggleton, P. Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Lett. 3, 331–335 (2007).

    CAS 

    Google Scholar 

  • Haverty, M. I. The proportion of soldiers in termite colonies: a list and a bibliography. Sociobiology 2, 199–216 (1977).

    Google Scholar 

  • Miramontes, O. & DeSouza, O. The nonlinear dynamics of survival and social facilitation in termites. J. Theor. Biol. 181, 373–380 (1996).

    Google Scholar 

  • Bourguignon, T. et al. Mitochondrial phylogenomics resolves the global spread of higher termites, ecosystem engineers of the tropics. Mol. Biol. Evol. 34, 589–597 (2017).

    CAS 

    Google Scholar 

  • Donovan, S. E., Eggleton, P. & Bignell, D. E. Gut content analysis and a new feeding group classification of termites. Ecol. Entomol. 26, 356–366 (2001).

    Google Scholar 

  • Maddison, W. P. & Maddison, D. R. Mesquite: A Modular System For Evolutionary Analysis http://mesquiteproject.org (2019).

  • Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).

    Google Scholar 

  • Maddison, W. P. Testing character correlation using pairwise comparisons on a phylogeny. J. Theor. Biol. 202, 195–204 (2000).

    CAS 

    Google Scholar 

  • Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015).

    Google Scholar