Queen pheromones out of context: a comment on Holman

Queen pheromones out of context: a comment on Holman Downloaded from https://academic.oup.com/beheco/article-abstract/29/6/1212/4994258 by Ed 'DeepDyve' Gillespie user on 15 January 2019 1212 Behavioral Ecology Smith AA, Liebig J. 2017. The evolution of cuticular fertility signals in as signals that “have a multitude of effects, including…eliciting eusocial insects. Curr Opin Insect Sci. 22:79–84. submissive…responses,” but also ignores fundamental concepts Wyatt TD. 2010. Pheromones and signature mixtures: defining species-wide in social insect behavior with respect to the social regulation of signals and variable cues for identity in both invertebrates and vertebrates. reproduction. Our behavioral experiments (Smith et  al. 2015 J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 196:685–700. Wyatt TD. 2014. Pheromones and animal behavior: chemical signals and contains 4 behavioral experiments, not 1 as Holman writes) dem- signatures. 2nd ed. Cambridge: Cambridge University Press. onstrate that submissive behaviors were only triggered by fertility- related CHCs in a relevant CHC context. Holman considers this as “no direct evidence for context-dependent responses” because “submissive behaviour might not translate into differences in fecundity.” The concept that submission is a ritualized response to dominance and is generally associated with reduced fecundity in social insect hierarchies is well established (e.g. Bourke 1988; Queen pheromones out of context: a Drews 1993). As further justification of the dismissal of these comment on Holman experiments, Holman claims that “the experiment was not per- a b c formed blind” even though the methods state that all behavioral Adrian A. Smith, Andrew V. Suarez, and Jürgen Liebig a data in Smith et  al. (2015) were collected from blind analysis of Research & Collections, North Carolina Museum of Natural video recordings. Sciences; Department of Biological Sciences, North Carolina Holman (2018) also focuses on the sample size (n = 13) of Smith State University, 11 West Jones Street, Raleigh, NC 27606, USA, b et  al.’s (2015) fifth experiment, a null result that an isolated fertil - Department of Animal Biology and Department of Entomology, ity signaling compound has no primer-effect of inhibiting worker University of Illinois at Urbana-Champaign, 505 South Goodwin c reproduction. This experiment compares group-level responses to Avenue, Urbana, IL 61801, USA, and School of Life Sciences, controls and treatments. Unfortunately, Holman conflates group- Arizona State University, 427 East Tyler Mall, Tempe, AZ 85287, USA level responses (presence of eggs in a colony) with individual-level responses (ovarian status) within groups by treating sample sizes Holman’s (2018) meta-analysis demonstrates that there is ample as equivocal. He concludes that a suitable sample size for this experimental evidence of fertility-correlated cuticular hydrocarbons experiment would have been about 130 for each treatment group. (CHCs) affecting worker fecundity across social insects. We agree However, group-level responses are often an average of individual with this finding; however, in framing and discussing his results, responses, especially for an egg-laying. For example, Smith et  al. he fails to properly consider biologically relevant behavioral data. (2015) measured 13 paired groups which consisted, on average, of Another concern we have is the way he represented our review on 21 workers. Thus, this experiment tested an average of 273 work- the topic and our experimental studies. ers per treatment. Furthermore, individual-level measures assume Smith and Liebig (2017) developed a hypothesis for the evolution that a significant proportion of workers will develop their ovaries in of CHCs as queen pheromones across insect societies that integrates response to the absence of a queen. This is not true for species in the evolutionary transition from behavioral to purely pheromonal which egg-laying is taken over by one or a few individuals. regulation of reproduction. We incorporated evidence for variation Finally, we agree with Holman (2018) that more work is needed in how CHCs function in reproductive communication from cue- on this topic. We are happy to see additional behavioral data like signature mixtures, to fertility signals with context-learning, to emerging, such as a recent study in termites supporting the idea innate queen pheromones. Holman positions his meta-analysis as a that perception of fertility signaling CHCs can be dependent on test of our work by giving the impression that our review exclusively chemical context (Funaro et al. 2018). favors “the theory that fertility-related CHCs only affect worker fecundity when presented in the correct context.” This was only one Address correspondence to A.A. Smith. E-mail: Adrian.Smith@ of 3 ways which we theorized fertility-related CHC function. naturalsciences.org. Holman (2018) states that our review “used ‘vote counting’ i.e. tallying studies that support, or did not support, a hypothesis.” Received 5 April 2018; editorial decision 10 April 2018; accepted 14 April However, we clearly stated that our review was not comprehensive 2018; Advance Access publication 9 May 2018 and had a “narrow focus” on “an outstanding problem involving doi:10.1093/beheco/ary065 seemingly conflicting experimental studies.” We explicitly did the opposite of “counting” or “tallying” by singling out studies that Editor-in-Chief: Leigh Simmons presented conflicting data and building an inclusive view of this field that considered how CHCs have different functions across spe - REFERENCES cies and social organizations. Bourke AFG. 1988. Dominance orders, worker reproduction, and queen- After singling out one hypothesis from our review, Holman finds no worker conflict in the slave-making ant Harpagoxenus sublaevis. Behav Ecol evidence for it, reporting “the great majority of experiments that pre- Sociobiol. 23:323–333. sented individual fertility-related CHCs recorded, strong, statistically Drews C. 1993. The concept and definition of dominance in animal behav - iour. Behaviour. 125:283–313. significant effects on fecundity” and dismissing the “few published Funaro CF, Böröczky K, Vargo EL, Schal C. 2018. Identification of a queen non-significant results” that did not show an inhibiting effect on ovar - and king recognition pheromone in the subterranean termite Reticulitermes ian development by isolated CHC compounds “as false negatives.” flavipes . Proc Natl Acad Sci USA. 115:3888–3893. Our review never advanced the idea that CHCs are interpreted as Holman L. 2018. Queen pheromones and reproductive division of labour: a meta-analysis. Behav Ecol. 26:1199–1209. fertility signals in a singular way, testable by tallying a consensus result. Smith AA, Liebig J. 2017. The evolution of cuticular fertility signals in To our surprise, Holman (2018) repeatedly dismisses behav- eusocial insects. Curr Opin Insect Sci. 22:79–84. ioral evidence for context-specific recognition of fertility signals. Smith AA, Millar JG, Suarez AV. 2015. A social insect fertility signal is He not only contradicts his own definition of queen pheromones dependent on chemical context. Biol Lett. 11:20140947. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Queen pheromones out of context: a comment on Holman

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Abstract

Downloaded from https://academic.oup.com/beheco/article-abstract/29/6/1212/4994258 by Ed 'DeepDyve' Gillespie user on 15 January 2019 1212 Behavioral Ecology Smith AA, Liebig J. 2017. The evolution of cuticular fertility signals in as signals that “have a multitude of effects, including…eliciting eusocial insects. Curr Opin Insect Sci. 22:79–84. submissive…responses,” but also ignores fundamental concepts Wyatt TD. 2010. Pheromones and signature mixtures: defining species-wide in social insect behavior with respect to the social regulation of signals and variable cues for identity in both invertebrates and vertebrates. reproduction. Our behavioral experiments (Smith et  al. 2015 J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 196:685–700. Wyatt TD. 2014. Pheromones and animal behavior: chemical signals and contains 4 behavioral experiments, not 1 as Holman writes) dem- signatures. 2nd ed. Cambridge: Cambridge University Press. onstrate that submissive behaviors were only triggered by fertility- related CHCs in a relevant CHC context. Holman considers this as “no direct evidence for context-dependent responses” because “submissive behaviour might not translate into differences in fecundity.” The concept that submission is a ritualized response to dominance and is generally associated with reduced fecundity in social insect hierarchies is well established (e.g. Bourke 1988; Queen pheromones out of context: a Drews 1993). As further justification of the dismissal of these comment on Holman experiments, Holman claims that “the experiment was not per- a b c formed blind” even though the methods state that all behavioral Adrian A. Smith, Andrew V. Suarez, and Jürgen Liebig a data in Smith et  al. (2015) were collected from blind analysis of Research & Collections, North Carolina Museum of Natural video recordings. Sciences; Department of Biological Sciences, North Carolina Holman (2018) also focuses on the sample size (n = 13) of Smith State University, 11 West Jones Street, Raleigh, NC 27606, USA, b et  al.’s (2015) fifth experiment, a null result that an isolated fertil - Department of Animal Biology and Department of Entomology, ity signaling compound has no primer-effect of inhibiting worker University of Illinois at Urbana-Champaign, 505 South Goodwin c reproduction. This experiment compares group-level responses to Avenue, Urbana, IL 61801, USA, and School of Life Sciences, controls and treatments. Unfortunately, Holman conflates group- Arizona State University, 427 East Tyler Mall, Tempe, AZ 85287, USA level responses (presence of eggs in a colony) with individual-level responses (ovarian status) within groups by treating sample sizes Holman’s (2018) meta-analysis demonstrates that there is ample as equivocal. He concludes that a suitable sample size for this experimental evidence of fertility-correlated cuticular hydrocarbons experiment would have been about 130 for each treatment group. (CHCs) affecting worker fecundity across social insects. We agree However, group-level responses are often an average of individual with this finding; however, in framing and discussing his results, responses, especially for an egg-laying. For example, Smith et  al. he fails to properly consider biologically relevant behavioral data. (2015) measured 13 paired groups which consisted, on average, of Another concern we have is the way he represented our review on 21 workers. Thus, this experiment tested an average of 273 work- the topic and our experimental studies. ers per treatment. Furthermore, individual-level measures assume Smith and Liebig (2017) developed a hypothesis for the evolution that a significant proportion of workers will develop their ovaries in of CHCs as queen pheromones across insect societies that integrates response to the absence of a queen. This is not true for species in the evolutionary transition from behavioral to purely pheromonal which egg-laying is taken over by one or a few individuals. regulation of reproduction. We incorporated evidence for variation Finally, we agree with Holman (2018) that more work is needed in how CHCs function in reproductive communication from cue- on this topic. We are happy to see additional behavioral data like signature mixtures, to fertility signals with context-learning, to emerging, such as a recent study in termites supporting the idea innate queen pheromones. Holman positions his meta-analysis as a that perception of fertility signaling CHCs can be dependent on test of our work by giving the impression that our review exclusively chemical context (Funaro et al. 2018). favors “the theory that fertility-related CHCs only affect worker fecundity when presented in the correct context.” This was only one Address correspondence to A.A. Smith. E-mail: Adrian.Smith@ of 3 ways which we theorized fertility-related CHC function. naturalsciences.org. Holman (2018) states that our review “used ‘vote counting’ i.e. tallying studies that support, or did not support, a hypothesis.” Received 5 April 2018; editorial decision 10 April 2018; accepted 14 April However, we clearly stated that our review was not comprehensive 2018; Advance Access publication 9 May 2018 and had a “narrow focus” on “an outstanding problem involving doi:10.1093/beheco/ary065 seemingly conflicting experimental studies.” We explicitly did the opposite of “counting” or “tallying” by singling out studies that Editor-in-Chief: Leigh Simmons presented conflicting data and building an inclusive view of this field that considered how CHCs have different functions across spe - REFERENCES cies and social organizations. Bourke AFG. 1988. Dominance orders, worker reproduction, and queen- After singling out one hypothesis from our review, Holman finds no worker conflict in the slave-making ant Harpagoxenus sublaevis. Behav Ecol evidence for it, reporting “the great majority of experiments that pre- Sociobiol. 23:323–333. sented individual fertility-related CHCs recorded, strong, statistically Drews C. 1993. The concept and definition of dominance in animal behav - iour. Behaviour. 125:283–313. significant effects on fecundity” and dismissing the “few published Funaro CF, Böröczky K, Vargo EL, Schal C. 2018. Identification of a queen non-significant results” that did not show an inhibiting effect on ovar - and king recognition pheromone in the subterranean termite Reticulitermes ian development by isolated CHC compounds “as false negatives.” flavipes . Proc Natl Acad Sci USA. 115:3888–3893. Our review never advanced the idea that CHCs are interpreted as Holman L. 2018. Queen pheromones and reproductive division of labour: a meta-analysis. Behav Ecol. 26:1199–1209. fertility signals in a singular way, testable by tallying a consensus result. Smith AA, Liebig J. 2017. The evolution of cuticular fertility signals in To our surprise, Holman (2018) repeatedly dismisses behav- eusocial insects. Curr Opin Insect Sci. 22:79–84. ioral evidence for context-specific recognition of fertility signals. Smith AA, Millar JG, Suarez AV. 2015. A social insect fertility signal is He not only contradicts his own definition of queen pheromones dependent on chemical context. Biol Lett. 11:20140947.

Journal

Behavioral EcologyOxford University Press

Published: Nov 27, 2018

References

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