Queen pheromones out of context: a comment on Holman

Abstract

Holman's (2018) meta-analysis demonstrates that there is ample experimental evidence of fertility-correlated cuticular hydrocarbons (CHCs) affecting worker fecundity across social insects. We agree with this finding; however, in framing and discussing his results, he fails to properly consider biologically relevant behavioral data. Another concern we have is the way he represented our review on the topic and our experimental studies. Smith and Liebig (2017) developed a hypothesis for the evolution of CHCs as queen pheromones across insect societies that integrates the evolutionary transition from behavioral to purely pheromonal regulation of reproduction. We incorporated evidence for variation in how CHCs function in reproductive communication from cuelike signature mixtures, to fertility signals with context-learning, to innate queen pheromones. Holman positions his meta-analysis as a test of our work by giving the impression that our review exclusively favors "the theory that fertility-related CHCs only affect worker fecundity when presented in the correct context." This was only one of 3 ways which we theorized fertility-related CHC function.Holman (2018) states that our review "used 'vote counting' i.e. tallying studies that support, or did not support, a hypothesis." However, we clearly stated that our review was not comprehensive and had a "narrow focus" on "an outstanding problem involving seemingly conflicting experimental studies." We explicitly did the opposite of "counting" or "tallying" by singling out studies that presented conflicting data and building an inclusive view of this field that considered how CHCs have different functions across species and social organizations.After singling out one hypothesis from our review, Holman finds no evidence for it, reporting "the great majority of experiments that presented individual fertility-related CHCs recorded, strong, statistically significant effects on fecundity" and dismissing the "few published non-significant results" that did not show an inhibiting effect on ovarian development by isolated CHC compounds "as false negatives." Our review never advanced the idea that CHCs are interpreted as fertility signals in a singular way, testable by tallying a consensus result.To our surprise, Holman (2018) repeatedly dismisses behavioral evidence for context-specific recognition of fertility signals.He not only contradicts his own definition of queen pheromones as signals that "have a multitude of effects, including…eliciting submissive…responses," but also ignores fundamental concepts in social insect behavior with respect to the social regulation of reproduction. Our behavioral experiments (Smith et al. 2015 contains 4 behavioral experiments, not 1 as Holman writes) demonstrate that submissive behaviors were only triggered by fertilityrelated 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 submissio...