in

Family before work: task reversion in workers of the red imported fire ant, Solenopsis invicta in the presence of brood

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

    Google Scholar 

  • Beshers, S. N. & Fewell, J. H. Models of division of labor in social insects. Annu. Rev. Entomol. 46, 413–440 (2001).

    CAS 

    Google Scholar 

  • Seeley, T. D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 4, 287–293 (1982).

    Google Scholar 

  • Tallamy, D. W. Insect parental care. Bioscience 34, 20–24. https://doi.org/10.2307/1309421 (1984).

    Article 

    Google Scholar 

  • Queller, D. C. Extended parental care and the origin of eusociality. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 256, 105–111. https://doi.org/10.1098/rspb.1994.0056 (1994).

    Article 
    ADS 

    Google Scholar 

  • Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta 1,2. Ann. Entomol. Soc. Am. 68, 301–304 (1975).

    CAS 

    Google Scholar 

  • Endler, A. et al. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl. Acad. Sci. USA 101, 2945–2950. https://doi.org/10.1073/pnas.0308447101 (2004).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Maisonnasse, A., Lenoir, J. C., Beslay, D., Crauser, D. & Le Conte, Y. E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS ONE 5, e13531. https://doi.org/10.1371/journal.pone.0013531 (2010).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Schultner, E., Oettler, J. & Helantera, H. The role of brood in eusocial hymenoptera. Q. Rev. Biol. 92, 39–78. https://doi.org/10.1086/690840 (2017).

    Article 

    Google Scholar 

  • Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A. & Omholt, S. W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering? J. Econ. Entomol. 97, 741–747 (2004).

    Google Scholar 

  • Calabi, P. & Traniello, J. F. Behavioral flexibility in age castes of the ant Pheidole dentata. J. Insect Behav. 2, 663–677 (1989).

    Google Scholar 

  • Gordon, D. W. Dynamics of task switching in harvester ants. Anim. Behav. 38, 194–204 (1989).

    Google Scholar 

  • Robinson, G. E. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665. https://doi.org/10.1146/annurev.en.37.010192.003225 (1992).

    Article 
    CAS 

    Google Scholar 

  • Robinson, E. J., Feinerman, O. & Franks, N. R. Flexible task allocation and the organization of work in ants. Proc. R. Soc. B: Biol. Sci. 276, 4373–4380 (2009).

    Google Scholar 

  • Nijhout, H. F. & Wheeler, D. E. Juvenile-hormone and the physiological-basis of Insect polymorphisms. Q. Rev. Biol. 57, 109–133. https://doi.org/10.1086/412671 (1982).

    Article 
    CAS 

    Google Scholar 

  • Herb, B. R. et al. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15, 1371–1373. https://doi.org/10.1038/nn.3218 (2012).

    Article 
    CAS 

    Google Scholar 

  • Kensuke, N. Age polyethism, idiosyncrasy and behavioural flexibility in the queenless ponerine ant, Diacamma sp. J. Ethol. 13, 113–123 (1995).

    Google Scholar 

  • Kensuke, N. Does behavioral flexibility compensate or constrain colony productivity? Relationship among age structure, labor allocation, and production of workers in ant colonies. J. Insect Behav. 9, 557–569 (1996).

    Google Scholar 

  • Shimoji, H., Kasutani, N., Ogawa, S. & Hojo, M. K. Worker propensity affects flexible task reversion in an ant. Behav. Ecol. 74, 1–8 (2020).

    Google Scholar 

  • Bernadou, A., Busch, J. & Heinze, J. Diversity in identity: Behavioral flexibility, dominance, and age polyethism in a clonal ant. Behav. Ecol. Sociobiol. 69, 1365–1375 (2015).

    Google Scholar 

  • Kohlmeier, P., Feldmeyer, B. & Foitzik, S. Vitellogenin-like A—Associated shifts in social cue responsiveness regulate behavioral task specialization in an ant. PLoS Biol. 16, e2005747 (2018).

    Google Scholar 

  • Tripet, F. & Nonacs, P. Foraging for work and age-based polyethism: The roles of age and previous experience on task choice in ants. Ethology 110, 863–877 (2004).

    Google Scholar 

  • Kohlmeier, P., Alleman, A. R., Libbrecht, R., Foitzik, S. & Feldmeyer, B. Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers. Mol. Ecol. https://doi.org/10.1111/mec.14971 (2018).

    Article 

    Google Scholar 

  • Levenbook, L. & Bauer, A. C. The fate of the larval storage protein calliphorin during adult development of Calliphora vicina. Insect Biochem. 14, 77–86 (1984).

    CAS 

    Google Scholar 

  • Zhou, X., Oi, F. M. & Scharf, M. E. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. 103, 4499–4504 (2006).

    ADS 
    CAS 

    Google Scholar 

  • Zhou, X., Tarver, M. R., Bennett, G., Oi, F. & Scharf, M. Two hexamerin genes from the termite Reticulitermes flavipes: Sequence, expression, and proposed functions in caste regulation. Gene 376, 47–58 (2006).

    CAS 

    Google Scholar 

  • Hawkings, C., Calkins, T. L., Pietrantonio, P. V. & Tamborindeguy, C. Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta). PLoS ONE 14, e0216800 (2019).

    CAS 

    Google Scholar 

  • Hoffman, E. A. & Goodisman, M. A. Gene expression and the evolution of phenotypic diversity in social wasps. BMC Biol. 5, 1–9 (2007).

    Google Scholar 

  • Hunt, J. H., Buck, N. A. & Wheeler, D. E. Storage proteins in vespid wasps: Characterization, developmental pattern, and occurrence in adults. J. Insect Physiol. 49, 785–794 (2003).

    CAS 

    Google Scholar 

  • Colgan, T. J. et al. Polyphenism in social insects: Insights from a transcriptome-wide analysis of gene expression in the life stages of the key pollinator, Bombus terrestris. BMC Genom. 12, 1–20 (2011).

    Google Scholar 

  • Cremer, S., Armitage, S. A. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).

    CAS 

    Google Scholar 

  • Cremer, S., Pull, C. D. & Fuerst, M. A. Social immunity: Emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2018).

    CAS 

    Google Scholar 

  • Danihlík, J., Aronstein, K. & Petřivalský, M. Antimicrobial peptides: A key component of honey bee innate immunity: Physiology, biochemistry, and chemical ecology. J. Apic. Res. 54, 123–136 (2015).

    Google Scholar 

  • Koch, S. I. et al. Caste-specific expression patterns of immune response and chemosensory related genes in the leaf-cutting ant, Atta vollenweideri. PLoS ONE 8, e81518 (2013).

    ADS 

    Google Scholar 

  • Chardonnet, F. et al. Food searching behaviour of a Lepidoptera pest species is modulated by the foraging gene polymorphism. J. Exp. Biol. 217, 3465–3473 (2014).

    Google Scholar 

  • Scheiner, R., Page, R. E. Jr. & Erber, J. Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav. Brain Res. 120, 67–73 (2001).

    CAS 

    Google Scholar 

  • Wang, Z. et al. Visual pattern memory requires foraging function in the central complex of Drosophila. Learn. Mem. 15, 133–142 (2008).

    Google Scholar 

  • Zhou, Y., Lei, Y., Lu, L. & He, Y. Temperature-and food-dependent foraging gene expression in foragers of the red imported fire ant Solenopsis invicta Buren (Hymenoptera: Formicidae). Physiol. Entomol. 45, 1–6 (2020).

    Google Scholar 

  • Ingram, K. K. et al. Context-dependent expression of the foraging gene in field colonies of ants: The interacting roles of age, environment and task. Proc. R. Soc. B: Biol. Sci. 283, 20160841 (2016).

    Google Scholar 

  • Ingram, K. K., Oefner, P. & Gordon, D. M. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol. 14, 813–818 (2005).

    CAS 

    Google Scholar 

  • Lucas, C. & Sokolowski, M. B. Molecular basis for changes in behavioral state in ant social behaviors. Proc. Natl. Acad. Sci. 106, 6351–6356 (2009).

    ADS 
    CAS 

    Google Scholar 

  • Ben-Shahar, Y. The foraging gene, behavioral plasticity, and honeybee division of labor. J. Comp. Physiol. A. 191, 987–994 (2005).

    CAS 

    Google Scholar 

  • Daugherty, T., Toth, A. & Robinson, G. Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus. Mol. Ecol. 20, 5337–5347 (2011).

    CAS 

    Google Scholar 

  • Morrison, L. W., Porter, S. D., Daniels, E. & Korzukhin, M. D. Potential global range expansion of the invasive fire ant, Solenopsis invicta. Biol. Invasions 6, 183–191 (2004).

    Google Scholar 

  • Valles, S. M., Wetterer, J. K. & Porter, S. D. The red imported fire ant (Hymenoptera: Formicidae) in the West Indies: Distribution of natural enemies and a possible test bed for release of self-sustaining biocontrol agents. Fls. Entomol. 98, 1101–1105 (2015).

    Google Scholar 

  • Greenberg, L., Vinson, S. & Ellison, S. Nine-year study of a field containing both monogyne and polygyne red imported fire ants (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 85, 686–695 (1992).

    Google Scholar 

  • Keller, L. & Ross, K. G. Selfish genes: A green beard in the red fire ant. Nature 394, 573–575 (1998).

    ADS 
    CAS 

    Google Scholar 

  • Vinson, S. B. Impact of the invasion of the imported fire ant. Insect Sci. 20, 439–455 (2013).

    Google Scholar 

  • Tschinkel, W. R. The Fire Ants (Harvard University Press, 2006).

    Google Scholar 

  • Cassill, D. L. & Tschinkel, W. R. Task selection by workers of the fire ant Solenopsis invicta. Behav. Ecol. Sociobiol. 45, 301–310 (1999).

    Google Scholar 

  • Mirenda, J. T. & Vinson, S. B. Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim. Behav. 29, 410–420 (1981).

    Google Scholar 

  • Wilson, E. O. Division of labor in fire ants based on physical castes (Hymenoptera: Formicidae: Solenopsis). J. Kansas Entomol. Soc. 51, 615–636 (1978).

    Google Scholar 

  • Sorensen, A., Busch, T. M. & Vinson, S. B. Behavioral flexibility of temporal subcastes in the fire ant, Solenopsis invicta in response to food. Psyche 91, 319–331 (1984).

    Google Scholar 

  • Bigley, W. S. & Vinson, S. B. Characterization of a brood pheromone isolated from the sexual brood of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 2, 301–304 (1975).

    Google Scholar 

  • Bajracharya, P., Lu, H. L. & Pietrantonio, P. V. The red imported fire ant (Solenopsis invicta Buren) kept Y not F: Predicted sNPY endogenous ligands deorphanize the short NPF (sNPF) receptor. PLoS ONE 9(10), e109590 (2014).

    ADS 

    Google Scholar 

  • Castillo, P. Short neuropeptide F receptor in the worker brain of the red imported fire ant (Solenopsis invicta Buren) and methodology for RNA interference M.S. thesis, Texas A&M University (2015).

  • Castillo, P. & Pietrantonio, P. V. Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: Indicators for division of labor and nutritional status? PLoS ONE 8, e83966 (2013).

    ADS 

    Google Scholar 

  • Cassill, D. L. & Tschinkel, W. R. Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim. Behav. 3, 801–813 (1995).

    Google Scholar 

  • Cassill, D. L., Stuy, A. & Buck, R. G. Emergent properties of food distribution among fire ant larvae. J. Theor. Biol. 3, 371–381 (1998).

    ADS 

    Google Scholar 

  • Dussutour, A. & Simpson, S. J. Communal nutrition in ants. Curr. Biol. 19, 740–744. https://doi.org/10.1016/j.cub.2009.03.015 (2009).

    Article 
    CAS 

    Google Scholar 

  • Petralia, R. S. & Vinson, S. B. Feeding in the larvae of the imported fire ant, Solenopsis invicta: Behavior and morphological adaptations. Ann. Entomol. Soc. Am. 71, 643–648 (1978).

    Google Scholar 

  • Petralia, R. S. & Vinson, S. B. Developmental morphology of larvae and eggs of the imported fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am. 72, 472–484 (1979).

    Google Scholar 

  • Chen, J. Advancement on techniques for the separation and maintenance of the red imported fire ant colonies. Insect Sci. 14, 1–4 (2007).

    Google Scholar 

  • Banks, W. A. et al. (Agricultural Research (Southern Region), Science and Education…, 1981).

  • Valles, S. M. & Porter, S. D. Identification of polygyne and monogyne fire ant colonies (Solenopsis invicta) by multiplex PCR of Gp-9 alleles. Insectes Soc. 2, 199–200 (2003).

    Google Scholar 

  • Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101 (2008).

    CAS 

    Google Scholar 

  • Cheng, D., Zhang, Z., He, X. & Liang, G. Validation of reference genes in Solenopsis invicta in different developmental stages, castes and tissues. PLoS ONE 8, e57718. https://doi.org/10.1371/journal.pone.0057718 (2013).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Qiu, H.-L., Zhao, C.-Y. & He, Y.-R. On the molecular basis of division of labor in Solenopsis invicta (Hymenoptera: Formicidae) workers: RNA-seq analysis. J. Insect Sci. 17, 48 (2017).

    Google Scholar 

  • Chen, J. et al. Role of the foraging gene in worker behavioral transition in the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Pest Manag. Sci. https://doi.org/10.1002/ps.6921 (2022).

    Article 

    Google Scholar 

  • Shorter, J. R. & Tibbetts, E. A. The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus. Insectes Soc. 56, 7–13 (2009).

    Google Scholar 

  • Pankiw, T., Page, R. E. Jr. & Kim Fondrk, M. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav. Ecol. Sociobiol. 44, 193–198. https://doi.org/10.1007/s002650050531 (1998).

    Article 

    Google Scholar 

  • Smedal, B., Brynem, M., Kreibich, C. D. & Amdam, G. V. Brood pheromone suppresses physiology of extreme longevity in honeybees (Apis mellifera). J. Exp. Biol. 212, 3795–3801. https://doi.org/10.1242/jeb.035063 (2009).

    Article 
    CAS 

    Google Scholar 

  • Solis, C. R. & Strassmann, J. E. Presence of brood affects caste differentiation in the social wasp, Polistes exclamans Viereck (Hymenoptera, Vespidae). Funct. Ecol. 4, 531–541. https://doi.org/10.2307/2389321 (1990).

    Article 

    Google Scholar 

  • Traynor, K. S. Decoding Brood Pheromone: The Releaser and Primer Effects of Young and Old Larvae on Honey Bee (Apis mellifera) Workers (Arizona State University, 2014).

    Google Scholar 

  • Wagoner, K. M., Spivak, M. & Rueppell, O. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 111, 2520–2530. https://doi.org/10.1093/jee/toy266 (2018).

    Article 
    CAS 

    Google Scholar 

  • Nijhout, H. F. & Wheeler, D. E. Juvenile hormone and the physiological basis of insect polymorphisms. Q. Rev. Biol. 57, 109–133 (1982).

    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

    Intra-individual variation of hen movements is associated with later keel bone fractures in a quasi-commercial aviary

    A latitudinal gradient of deep-sea invasions for marine fishes