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Queen pheromones, colony odors, and better science: a comment on Holman

Queen pheromones, colony odors, and better science: a comment on Holman QUEEN PHEROMONES With the identification of a growing number of queen pheromones in ants, wasps, bees, and termites in recent years, Holman’s (2018) analysis offers a timely stocktake of our current understanding. This paper shows the usefulness of systematic meta-analysis compared with “vote counting” or entirely qualitative reviews. The focus on effect sizes allows the assessment of evidence for recently proposed hypotheses, such as, for example, the interesting experiments which suggest that queen pheromones in some ant species are not effective unless they are perceived alongside familiar colony odors (reviewed in Smith and Liebig 2017). Holman observes that the small sample sizes in the experiments do not allow firm conclusions to be drawn. It would repay repetition, if possible, with larger samples designed to take account of the likely effect sizes (for which Holman (2018) offers estimates). Queen pheromones can be identified because they are consistently carried by queens in different colonies (and have been demonstrated to have the effects on worker reproduction). Pheromones superimposed on a colony-odor background that varies between colonies are a feature of social insect pheromones (Wyatt 2010, 2014). The convergent evolution of queen pheromones in independently evolved eusocial lineages of ants, bees, and wasps is fascinating (see Holman 2018 for references) but the conservation of molecules as queen pheromones in many, but not all, taxa is not unprecedented. In the absence of selection, pheromones need not change. For example, in aphids, there is no selective advantage in species-specific alarm pheromones (if anything, cross-species response is an advantage) and so aphid species across more than 30 genera share the same molecule, (E)-β-farnesene, as their alarm pheromone. It is possible that queen pheromones in some species, currently single molecules, will turn out to be multicomponent, even perhaps with components from a variety of glands. The complexity and nonhydrocarbon nature of honeybee queen pheromones does not fit with the pattern of other hymenopteran queen pheromones but examples from around the animal kingdom show that the evolution of new pheromones occurs commonly, as demonstrated by the enormous variety of independently evolved male moth sex pheromones (see Wyatt 2014). A multitude of effects have been ascribed to queen pheromones. Blum noted that pheromone molecules often have multiple functions in social insects (“parsimony,” see Wyatt 2014). It will be interesting to see if the king and queen recognition pheromone in Reticulitermes termites, the hydrocarbon heneicosane, identified by behavioral responses of workers (Funaro et al. 2018), turns out to also have effects on worker reproduction. RANDOMIZED, BLIND, TRIALS AND THE QUEST FOR RELIABLE SCIENCE The response of biomedical and psychological researchers to the “reproducibility crisis” seems to be well ahead of those in ecology and evolution in recognizing potential sources of bias in designing, running, analyzing, and interpreting experiments, as well as proposing remedies (see e.g. the Catalogue of Bias www.catalogofbias.org). Munafò et al. (2017) present a manifesto for more reproducible behavioral science, starting with the design and conduct of experiments. Randomization and blinding are key requirements, as highlighted by Holman (2018), who observed that effect sizes were larger in queen pheromone experiments that were not run blind. Increasing scientific transparency is also important: pre-registration of experiments (to avoid p-Hacking for example) and incentives for open data sharing are starting to be encouraged in evolutionary biology and ecology too (Parker et al. 2016; Fidler et al. 2017). References Fidler F , Chee YE , Wintle BC , Burgman MA , McCarthy MA , Gordon A . 2017 . Metaresearch for evaluating reproducibility in ecology and evolution . Bioscience . 67 : 282 – 289 . Google Scholar PubMed Funaro CF , Boroczky K , Vargo EL , Schal C . 2018 . Identification of a queen and king recognition pheromone in the subterranean termite Reticulitermes flavipes . Proc Natl Acad Sci USA . 115 : 3888 – 3893 . Google Scholar Crossref Search ADS PubMed Holman L ( 2018 ) Queen pheromones and reproductive division of labour: a meta-analysis . Behav Ecol . 26 : 1199 – 1209 . Munafò MR , Nosek BA , Bishop DVM , Button KS , Chambers CD , Percie du Sert N , Simonsohn U , Wagenmakers E-J , Ware JJ , Ioannidis JPA . 2017 . A manifesto for reproducible science . Nature Human Behaviour . 1 : 0021 . Google Scholar Crossref Search ADS Parker TH , Nakagawa S , Gurevitch J , IIEE (Improving Inference in Evolutionary Biology and Ecology) workshop participants . 2016 . Promoting transparency in evolutionary biology and ecology . Ecol Lett . 19 : 726 – 728 . 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 Wyatt TD . 2010 . Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates . J Comp Physiol A Neuroethol Sens Neural Behav Physiol . 196 : 685 – 700 . Google Scholar Crossref Search ADS PubMed Wyatt TD . 2014 . Pheromones and animal behavior: chemical signals and signatures . 2 nd ed. Cambridge : Cambridge University Press . © 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: journals.permissions@oup.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/open_access/funder_policies/chorus/standard_publication_model) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Queen pheromones, colony odors, and better science: a comment on Holman

Behavioral Ecology , Volume 29 (6) – Nov 27, 2018

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References (12)

Publisher
Oxford University Press
Copyright
© 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: journals.permissions@oup.com
ISSN
1045-2249
eISSN
1465-7279
DOI
10.1093/beheco/ary074
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Abstract

QUEEN PHEROMONES With the identification of a growing number of queen pheromones in ants, wasps, bees, and termites in recent years, Holman’s (2018) analysis offers a timely stocktake of our current understanding. This paper shows the usefulness of systematic meta-analysis compared with “vote counting” or entirely qualitative reviews. The focus on effect sizes allows the assessment of evidence for recently proposed hypotheses, such as, for example, the interesting experiments which suggest that queen pheromones in some ant species are not effective unless they are perceived alongside familiar colony odors (reviewed in Smith and Liebig 2017). Holman observes that the small sample sizes in the experiments do not allow firm conclusions to be drawn. It would repay repetition, if possible, with larger samples designed to take account of the likely effect sizes (for which Holman (2018) offers estimates). Queen pheromones can be identified because they are consistently carried by queens in different colonies (and have been demonstrated to have the effects on worker reproduction). Pheromones superimposed on a colony-odor background that varies between colonies are a feature of social insect pheromones (Wyatt 2010, 2014). The convergent evolution of queen pheromones in independently evolved eusocial lineages of ants, bees, and wasps is fascinating (see Holman 2018 for references) but the conservation of molecules as queen pheromones in many, but not all, taxa is not unprecedented. In the absence of selection, pheromones need not change. For example, in aphids, there is no selective advantage in species-specific alarm pheromones (if anything, cross-species response is an advantage) and so aphid species across more than 30 genera share the same molecule, (E)-β-farnesene, as their alarm pheromone. It is possible that queen pheromones in some species, currently single molecules, will turn out to be multicomponent, even perhaps with components from a variety of glands. The complexity and nonhydrocarbon nature of honeybee queen pheromones does not fit with the pattern of other hymenopteran queen pheromones but examples from around the animal kingdom show that the evolution of new pheromones occurs commonly, as demonstrated by the enormous variety of independently evolved male moth sex pheromones (see Wyatt 2014). A multitude of effects have been ascribed to queen pheromones. Blum noted that pheromone molecules often have multiple functions in social insects (“parsimony,” see Wyatt 2014). It will be interesting to see if the king and queen recognition pheromone in Reticulitermes termites, the hydrocarbon heneicosane, identified by behavioral responses of workers (Funaro et al. 2018), turns out to also have effects on worker reproduction. RANDOMIZED, BLIND, TRIALS AND THE QUEST FOR RELIABLE SCIENCE The response of biomedical and psychological researchers to the “reproducibility crisis” seems to be well ahead of those in ecology and evolution in recognizing potential sources of bias in designing, running, analyzing, and interpreting experiments, as well as proposing remedies (see e.g. the Catalogue of Bias www.catalogofbias.org). Munafò et al. (2017) present a manifesto for more reproducible behavioral science, starting with the design and conduct of experiments. Randomization and blinding are key requirements, as highlighted by Holman (2018), who observed that effect sizes were larger in queen pheromone experiments that were not run blind. Increasing scientific transparency is also important: pre-registration of experiments (to avoid p-Hacking for example) and incentives for open data sharing are starting to be encouraged in evolutionary biology and ecology too (Parker et al. 2016; Fidler et al. 2017). References Fidler F , Chee YE , Wintle BC , Burgman MA , McCarthy MA , Gordon A . 2017 . Metaresearch for evaluating reproducibility in ecology and evolution . Bioscience . 67 : 282 – 289 . Google Scholar PubMed Funaro CF , Boroczky K , Vargo EL , Schal C . 2018 . Identification of a queen and king recognition pheromone in the subterranean termite Reticulitermes flavipes . Proc Natl Acad Sci USA . 115 : 3888 – 3893 . Google Scholar Crossref Search ADS PubMed Holman L ( 2018 ) Queen pheromones and reproductive division of labour: a meta-analysis . Behav Ecol . 26 : 1199 – 1209 . Munafò MR , Nosek BA , Bishop DVM , Button KS , Chambers CD , Percie du Sert N , Simonsohn U , Wagenmakers E-J , Ware JJ , Ioannidis JPA . 2017 . A manifesto for reproducible science . Nature Human Behaviour . 1 : 0021 . Google Scholar Crossref Search ADS Parker TH , Nakagawa S , Gurevitch J , IIEE (Improving Inference in Evolutionary Biology and Ecology) workshop participants . 2016 . Promoting transparency in evolutionary biology and ecology . Ecol Lett . 19 : 726 – 728 . 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 Wyatt TD . 2010 . Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates . J Comp Physiol A Neuroethol Sens Neural Behav Physiol . 196 : 685 – 700 . Google Scholar Crossref Search ADS PubMed Wyatt TD . 2014 . Pheromones and animal behavior: chemical signals and signatures . 2 nd ed. Cambridge : Cambridge University Press . © 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: journals.permissions@oup.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/open_access/funder_policies/chorus/standard_publication_model)

Journal

Behavioral EcologyOxford University Press

Published: Nov 27, 2018

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