One might think that the existence or otherwise of queen pheromones to be a straight-forward matter that was satisfactorily answered when de Groot and Voogd (1954) showed that the heads of decapitated queen honey bees suppress ovary activation in caged workers. This remarkable finding was followed by the isolation and synthesis of a chemical from a gland in the queen’s mandibles, (E)-9-Oxodec-2-enoic acid (9-ODA), that mediates the effect on worker fecundity (Butler et al. 1961). 9-ODA fits the definition of a pheromone precisely: “substances [that] are secreted … by one individual… and received by a second individual … in which they release a specific reaction” (Karlson and Lüscher 1959). Nonetheless, outside honeybees, the existence of queen pheromones has remained controversial. In ants and stingless bees, there are no known 9-ODA homologues—a single chemical that is (almost) unique to queens and suppresses worker ovary activation. Rather, it seems that certain cuticular hydrocarbons (CHs) of queens suppress ovary activation in workers (van Oystaeyen et al. 2014). Cuticular hydrocarbons seem unlikely candidates for a queen pheromone. All insects have a waxy layer of hydrocarbons on their cuticle. Although CHs vary in composition and amount between queens and workers in ants and stingless bees, these are quantitative, not qualitative differences and may therefore open to cheating and misinterpretation. More broadly, theoretical work on biological signals (e.g. Guilford and Stamp Dawkins 1991) has demonstrated that receivers of a signal will evolve to ignore it if it reduces their fitness. How best then, to interpret queen pheromones? Are they merely cues that workers use to determine whether there is an active queen in their colony, or contraceptives that queens use to manipulate the fertility of their daughter workers (Keller and Nonacs 1993; Peso et al. 2015)? Notably, the blend of CHs produced by female insects is correlated with their reproductive physiology (reviewed in Smith and Liebig 2017) making CHs candidates for “honest” queen pheromones. However, empirical evidence that CHs can act as queen pheromones has not been unanimous (e.g. Amsalem et al. 2015), and theoreticians continue to disagree over the evolutionarily plausibility of “manipulative” pheromones. The extent to which the worker response to pheromones involves learning or nuanced decision-making, versus being “hard-wired,” is also a topic of debate (Smith and Liebig 2017). Luke Holman (2018) has done those of us that worry about such matters a great service by scouring the literature to amass data from 55 experiments from 44 papers covering 16 species and then critically probing the evidence for the existence of queen pheromones using a meta-analysis. He shows that there is evidence from multiple studies, research groups, and taxa that queens produce substances to which workers respond by not activating their ovaries. I am happy that such substances be known as queen pheromones, for they clearly are. But, this does not resolve the more philosophical question as to “why” workers respond to the pheromone. Is it an automatic release of programmed cell death in the ovary, or a more nuanced behavioral response that maximizes overall reproductive success and is context dependent? Holman argues that evidence for context dependence is weak. I have often thought that it will be impossible to resolve the paradox of queen pheromones empirically because the predictions of the “honest signal” and “manipulative contraceptive” hypotheses are the same: queen presence leads to sterile workers. However, Nunes et al. (2017) showed that there was no relationship between CH profiles and facultative worker sterility across 21 stingless bee species, suggesting that CHs are signals not contraceptives. Furthermore, workers of some ant genera like Pheidole are completely sterile because they lack ovaries. Such species still need an “I’m here laying eggs” signal, but have no need for a contraceptive. It would be interesting to see whether the CH profiles differ between queens and workers in these species. If they do, this would further suggest that CHs are a fertility signal and not a contraceptive. REFERENCES Amsalem E , Orlova M , Grozinger CM . 2015 . A conserved class of queen pheromones? Re-evaluating the evidence in bumblebees (Bombus impatiens) . Proc R Soc Lon B . 282 : 20151800 . Google Scholar CrossRef Search ADS Butler CG , Callow RK , Johnston NC . 1961 . The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honey bee pheromone . Pro R Soc Lond B . 155 : 417 – 432 . Google Scholar CrossRef Search ADS De Groot AP , Voogd S . 1954 . On the ovary development in queenless worker bees (Apis mellifica L.) . Experientia . 10 : 384 – 385 . Google Scholar CrossRef Search ADS PubMed Guilford T , Stamp Dawkins M . 1991 . Receiver psychology and the evolution of animal signals . Animal Behaviour . 42 : 1 – 14 . Google Scholar CrossRef Search ADS Holman L . Forthcoming 2018 . Queen pheromones and reproductive division of labour: a meta-analysis . Behav Ecol . Karlson P , Luscher M . 1959 . Pheromones’: a new term for a class of biologically active substances . Nature . 183 : 55 – 56 . Google Scholar CrossRef Search ADS PubMed Keller L , Nonacs P . 1993 . The role of queen pheromones in social insects: queen control or queen signal ? Animal Behaviour . 45 : 787 – 794 . Google Scholar CrossRef Search ADS Nunes TM , Oldroyd BP , Elias LG , Mateus S , Tuatti IC , Lopes NP . 2017 . Evolution of queen cuticular hydrocarbons and worker reproduction in stingless bees . Nature Ecology & Evolution . 2 : 185 . Peso M , Elgar MA , Barron AB . 2015 . Pheromonal control: reconciling physiological mechanism with signalling theory . Biol Rev Camb Philos Soc . 90 : 542 – 559 . Google Scholar CrossRef Search ADS PubMed Smith AA , Liebig J . 2017 . The evolution of cuticular fertility signals in eusocial insects . Curr Opin Insect Sci . 22 : 79 – 84 . Google Scholar CrossRef Search ADS PubMed Van Oystaeyen A , Oliveira RC , Holman L , van Zweden JS , Romero C , Oi CA , d’Ettorre P , Khalesi M , Billen J , Wäckers F et al. 2014 . Conserved class of queen pheromones stops social insect workers from reproducing . Science . 343 : 287 – 290 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: email@example.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
Behavioral Ecology – Oxford University Press
Published: Apr 28, 2018
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