Identification of a queen and king recognition pheromone in the subterranean termite
            <i>Reticulitermes flavipes</i>

Funaro, Colin F.; Böröczky, Katalin; Vargo, Edward L.; Schal, Coby

doi:10.1073/pnas.1721419115

Cited by 74 publications

(85 citation statements)

References 39 publications

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“…However, these results do not reject the hypothesis that brood pheromones affect sleep. It is possible that some active components were not effectively extracted by the protocol we used, that these components lost their potency, or that the pheromonal effect depends on the presence of other chemicals (Funaro et al 2018). This premise is supported by the finding that the pupal extracts retained only a partial effect on the propensity to build wax pots.…”

Section: Discussionmentioning

confidence: 83%

Signals from the brood modulate the sleep of brood tending bumblebee workers

Nagari

Jönsson

et al. 2018

Preprint

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Sleep is ubiquitous in vertebrates and invertebrates, and its chronic lost is typically associated with reduced performance, health, or survival. Nevertheless, some animals can give up sleep in order to increase survival or mating opportunities. We studied the interplay between sleep and brood care in the social bumblebee Bombus terrestris. We first used video recording and detailed behavioral analyses to confirm that the bumblebee shows the essential behavioral characteristics of sleep. Based on these analyses we next used immobility bouts of >5' as proxy for sleep in automatic activity monitoring records, and found that sleep is severely reduced in the presence of larvae that require feeding or pupae that are not fed. Reduced sleep was correlated with wax pot building, which is a behavior typical to nest founding mother queens. Sleep was also reduced in the presence of empty cocoons, but this effect was transient and reduced with time. This observation that is consistent with the presence of a sleep modulating pheromonal signal. These results provide the first evidence for brood modulation of sleep in an insect, and are consistent with the hypothesis that plasticity in sleep can evolve as a mechanism to improve care for dependent juveniles.

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Section: Discussionmentioning

confidence: 83%

Signals from the brood modulate the sleep of brood tending bumblebee workers

Nagari

Jönsson

et al. 2018

Preprint

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“…If sexual conflict between males and females over their respective investment in parental care is absent in these species, we expected queens and kings to express a similar level of grooming, antennation, and trophallaxis toward their offspring. Note that body-shaking is a behavior that has been frequently reported in termites, but for which the role is still unclear (Funaro, Böröczky, Vargo, & Schal, 2018;Whitman & Forschler, 2007). Our study will thus also provide novel insights into our understanding of its expression and function during colony foundation.…”

mentioning

confidence: 71%

“…Although body-shaking has been described as a response to disturbance in a large number of termites (Bagnères & Hanus, 2015;Howse, 1965), the modality of its expression remained unclear (Funaro et al, 2018) and was not previously studied in incipient colonies (Rosengaus & Traniello, 1991;Shellman-Reeve, 1990). …”

Section: Discussionmentioning

confidence: 99%

“…Because we aimed at taking a broader perspective and exploring whether this biparental organization was species specific, we used two species of subterranean termites: the invasive Reticulitermes flavipes (Kollar, 1837) and the native R. grassei (Clément, 1978). Note that body-shaking is a behavior that has been frequently reported in termites, but for which the role is still unclear (Funaro, Böröczky, Vargo, & Schal, 2018;Whitman & Forschler, 2007). Note that body-shaking is a behavior that has been frequently reported in termites, but for which the role is still unclear (Funaro, Böröczky, Vargo, & Schal, 2018;Whitman & Forschler, 2007).…”

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confidence: 99%

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Unbalanced biparental care during colony foundation in two subterranean termites

Brossette

Meunier

Dupont

et al. 2018

Ecology and Evolution

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Parental care is a major component of reproduction in social organisms, particularly during the foundation steps. Because investment into parental care is often costly, each parent is predicted to maximize its fitness by providing less care than its partner. However, this sexual conflict is expected to be low in species with lifelong monogamy, because the fitness of each parent is typically tied to the other's input. Somewhat surprisingly, the outcomes of this tug‐of‐war between maternal and paternal investments have received important attention in vertebrate species, but remain less known in invertebrates. In this study, we investigated how queens and kings share their investment into parental care and other social interactions during colony foundation in two termites with lifelong monogamy: the invasive species Reticulitermes flavipes and the native species R. grassei. Behaviors of royal pairs were recorded during six months using a non‐invasive approach. Our results showed that queens and kings exhibit unbalanced investment in terms of grooming, antennation, trophallaxis, and vibration behavior. Moreover, both parents show behavioral differences toward their partner or their descendants. Our results also revealed differences among species, with R. flavipes exhibiting shorter periods of grooming and antennation toward eggs or partners. They also did more stomodeal trophallaxis and less vibration behavior. Overall, this study emphasizes that despite lifelong monogamy, the two parents are not equally involved in the measured forms of parental care and suggests that kings might be specialized in other tasks. It also indicates that males could play a central, yet poorly studied role in the evolution and maintenance of the eusocial organization.

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“…We are happy to see additional behavioral data emerging, such as a recent study in termites supporting the idea that perception of fertility signaling CHCs can be dependent on chemical context (Funaro et al 2018).…”

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confidence: 82%

Queen pheromones out of context: a comment on Holman

2018

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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...

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Identification of a queen and king recognition pheromone in the subterranean termite Reticulitermes flavipes

Cited by 74 publications

References 39 publications

Signals from the brood modulate the sleep of brood tending bumblebee workers

Signals from the brood modulate the sleep of brood tending bumblebee workers

Unbalanced biparental care during colony foundation in two subterranean termites

Queen pheromones out of context: a comment on Holman

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