Octopamine drives honeybee thermogenesis
Curation statements for this article:-
Curated by eLife
Evaluation Summary:
This study is of broad interest to researchers in the field of entomology and physiology. These findings may shed light on at least one mechanism underlying selective advantages conferred to insect species on evolutionary timescales. Though the chemical signal, its source and recipient tissues underlying thermogenesis are elucidated, hypotheses regarding their downstream effects remain to be substantiated.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
- Neuroscience (eLife)
Abstract
In times of environmental change species have two options to survive: they either relocate to a new habitat or they adapt to the altered environment. Adaptation requires physiological plasticity and provides a selection benefit. In this regard, the Western honeybee ( Apis mellifera ) protrudes with its thermoregulatory capabilities, which enables a nearly worldwide distribution. Especially in the cold, shivering thermogenesis enables foraging as well as proper brood development and thus survival. In this study, we present octopamine signaling as a neurochemical prerequisite for honeybee thermogenesis: we were able to induce hypothermia by depleting octopamine in the flight muscles. Additionally, we could restore the ability to increase body temperature by administering octopamine. Thus, we conclude that octopamine signaling in the flight muscles is necessary for thermogenesis. Moreover, we show that these effects are mediated by β octopamine receptors. The significance of our results is highlighted by the fact the respective receptor genes underlie enormous selective pressure due to adaptation to cold climates. Finally, octopamine signaling in the service of thermogenesis might be a key strategy to survive in a changing environment.
Article activity feed
-
-
Evaluation Summary:
This study is of broad interest to researchers in the field of entomology and physiology. These findings may shed light on at least one mechanism underlying selective advantages conferred to insect species on evolutionary timescales. Though the chemical signal, its source and recipient tissues underlying thermogenesis are elucidated, hypotheses regarding their downstream effects remain to be substantiated.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
-
Reviewer #1 (Public Review):
The authors of this manuscript present data suggesting that octopamine signals from neurons arising in the mesometathoracic ganglion, through cognate receptors on flight muscles that they innervate, drive thermogenesis in honey bees. They employ temperature measurements on castes of honey bees where octopamine function is pharmacologically inhibited or stimulated in with the appropriate controls in addition to showing the presence of Octopamine and its receptors in relevant tissue. They make a connection of these manipulations to possible downstream metabolic events through measured alterations in flight muscle cAMP levels. In all, these findings are very interesting and noteworthy from the standpoint of physiology.
The data presented in this study suggest that Octopamine signals to flight muscles contribute …
Reviewer #1 (Public Review):
The authors of this manuscript present data suggesting that octopamine signals from neurons arising in the mesometathoracic ganglion, through cognate receptors on flight muscles that they innervate, drive thermogenesis in honey bees. They employ temperature measurements on castes of honey bees where octopamine function is pharmacologically inhibited or stimulated in with the appropriate controls in addition to showing the presence of Octopamine and its receptors in relevant tissue. They make a connection of these manipulations to possible downstream metabolic events through measured alterations in flight muscle cAMP levels. In all, these findings are very interesting and noteworthy from the standpoint of physiology.
The data presented in this study suggest that Octopamine signals to flight muscles contribute to thermogenesis. The downstream metabolic pathways that might underly this correlation is a "hypothetical cascade" albeit with support from studies in other species of insects. Results from testing these biochemical hypotheses may greatly substantiate this study.
-
Reviewer #2 (Public Review):
The authors have tested the hypothesis that the biogenic amine octopamine is of major importance for shivering thermogenesis in bees. This hypothesis is based on previous studies in which octopamine was correlated on the one hand with the control of muscle activity in insects and on the other hand with the known functions of noradrenaline in the context of thermogenesis in mammals. They could show that octopamine is indeed found in the relevant flight muscles responsible for shivering thermogenesis and that the amount of this hormone increases with age. Anatomical studies could directly show that octopaminergic neurons indeed innervate these muscle groups. With the help of pharmacological studies, they finally succeeded in demonstrating the importance of octopamine and selected octopamine receptors for …
Reviewer #2 (Public Review):
The authors have tested the hypothesis that the biogenic amine octopamine is of major importance for shivering thermogenesis in bees. This hypothesis is based on previous studies in which octopamine was correlated on the one hand with the control of muscle activity in insects and on the other hand with the known functions of noradrenaline in the context of thermogenesis in mammals. They could show that octopamine is indeed found in the relevant flight muscles responsible for shivering thermogenesis and that the amount of this hormone increases with age. Anatomical studies could directly show that octopaminergic neurons indeed innervate these muscle groups. With the help of pharmacological studies, they finally succeeded in demonstrating the importance of octopamine and selected octopamine receptors for thermogenesis.
I consider the investigations of Kaya-Zeeb and colleagues to be very interesting and relevant in principle, as they were able to elucidate an essential aspect of bee life in this way. In most aspects, the manuscript is well written and the experiments are comprehensible. The experiments are mostly adequately and competently performed.
-
